Hypotheses, mechanisms and trade‐offs of tolerance and adaptation to serpentine soils: from species to ecosystem level

Abstract

Understanding the relative importance of the abiotic environment and species interactions in determining the distribution and abundance of organisms has been a challenge in ecological research. Serpentine substrata are stressful environments for plant growth due to multiple limitations, collectively called the "serpentine syndrome". In the present review, our aim is not only to describe recent work in serpentine ecology, but also to highlight specific mechanisms of species tolerance and adaptation to serpentine soils and their effects on community structure and ecosystem functioning. We present hypotheses of the development of serpentine endemism and a description of functional traits of serpentine plants together with a synthesis of species interactions in serpentine soils and their effects on community structure and ecosystem productivity. In addition, we propose hypotheses about the effects of the 'serpentine syndrome' on ecosystem processes including productivity and decomposition.

Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex

“…The other hypothesis proposes a single origin of a genetic adaptation to metalliferous substrates, its spread across outlying metalliferous sites and subsequent differentiation between more recently established metallicolous populations because of genetic drift. These alternative views resonate with earlier debates as to whether local populations of metal-tolerant plants occurring on metalliferous outcrops represent 'neoendemics' or 'palaeoendemics', respectively (equivalent to the 'insular' and 'depleted' species of Stebbins (1942), as discussed by Kazakou et al (2008)). Correspondingly, non-metallicolous populations of such species could be either ancestral, as in the first scenario, or locally derived from metallicolous populations, as in the second.…”

“…However, only 15 described species are known to display zinc hyperaccumulation (Meerts and Van Isacker, 1997;Bert et al, 2000;Krämer, 2010), and nickel hyperaccumulation warrants further research as part of attempts to understand the evolutionary basis of plant adaptation to serpentine (Brady et al, 2005;Kazakou et al, 2008;Turner et al, 2010). The present paper thus focusses on evolution of nickel hyperaccumulation in the genus Alyssum (Brassicaceae) that contains 51 known hyperaccumulator taxa out of ∼ 190 species, making this the largest number of hyperaccumulating species found within a single genus (Brooks, 1998;Burge and Barker, 2010).…”

“…Ultramafic substrates are derived from igneous rocks with a low silica content but rich in mafic minerals such as magnesium, iron and nickel. Weathering of ultramafic bedrock creates serpentine soils with distinctive physical and chemical characteristics, including particularly high contents of nickel, cobalt and chromium, high Mg/Ca ratio and low levels of the essential macronutrients nitrogen, phosphorus and potassium (Brooks, 1987;Kazakou et al, 2008). Most types of soil show nickel concentrations typically between 7 and 50 mg kg − 1 , whereas in serpentine soils the nickel content usually ranges from 700 to 8000 mg kg − 1 (Reeves, 1992;Reeves and Baker, 2000).…”

Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora

“…In an evolutionary perspective, serpentine soils might be considered, similar to other metal contaminated soils, as "ecological islands" (Lefèbvre and Vernet 1990), inhabited by particular, often endemic, taxa. The ecological island model has boosted much research on evolution and adaptation and provoked discussion on the microevolutionary dynamics of metal tolerance and metal hyperacumulation in plants, from the population to the single-gene level (for examples see Berglund et al 2004;Kazakou et al 2008;Mengoni et al 2003a;Mengoni et al 2003b;Rajakaruna et al 2003;Vekemans and Lefèbvre 1997). Despite the long history of interest in serpentine plants, the attention of microbiologists towards bacteria from serpentine habitats is more recent, with the relevant exception of Lipman (1926), and intimately linked to the peculiar botanical features of serpentine outcrops.…”

How are rare species maintained?: Reproductive barriers between Layia jonesii, a rare serpentine endemic, and L. platyglossa

“…These results show that L. jonesii is sensitive to competition from surrounding species. Reduced competitive ability of some serpentine endemics may be due to an evolutionary trade-off between serpentine tolerance and competitive ability (Kruckeberg, 1954;Kazakou et al, 2008;Kay et al, 2011). It hypothesized that serpentine soils serve as a kind of refuge from competition for many serpentine species which have a lowered ability to compete with species on nonserpentine soils (Alexander et al, 2007;Brady et al, 2005;Kruckeberg, 1954), but my results suggest competitive interactions could influence the distribution of serpentine endemics at an even finer scale.…”