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Bryophytes play important roles in many ecosystems, especially in rain forests and cold biomes (Longton, 1997; Tan & Pocs, 2000), where they are abundant and in close contact with vascular plants. Interactions between bryophytes and vascular plants comprise a large spectrum of relations, including resource competition (Chapin et al., 1987), as well as suppression and facilitation, mostly attributed to the altered microclimatic conditions for vascular plants within bryophyte patches (van Tooren & During, 1990; J. L. Gornall et al. unpublished data). Although these interactions have been shown to be species specific for vascular plants (Sohlberg & Bliss, 1984; van Tooren & During, 1990), virtually nothing is known about the importance of interspecific differences between bryophytes with respect to their effects on vascular plants (but see Ohlson & Zackrisson, 1992), or about the functional traits of bryophyte species that are responsible for such effects (Cornelissen et al., 2007).
Bryophyte mats have been shown to greatly affect vascular plant seedling emergence (Sthilaire & Leopold, 1995; Sedia & Ehrenfeld, 2003; Dostal, 2007) and survival (Zamfir et al., 1999; Sedia & Ehrenfeld, 2003; Otsus & Zobel, 2004; Spackova & Leps, 2004; Morgan, 2006; Dostal, 2007; Donath & Eckstein, 2010). Usually the effect is negative, as a result of allelopathic effects on germination (Steijlen et al., 1995; Zamfir, 2000), reduced moisture availability (Equihua & Usher, 1993) or the creation of a physical barrier that prevents seeds from reaching the soil (McIlvanie, 1942; Morgan, 2006), thereby increasing the likelihood of desiccation, predation, a chemically unfavourable environment or destruction by fire. Furthermore, bryophyte mats reduce light intensity and the red : far red ratio below the cushions, which may suppress germination (Haeussler & Tappeiner, 1993). Among these effects, allelopathy seems to be the most controversial. Steijlen et al. (1995) suggested that it only affects germination, but not subsequent seedling survival, whereas Equihua & Usher (1993) found no allelopathic effects of bryophytes at all. Positive effects of bryophytes on seedling emergence and survival (Bell & Bliss, 1980; Sohlberg & Bliss, 1984) have been reported mostly from harsh environments, where facilitation prevails over competition (Bertness & Callaway, 1994; Callaway & Walker, 1997). Facilitation has been attributed to improved moisture conditions, higher soil temperature, reduced wind speed and a seed trap effect (Bell & Bliss, 1980; Sohlberg & Bliss, 1984; van Tooren & During, 1990; Groeneveld et al., 2007; Jeschke & Kiehl, 2008).
Experimental manipulations, climatic gradient studies and microfossil analyses suggest that climate change will strongly affect the abundance and species’ composition of bryophytes in many plant communities (Potter et al., 1995; Molau & Alatalo, 1998; Weltzin et al., 2000, 2001; Dorrepaal et al., 2004; Bauer et al., 2009; Lang et al., 2009). Changes in bryophyte community composition will, in turn, affect species-specific interactions between vascular plants and bryophytes, including reproduction, the most crucial aspect of community composition. Vascular plant seedlings are more sensitive to bryophyte influence, positive as well as negative, than the established vascular vegetation (Spackova et al., 1998), because of their great dependence on microsite conditions (Eriksson & Ehrlen, 1992; Steijlen et al., 1995).
Sparse data suggest that distinct bryophyte species may have distinct effects on seedling germination and survival (Cross, 1981; Zamfir, 2000; Serpe et al., 2006), attributed to differences in mat thickness (Zamfir, 2000). However, as yet, little is known about the generality of interspecific differences between bryophytes in this respect, or about the mechanisms underpinning these differences.
The aims of this study were to assess the differences between bryophyte species with regard to their effects on vascular plant generative recruitment, including germination and first-year seedling establishment, and to unveil the mechanisms underlying these effects. We tested the following suppositions:
Bryophyte effects on the recruitment of vascular plants are species specific for bryophytes (i.e. there is a significant difference between bryophytes) as well as for vascular plants (i.e. there is an interaction effect between vascular plants and bryophyte species, indicating that the effects of bryophytes differ according to the vascular plant species).
The mechanisms underpinning the effects of bryophytes on vascular plant recruitment include phenolic leakages that inhibit germination, mechanical obstruction that prevents seeds from reaching the soil and alters the light regime, alteration of the soil microclimate (moisture and temperature regimes) and retarded seedling growth in thicker and denser cushions with reduced light availability. With respect to this research question, we aimed to find easy-to-measure bryophyte traits (Cornelissen et al., 2007
) that could be used as proxies for these factors.
Previous studies on the effects of bryophyte mats on vascular plant recruitment have featured experimental removal of the bryophyte mat (but seeZamfir, 2000) or the sowing of seeds in bryophyte mats at their natural habitats (Ohlson & Zackrisson, 1992; Hanssen, 2002). However, neither of these methods targets the effects of bryophytes per se, because the former method causes considerable soil disturbance, affecting germination by itself via an enhanced mineralization rate, and the latter does not allow the separation of the effects of bryophytes from the effects of microhabitat. By contrast, our experimental bryophyte cushion transplantations ensured identical soils in different control and bryophyte treatments, allowing the explicit examination of bryophyte (species’) effects.
We ran this study in a subarctic forest where bryophytes co-dominate the understory vegetation and therefore greatly determine the abiotic and biotic conditions for co-occurring species (Longton, 1988; Grime, 1998). Although many vascular plant species in polar regions possess vegetative reproduction, reproduction by seeds here is an extremely important process enabling longer term genetic flexibility of plant populations and long-distance dispersal (Welling & Laine, 2002; Alsos et al., 2007). The climate is harsh here and seedling recruitment success is mediated by soil temperature (Milbau et al., 2009; Shevtsova et al., 2009) and moisture regimes (Bell & Bliss, 1980; Sohlberg & Bliss, 1984), allowing us to properly test for the importance of bryophyte-driven modifications of soil microclimate vs effects of mechanical obstruction and allelopathic suppression, the latter being unraveled through a complementary controlled laboratory experiment.
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This study is the first assessment of interaction mechanisms between vascular plant seedlings and bryophyte species. All bryophytes in our study strongly suppressed the regeneration of vascular plants. This may be explained by the enormous proportion of seeds intercepted by bryophyte cushions (see Methods S3 for details). However, between bryophyte species, the difference in the number of established seedlings could not be attributed to mechanical obstruction, but rather to altered soil temperature regime. Clear differences between bryophyte species in terms of suppressive effects on seedlings strongly imply that the climatically and anthropogenically driven transformations in the structure and composition of bryophyte communities (Molau & Alatalo, 1998; Nygaard & Odegaard, 1999; Makipaa & Heikkinen, 2003; Lang et al., 2009) will affect the generative reproduction of vascular plants.
Interestingly, the suppressive effect of a bryophyte species on seedling performance coincided with its association with the forest understory, as reported in several subarctic vegetation surveys (Schoweld, 1992; Frego, 1996; Makipaa & Heikkinen, 2003; Locky et al., 2005). The most widespread bryophytes of boreal and subartic forests, Hylocomium splendens and Pleurozium schreberi, were among the strongest suppressors of vascular plant seedlings. Dicranum scoparium had an intermediate position and liverworts, rather scarce in subarctic forests, formed the best sites for vascular plant regeneration in the field. This suggests that effective suppression of vascular plant seedlings is an important mechanism to maintain dominance in the forest understory, although Polytrichum strictum, which is less widespread than Hylocomium and Pleurozium, had a similar suppressive effect on vascular plant seedlings in our study. However, in contrast with other bryophytes investigated in this study, Polytrichum is a typical early successional species in subarctic forest (Benscoter, 2006; Benscoter & Vitt, 2008) and this might explain its lower abundance in the established forest.
To our surprise, we did not find interaction effects between bryophyte species and vascular plant species, suggesting that vascular plants do not possess species-specific adaptation mechanisms for recruitment in bryophyte cushions. This partly contradicts the results of Ohlson & Zackrisson (1992), who detected species-specific preferences of coniferous trees for habitats dominated by Sphagna vs Pleurozium. However, in that study, seeds were sown into existing bryophyte mats, and therefore it was not possible to distinguish between the effects of bryophytes per se and the effects of habitat, such as macro-light conditions, soil quality and moisture availability.
We found a striking contrast between the results of laboratory and field experiments with respect to allelopathic effects of bryophytes. In the laboratory experiment, bryophyte phenolics negatively affected germination and, even more strongly, the early development of seedlings, as in some previous laboratory studies (Tsubota et al., 2006; Kato-Noguchi et al., 2010). By contrast, the field experiment revealed no difference in the amount of phenolics between bryophytes. In addition, seedling performance was not related to phenolics measured in the field. Consistently smaller amounts of phenolics in charcoal-treated soils indicated, however, that there was no error in the experimental treatments or measurements. Phenolic degradation and the composition of the microorganism community responsible for this process are strongly affected by plant inputs (Brant et al., 2006). We speculate that, in our case, because of the difference in phenolic compound composition and the possible presence of other bryophyte leachates, the bryophyte-derived phenolics underwent distinct degradation, resulting in similar soil phenolic concentrations associated with different bryophytes. The striking difference between the results of the laboratory and field experiments highlights the danger of drawing conclusions about complex ecological processes based on laboratory experiments only, without field verification (Mokany & Ash, 2008; Soudzilovskaia et al., 2010).
Contrary to our expectations, bryophyte species did not vary greatly in their effect on soil moisture or associated effects on seedling establishment success. Moreover, the soil under some bryophytes was drier than the bare soil on control plots. This is probably a result of the generally low (300 mm yr−1) level of precipitation in the Abisko area (Malmer & Nilgård, 1980), which often falls as drizzle and may be absorbed by bryophytes without reaching the soil. The absence of bryophyte-mediated moisture effects on vascular plant seedlings could be attributed to the lower sensitivity of seedlings to differences in moisture than to differences in temperature (Burton & Bazzaz, 1991), in combination with the relatively small differences in moisture found.
Our data suggest that competition between bryophytes and vascular plant seedlings is mediated by the soil temperature regime under bryophyte mats. Our experimental set-up did not allow the unambiguous disentanglement of the importance of individual aspects of temperature regime. However, we detected a strong negative correlation between diurnal temperature fluctuations during the time of germination and the number of established seedlings. Similarly, Sthilaire & Leopold (1995) found better germination in mats of Hypnum imponens than in Hylocomium splendens and Sphagnum girgensohnii in the field, but not in the glasshouse at constant temperature. As Thompson et al. (1977) demonstrated the crucial importance of temperature fluctuations for breaking seed dormancy, we suggest that this mechanism is key to the suppression of vascular plant establishment in bryophyte mats in the subarctic, where understory vegetation is dominated by various bryophytes with distinct heat conductance. Thompson et al. (1977) reported that fluctuation ranges of 1–8°C were needed to break dormancy in light and 4–12°C in dark conditions. Our results are consistent with this temperature range.
Gornall et al. (2007, 2009) and Van der Wal & Brooker (2004) reported a reduction in soil temperature associated with bryophyte mat presence and thickness in high-arctic tundra (Van der Wal & Brooker, 2004). We also expected bryophytes to decrease the temperature during the growing season and thereby suppress the germination and seedling establishment of vascular plants. However, although soil temperature was lower under bryophytes at the beginning of the growing season, at the end it was higher, and the average soil temperature over the whole growing season did not differ between mats of different bryophyte species or from the control. As we harvested the experiment in September, our experimental set-up did not allow appropriate testing for the effects of the temperature regime at the end of the growing season on 1-yr-old seedlings. Jeschke & Kiehl (2008) reported that, in grasslands of Bavaria (Germany), removal of the moss layer improved the germination of vascular plants, but ultimate seedling survival was higher in moss mats, because the seedlings were better protected against frost. However, we do not expect this effect to be strong with respect to seedling survival in different bryophyte mats, because, in our as well as other experiments (Gornall et al., 2007), the strongest difference between bryophytes with distinct canopy height was in the amplitude of temperature and not absolute temperature, and there is evidence (Prock & Körner, 1996) that the early season is the most critical period for the development of cold climate plants; late-season growth is generally much less important because, by that time, sufficient biomass has been produced to ensure successful winter survival.
We did not detect a correlation between the effects of moisture and temperature regimes on seedling establishment. Similarly, Van der Wal & Brooker (2004) reported, for high-arctic tundra, that the ‘moss layer acts as an insulating blanket irrespective of soil moisture’, after detecting a marginally significant impact of moisture on soil temperature, with only a < 1°C drop in temperature over the range of soil moisture contents from 10% to 60%. Considering that, in our study, the moisture range was much smaller (Fig. S3), the absence of correlation with temperature is not surprising. It is important to realize, however, that our study does not necessarily represent all relevant aspects of subarctic soil moisture and temperature regimes, but only those showing a clear relation to seedling establishment.
The absence of a bryophyte effect on the mass of individual vascular plant seedlings suggests that bryophytes exclusively affect germination and very early seedling establishment, but do not influence the fitness of established seedlings. This is supported by the responses to changes in temperature regime under bryophyte cushions: the strongest differences between bryophyte treatments were related to spring temperature fluctuations, which are known to affect germination, whereas differences related to the length of vegetation season were not significant. However, it is necessary to keep in mind that the commercial potting soil underneath the bryophytes probably created a favorable nutrient supply to the seedlings. Thus, the fitness of seedlings in control plots and bryophyte cushions in the species’ natural habitats may vary more strongly owing to larger differences in soil nutrition regime.
Our study has clearly demonstrated the importance of bryophyte species for vascular plant generative reproduction, and thereby community composition. However, we did not find evidence of vascular plant species-specific adaptations for recruitment in bryophyte cushions. In the subarctic, bryophytes affect mostly germination and very early seedling survival, but not the fitness of established seedlings. The difference between bryophyte species with respect to vascular plant seedling establishment success in bryophyte mats is best explained by the altered soil temperature regime, specifically by the reduction in temperature fluctuations during germination time.
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Fig. S1 Soil phenolic content under mats of distinct subarctic bryophyte species.
Fig. S2 Performance of individual vascular plant species in subarctic bryophyte mats.
Fig. S3 Volumetric soil moisture content measured over the summer months under subarctic bryophyte cushions.
Table S1 Results of the regression analyses of the dependences between individual proxies for soil temperature regime under bryophytes, vascular plant seedling establishment and bryophyte cushion thickness
Table S2 Mean values and errors for bryophyte cushion thickness, density and mechanical obstruction
Methods S1 Control for the external seed influx.
Methods S2 The use of the mixed-model regression technique.
Methods S3 Measurement of mechanical obstruction created by bryophyte cushions.
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