Combined ecological niche models and dispersal simulations to predict bryophytes dynamic response to climate changes

The extent to which species can balance out the loss of suitable habitats due to climate warming by shifting their ranges is an area of controversy. Here, we assess whether highly efficient wind-dispersed organisms like bryophytes can keep-up with projected shifts in their areas of suitable climate. Using a hybrid statistical-mechanistic approach accounting for spatial and temporal variations in both climatic and wind conditions, we simulate future migrations across Europe for 40 bryophyte species until 2050. The median ratios between predicted range loss vs expansion by 2050 across species and climate change scenarios range from 1.6 to 3.3 when only shifts in climatic suitability were considered, but increase to 34.7-96.8 when species dispersal abilities are added to our models. This highlights the importance of accounting for dispersal restrictions when projecting future distribution ranges and suggests that even highly dispersive organisms like bryophytes are not equipped to fully track the rates of ongoing climate change in the course of the next decades.

Despite a growing number of climate change mitigation policies, anthropogenic greenhouse gas emissions have continued to increase over 1970 to 2010, with larger absolute increases between 2000 and 2010. Indeed, the period from 1983 to 2012 has been identified as the warmest 30-year period of the last 1400 years in the Northern Hemisphere. As a result, climate changes have been identified as one of the major biodiversity threats, with the worst-case scenarios leading to extinction rates that would qualify as the sixth mass extinction in the history of the earth. Species distribution models (SDMs) have been the most widely used tool to assess the impact of future climate changes on biodiversity patterns, using spatial information to infer species ecological niches from climatic conditions that prevail today across the distribution range occupied by the species. One of the main assumptions of these models is, however, that species live at equilibrium with their environment, as if they had no dispersal limitations. Such an assumption is critical if we aim at projecting these modeled ecological niches under future climatic conditions. The main goal of the present thesis was to develop an integrative, spatially explicit model to make predictions of range shifts in wind-dispersed organisms in a context of climate changes. More precisely, we calibrated a Wald analytical long distance dispersal model with species intrinsic biomechanical features (i.e., the settling velocity of diaspores and their release height) and environmental variables (i.e., canopy height, wind intensity and turbulence), through direct observations of diaspore deposition patterns. We then integrated this dispersal model combined with habitat suitability maps into a modified version of MigClim’s cellular automaton that allows migration simulation of species across the landscape, while implementing environmental change scenarios. Initially, MigClim assumed an isotropic colonization probability around a source population with a single constant dispersal kernel across the landscape. This was challenging its use for wind-dispersed organisms because (i) wind movements are directional and (ii) wind velocity varies widely from an area to another across the landscape. We therefore developed this method to (i) allow the integration of asymmetrical dispersal depending on wind parameters and (ii) render the dispersal kernel spatially-explicit by sampling pixel-specific wind speed and canopy structure along the migration simulations. We applied this method to predict how climate changes will impact future distribution ranges in bryophytes, which are particularly sensitive to climatic variations due to their poïkilohydry. We started by measuring bryophytes spores settling velocities using a high-speed camera experiment and produced a predictive model as a function of spore size. The non-sphericity and particular ornamentation patterns of the outer spore wall caused some mismatch between observed and predicted settling velocities, raising questions on how these striking variations in shape and texture affect their dispersal capacity. However, we globally identified a significant relationship between spore9 settling velocity and size. Based on these spore fall speed estimates and a set of SDM derived maps of habitats suitability at present time and in predicted 2050 climatic conditions in Europe, we ran a sensitivity analysis on a modified version of MigClim to test the impact of differences in spores release height and horizontal mean wind speed. Variation in predicted colonization success was significantly driven by release height but not by differences in horizontal mean wind speed, suggesting that, in small-sized wind-dispersed organisms like bryophytes, there is a strong evolutionary pressure for elevating the sporophyte above ground. The implementation of the combined model on three species of contrasted distribution across Europe reveals much higher extinction than colonization rates, even for the most optimistic climatic scenarios and the most successful wind dispersal kernels. Although additional models need to be produced to forecast climate changes impacts on a wide range of bryophyte species, our preliminary results point to a much more severe impact of climate warming for bryophytes as compared to vascular plants. This highlights the primary role of bryophytes as indicators of climate changes.

Dispersal is a fundamental biological process that can be divided into three phases: release, transportation, and deposition. Determining the mechanisms of diaspore release is of prime importance to understand under which climatic conditions and at which frequency diaspores are released and transported. In mosses, wherein spore dispersal takes place through the hygroscopic movements of the peristome, the factors enhancing spore release has received little attention. Here, we determine the levels of relative humidity (RH) at which peristome movements are induced, contrasting the response of species with perfect (fully developed) and specialized (reduced) peristomes. All nine investigated species with perfect peristomes displayed a xerochastic behavior, initiating a closing movement from around 50%–65% RH upon increasing humidity and an opening movement from around 90% RH upon drying. Five of the seven species with specialized peristomes exhibited a hygrochastic behavior, initiating an opening movement under increasing RH (from about 80%) and a closing movement upon drying (from about 90%). These differences between species with hygrochastic and xerochastic peristomes suggest that spore dispersal does not randomly occur regardless of the prevailing climate conditions, which can impact their dispersal distances. In species with xerochastic peristomes, the release of spores under decreasing RH can be interpreted as an adaptive mechanism to disperse spores under optimal conditions for long‐distance wind dispersal. In species with hygrochastic peristomes, conversely, the release of spores under wet conditions, which decreases their wind long‐distance dispersal capacities, might be seen as a safe‐site strategy, forcing spores to land in appropriate (micro‐) habitats where their survival is favored. Significant variations were observed in the RH thresholds triggering peristome movements among species, especially in those with hygrochastic peristomes, raising the question of what mechanisms are responsible for such differences.

Background and aims: The settling velocity of diaspores is a key parameter for the measurement of dispersal ability in wind-dispersed plants and one of the most relevant parameters in explicit dispersal models, but remains largely undocumented in bryophytes. The settling velocities of moss spores were measured and it was determined whether settling velocities can be derived from spore diameter using Stokes' Law or if specific traits of spore ornamentation cause departures from theoretical expectations. Methods: A fall tower design combined with a high-speed camera was used to document spore settling velocities in nine moss species selected to cover the range of spore diameters within the group. Linear mixed effect models were employed to determine whether settling velocity can be predicted from spore diameter, taking specific variation in shape and surface roughness into account. Key results: Average settling velocity of moss spores ranged from 0·49 to 8·52 cm s(-1) There was a significant positive relationship between spore settling velocity and size, but the inclusion of variables of shape and texture of spores in the best-fit models provides evidence for their role in shaping spore settling velocities. Conclusions: Settling velocities in mosses can significantly depart from expectations derived from Stokes' Law. We suggest that variation in spore shape and ornamentation affects the balance between density and drag, and results in different dispersal capacities, which may be correlated with different life-history traits or ecological requirements. Further studies on spore ultrastructure would be necessary to determine the role of complex spore ornamentation patterns in the drag-to-mass ratio and ultimately identify what is the still poorly understood function of the striking and highly variable ornamentation patterns of the perine layer on moss spores.

Dispersal is a key evolutionary force that determines the survival, growth and reproduction of individuals, cycles of colonization and extinction of populations and globally drives species dynamic responses to their environment. In the context of extent climate changes, these dynamics take on even greater importance as the survivability of species depends on their ability to shift their distribution or adapt to changes in local climatic conditions. We focus on bryophytes, whose documented long distance dispersal ability, together with their lack of vascular system, position as likely indicator species to monitor the effects of climate changes. We use an approach combining Ecological Niche Models (ENM) and Dispersal Simulations (MigClim) to model the actual niche and simulate the future potential response of bryophytes to environmental changes in Europe. For this purpose we computed specific dispersal kernels using WALD analytical models that integrate both experimentally derived spores settling velocity and continental wind and forest canopy data to infer potential species dispersal capacities. MigClim cellular automaton was then used to simulate atmospheric dispersal over maps of habitat suitability generated from ENMs and enabled us to question European bryophytes ability to colonize suitable areas under actual, and predicted future climatic conditions.