Tropical seagrass Halophila stipulacea shifts thermal tolerance during Mediterranean invasion

Abstract

Exotic species often face new environmental conditions that are different from those that they are adapted to. The tropical seagrass Halophila stipulacea is a Lessepsian migrant that colonized the Mediterranean Sea around 100 years ago, where at present the minimum seawater temperature is cooler than in its native range in the Red Sea. Here, we tested if the temperature range in which H. stipulacea can exist is conserved within the species or if the exotic populations have shifted their thermal breadth and optimum due to the cooler conditions in the Mediterranean. We did so by comparing the thermal niche (e.g. optimal temperatures, and upper and lower thermal limits) of native (Saudi Arabia in the Red Sea) and exotic (Greece and Cyprus in the Mediterranean Sea) populations of H. stipulacea . We exposed plants to 12 temperature treatments ranging from 8 to 40°C for 7 days. At the end of the incubation period, we measured survival, rhizome elongation, shoot recruitment, net population growth and metabolic rates. Upper and lower lethal thermal thresholds (indicated by 50% plant mortality) were conserved across populations, but minimum and optimal temperatures for growth and oxygen production were lower for Mediterranean populations than for the Red Sea one. The displacement of the thermal niche of exotic populations towards the colder Mediterranean Sea regime could have occurred within 175 clonal generations.

Projected Rapid Habitat Expansion of Tropical Seagrass Species in the Mediterranean Sea as Climate Change Progresses

“…The SDMs pointed out that maximum annual temperatures, and to a lesser degree maximum annual salinity, are essential factors determining the fundamental niche of H. stipulacea in the Mediterranean Sea. Our results are consistent with recent experimental studies demonstrating the first evidence of optimal acclimatization of native and invasive Mediterranean populations of H. stipulacea to projected scenarios of Mediterranean climate change, including temperatures of 30-32 • C and salinities higher than 40 PSU (Georgiou et al, 2016;Oscar et al, 2018;Nguyen et al, 2020;Wesselmann et al, 2020). Similarly, native populations from the Persian Gulf are adapted to even more extreme conditions, with in situ summer temperatures of 33-34 • C and summer salinities of 39.0-39.5 PSU (Tyberghein et al, 2012), defining H. stipulacea as an exceptional euryhaline and thermal-tolerant species.…”

“…While the presence of cold waters may represent a barrier to the expansion of H. stipulacea into westernmost habitats in the Mediterranean Sea, a recent study identified this region as a habitat refuge for the foundation species P. oceanica and C. nodosa under future climate scenarios (Chefaoui et al, 2018). Similarly, an even newer study reported that H. stipulacea in the Mediterranean Sea can cope with significantly lower temperatures (∼14 • C) than what observed in its native habitats (∼23 • C), suggesting a thermal niche shift to the lower temperatures in the Mediterranean Sea and potentially allowing this species to colonize temperate regions (Nguyen et al, 2020;Wesselmann et al, 2020). This physiological capability may be explained by the capacity to produce and accumulate high levels of unsaturation in the lipidic structures of the leaves of H. stipulacea (Beca-Carretero et al, 2019).…”

“…Climate change is expected to compromise the distribution of the large and slow-growing endemic Mediterranean seagrass species P. oceanica and, to a lesser degree, the fast-growing C. nodosa (i.e., Olesen et al, 2002 ; Chefaoui et al, 2018 ; Ruocco et al, 2018 ; Ontoria et al, 2019 ). In contrast, increases in temperature and salinity are expected to promote the performance and distribution of the invasive species H. stipulacea ( Oscar et al, 2018 ; Nguyen et al, 2020 ; Wesselmann et al, 2020 ). Our results clearly show a critical expansion of the biogeographical range of H. stipulacea and H. decipiens as climate change progresses during this century, with 80% of the Mediterranean coastline predicted to be suitable for colonizing based on temperature and salinity conditions alone.…”

Species-Specific Trait Responses of Three Tropical Seagrasses to Multiple Stressors: The Case of Increasing Temperature and Nutrient Enrichment

“…Shorter IL, as a proxy of higher shoot and root density, is a common feature under stressful environmental factors, suggesting that H. stipulacea invests excess energy (increased Alpha values) in increasing number of shoots ( Jensen and Bell, 2001 ; Kilminster et al, 2008 ) rather than on leaf length. In the literature, H. stipulacea thermal optima and limits showed differences between populations ( Nguyen et al, 2020 ; Wesselmann et al, 2020 ) but thermal optima at the Red Sea was set at 30°C ( Anton et al, 2020 ; Wesselmann et al, 2020 ). It is possible that these differences highlight the importance of the different population responses in coping with stressors ( McMillan and Phillips, 1979 ; Winters et al, 2011 ; Nguyen et al, 2020 ; Wesselmann et al, 2020 ) where other environmental factors, such as light irradiance, or population genetics influence the responses ( Collier et al, 2016 ).…”

“…H. stipulacea , contrary to the large blades species, did not appear to be negatively affected by the studied factors, showing potentially a dormancy strategy under the different treatments. Even though performance differences have been observed between individuals from its native and invasive ranges ( Nguyen et al, 2020 ; Wesselmann et al, 2020 ) this species is generally recognized to be tolerant to a wide range of trophic conditions and temperatures ( Winters et al, 2020 ). Although H. stipulacea is considered as invasive in the Mediterranean and Caribbean Seas, there is no evidence of competition and displacement of native species in these areas ( Boudouresque et al, 2009 ; Al-Rousan et al, 2011 ; Gambi et al, 2018 ; Apostolaki et al, 2019 ).…”