The results indicate that habitat temperature decreased but water availability increased with increasing altitude. During the observation period, the mean air temperature increased by 5.9oC, the dew point increased by 3.6oC, relative humidity decreased by 10%, and rainfall decreased by 84 mm in the lowland area compared with the high elevation. Under rapid and persistent global warming and a likely declining trend of relative humidity and rainfall (Hijmans et al. 2005; Ramirez and Jarvis 2008), the relocation of terrestrial mosses from high to low elevations can be used to estimate the impacts of future global climate change in the study area.
The most marked result of this study is that only a few moss species survived six months after transplanting to the warmer and drier lowlands, and even in these species the health status deteriorated severely (Figs. 2 and 4). We did not detect a positive growth rate after June at lower elevations, so survival might be pro-acclimated to warmer and drier lowlands. The simulated climate change significantly negatively affected the growth and health of most moss species studied in the six-month period (Figs. 2–5). Similar results were obtained in our laboratory study: as the temperature increases, the health status, photosynthetic activities, and biomass gains decline sharply (JW. Hao, unpubl. data). Song et al. (2014) also observed markedly declined growth rates and a negative effect on the health of transplanted epiphytes within two years. In addition, Wagner et al. (2014b) found that no short-term acclimation existed, and that a temperature increase led to poorer health and eventually high mortality of transplanted bryophytes. The relative abundance of species in the field changed significantly with a 1.5–2.5 oC temperature increase over two years (Jácome et al. 2011).
These results can be explained in two ways. First, high respiratory carbon losses and a shorter period of photosynthetic activities induced by increased temperature contributed to the decline of growth gains (Proctor 2011; Wagner et al. 2013). Second, mosses are poikilohydric, rapidly losing water and thus photosynthetic capacity when the relative humidity decreases, with photosynthetic capacity resuming only if they are rehydrated (Sillett and Antoine 2004). Wagner et al. (2013) suggested that the timing and duration of wetting rather than the water content were the main drivers in this respect, and temperature-dependent metabolism is limited with increasing evaporation rates, restricting the period for net photosynthesis. This situation was exacerbated by wet and warm nights. Consequently, the mosses were incapable of the high photosynthetic rates needed to counteract the respiratory carbon losses in warmer and drier lowland areas.
Another striking result was that net growth rates were found only in the first observation period irrespective of whether mosses were transplanted to lower elevations. We cannot differentiate whether the reduced growth rate was caused by the warmest year since records began in 1884 or whether this represents a seasonal phenomenon. A possible explanation for the positive growth rates in the first measurement period is that the highest relative humidity occurred in the first two months. Wet and warm nights might be the possible reasons for negative growth rates recorded in the subsequent measurement periods because the highest air temperature, dew point, and rainfall occurred in August.
Other studies have also documented the responses of bryophytes to climate change, and even slight shifts in climate conditions may have negative consequences. Range shifts of vascular plants induced by higher temperatures in high-latitude ecosystems led to a reduction in bryophyte cover (Tømmervik et al. 2004; Guglielmin et al. 2014; Royles and Griffiths 2014). Bjerke et al. (2011) suggested that a warm winter had negative effects on the photosynthetic activities and growth rates of moss species in sub-arctic heathlands. Furthermore, the range for many European bryophyte species has contracted whereas range expansions for other species have occurred at their northern limits (Bergamini et al. 2009; Désamoré et al. 2012; Hodd et al. 2014).
Bryophytes, especially epiphytes, have long been used as excellent indicators to monitor climate change (Gignac 2001). S. subhumile and P. pohliaecarpum showed the most significant and substantial differences in growth and health four months after being exposed to warmer and drier environments. Therefore, S. subhumile and P. pohliaecarpum could be employed as potential climate change indicators in the marginal tropics. A significant negative effect of relocation to lowland areas on the health and biomass of B. buchananii was detected six months after transplanting. These results indicate that B. buchananii is susceptible to climate change. The five other moss species survived the experiment even though they experienced severely deteriorated health and reduced growth rates. This implies that these species are not good indicators of climate change, and might indicate that even warmer and drier sites are suitable for some species due to their phenotypic plasticity (Bradshaw 1965; Callahan et al. 1997). Why these five species were unsuccessful in establishing in lowland areas remains unresolved. All species have limitations to their capacity for adaptive response to changing environments (Williams et al. 2008), and these limits are unlikely to increase for species already experiencing warm temperatures close to their tolerance limits (Araújo et al. 2013).
Implications for conservation
To understand the rapid, persistent impact of climate change, we generally need several decades of data to rigorously assess pre- and post-climate change trends at the level of species and ecosystems (Brown et al. 2016); however, such long-term data sets are rare for biological systems (Laurance et al. 2011). In this study, we attempted to assess the possible short-term impact of climate change on the health status, growth, and survival rate of terrestrial moss species. These species were susceptible to simulated climate change and may be more vulnerable than vascular species. This study fills the gap in empirical evidence on the sensitivity of terrestrial moss species to climate change. As climate conditions in the tropics are expected to become hotter and drier (Ramirez and Jarvis 2008; Lewis et al. 2011), many moss species might be negatively affected or even at the risk of extinction. The bryophyte communities in the tropics might be one of the best biological populations to reflect the direct impact of climate change and provide an early warning of biological outcomes induced by ongoing climate change, even though we cannot predict the long-term influence of climate change from the present study.
Because bryophytes have essential ecological functions in land ecosystems, the adverse effects of climate change on moss species cannot be considered in isolation (Zotz and Bader 2009). The dying back and even disappearance of terrestrial moss species related to climate change may have cascading negative effects on the whole forest ecosystem. Thus, conservation efforts to sustain and improve the stability and resiliency of tropical forest ecosystems to climate change should include bryophyte communities.
Although there is an enormous body of basic research on climate change, few long-term conclusions can be drawn about future consequences. Local adaptation due to phenotypic plasticity may be overestimated due to current climatic conditions. However, as the rate of future climate change will likely outweigh the potential acclimation of many species, in addition to human-induced habitat loss and habitat fragmentation, the challenges of moss species redistribution induced by climate change may not occur.