Patterns and mechanisms of heavy metal accumulation and tolerance in two terrestrial moss species with contrasting habitat specialization

Abstract

Anthropogenic activities have increased exposure to heavy metal pollution in previously uncontaminated ecosystems, threatening plant communities. Considering that phenotypic variation underlies rapid adjustment to challenging environmental conditions in natural populations, the study of variation in traits related to plant response to heavy metal stress provides valuable insight into the likelihood of a population’s survival. This paper investigates patterns of intraspecific phenotypic variation for heavy metal accumulation and tolerance in bryophytes, one of the most resilient and relatively understudied plant taxa. We examined two moss species with contrasting affinities for heavy metals: the heavy metal specialist Scopelophila cataractae, and the facultative metallophyte Ceratodon purpureus. We sampled four populations of S. cataractae in close microhabitats with different contamination levels of Cd and Cu, one population of C. purpureus in an urban area, and separate lab-maintained male and female isolates from one population of C. purpureus growing in axenic conditions. After clonally propagating all populations under control, Cd and Cu treatments, we measured plant fitness, oxidative damage, and Cd and Cu accumulation. Scopelophila cataractae isolates from microhabitats with higher levels of metals in the field (Sc2, Sc3) were more tolerant than those collected in less contaminated microhabitats (Sc1, Sc4). Sc2 and Sc3 accumulated significantly less Cu in the leaves compared to the stem which could limit damage to their main photosynthetic organs and contribute to the observed differences in Cu tolerance. In contrast C. purpureus showed intraspecific differences in tolerance to Cd and Cu, but not in accumulation. These differences arose among isolates that had never been exposed to heavy metals before. We also report the first evidence for sexual dimorphism for Cd tolerance in this species, with females being more tolerant than males. Altogether, our results provide novel insights into the mechanisms used by bryophytes to deal with heavy metal stress, as well as the first evidence for metal-dependent, sex-specific differences in heavy metal tolerance in bryophytes.