Effects of thermal stress on seagrass populations
Patterns of thermal performance in P. oceanica varied among populations and deviated from expectations with respect to range position, highlighting the challenges of extrapolating climate change vulnerability predictions from local observations. Among cool, central and warm-edge populations, only measures of new leaf production supported models of local-adaptation/acclimatization and no metrics consistently supported expectations of thermal-niche conservatism between populations. The positive relationship between new-leaf production and thermal anomalies indicates higher rates of leaf turnover (i.e., shorter lifespan) under warmer conditions, potentially reflecting a coping strategy for thermal stress within fragments. Cool-edge and warm-edge populations did display similar rates of growth and survival under warm-edge (29ºC) conditions, suggestive of niche conservatism, however central populations exhibited comparatively poor performance, in contrast to expectations. Moreover, patterns of poor thermal performance by central populations at the warm edge were consistent with results among centre-centre procedural controls, which experienced similar absolute temperatures to warm-edge treatments. Growth patterns from the natural meadows over the same period further support these findings, showing lower growth rates and higher new-leaf production in centre-populations relative to cool and warm-edge meadows following the thermal stress period, reinforcing that experimental findings were not an experimental artefact.
Unlike centre-populations, the high resilience of cool-edge P. oceanica to thermal stress was consistent with documented responses of congeneric Posidonia species to a natural heatwave of similar magnitude. In 2011, Western Australia experienced the most intense marine heatwave on record (Hobday et al. 2016) andPosidonia australis displayed relatively minor impacts despite experiencing thermal anomalies in excess of 5ºC and absolute temperatures reaching 30ºC (Strydom et al. 2020). In contrast toP. australis, other seagrasses (i.e. Amphibolis antarctica ) experienced severe losses (Fraser et al. 2014) and kelp forests (Ecklonia radiata ) suffered a 100 km range contraction (Wernberg et al. 2016) in response to the 2011 heatwave. While the response by P. oceanica to large anomalies in the current study was relative to cool-edge (c.f. warm-edge in P. australis ) conditions, the similarity between species to survive temperatures up to 30ºC highlights a remarkable latent capacity to withstand thermal stress in these edge populations. Latent tolerance to extreme events potentially reflects the warm evolutionary origins of the genus and the high resilience Posidonia has displayed to climatic upheaval over the past 60 mya (Por 2009; Bianchi et al. 2012).
The idea of P . oceanica as resilient to heat stress may appear at odds with the prevailing literature, which has demonstrated (Diaz-Almela et al. 2009; Marba & Duarte 2010) and projected (Jordà et al. 2012; Chefaoui et al. 2018) high sensitivity of P. oceanica to warming. However, the results of the current study are consistent with these previous findings and help place them in a broader geographical context. Central populations of P. oceanica were severely affected by thermal anomalies up to 1.5ºC above long term summer maxima in the current study. Anomalies of this magnitude are slightly cooler than those experienced during the 2003 Mediterranean heatwave, which caused a steep increase in shoot mortality in central populations (Marba & Duarte 2010). Our findings therefore support previous evidence that P. oceanica in central populations are living close to their thermal limits but suggest that populations elsewhere may indeed have greater tolerance of high temperatures. The reason why central populations of P. oceanica are more severely affected by high temperatures than cool and warm-edge populations is unclear. The genetic structure of P. oceanica is characterised by strong separation between the eastern and western basins, consistent with a vicariance event during the last glacial maxima (Arnaud‐Haondet al. 2007). Within the western basin, genetic connectivity is relatively low for both the cool-edge and central experimental collection locations, but both these locations are directly connected to the same central node within the regional metapopulation (Rozenfeldet al. 2008). Central and cool-edge populations, therefore, share more genetic and climatological similarities over geological timescales than cool-edge and warm-edge populations (Chefaoui et al. 2017), whereas central and warm-edge populations share more contemporary similarities in terms of selection pressure on upper thermal limits. Despite this, central populations exhibit the greatest sensitivity to temperature, across the distribution of P. oceanica forcing a re-evaluation of the vulnerability and management of this species in response to climate change.
While field-based evidence of performance could not separate cool-edge and warm-edge populations, the maximum realised temperature in our experiment was 29.3ºC. Therefore, we cannot rule out the possibility that differences in performance between populations occur at higher temperatures. Indeed, previous laboratory-based experiments have suggested that warm-edge populations can survive temperature up to 36ºC, whereas cool-edge populations and central populations of P. oceanica display upper thermal limits around 30ºC (Bennett et al. 2021). Such experimental evidence would suggest that cool-edge populations were close to their upper threshold during the current experiment whereas warm-edge populations retained a larger thermal buffer. Previous laboratory experiments, however, did not document the subsequent recovery of P. oceanica following thermal stress. While cool-warm and cool-centre treatments clearly showed signs of thermal stress in the current study, our results suggest that they have greater capacity to endure and recover from heat stress than central-populations.