Responses of serpentine plants to pine invasion: Vegetation diversity and nickel accumulation in species with contrasting adaptive strategies

Highlights

• Effects of pine invasion on serpentine vegetation and Ni accumulation were analyzed.

• Vegetation α-diversity and distinctness were decreased and composition was changed.

• Pine trees caused acidification, drop of soil total Ni and decline of endemic taxa.

• Pine stands did not affect shoot Ni hyperaccumulation despite lower root Ni level.

• Ni level decreased in non-accumulator species, which did not decline in pine stands.

Abstract

Introduction of non-native trees is one of the major threats to ecosystem integrity and biodiversity. Stands of maritime pine (Pinus pinaster Ait.) introduced decades ago represent a threat to the specialized plant communities of serpentine outcrops in Italy. This study investigates the effects of such invasions at the community and species level, based on vegetation sampling in three selected sites with comparable environmental conditions. Pine cover caused a decrease of α-diversity by lowering the species evenness of the community, though species richness was not negatively affected. Compositional changes between the two habitats were significant but not clearly associated with a decrease in taxonomic distinctness in the pine stands. As many as nine indicator species were found in the open vegetation, along with the obligate endemics Odontarrhena bertolonii and Armeria denticulata. Both of them declined in the pine stands. Here, an increase in the phytoavailable nickel fraction was associated with a decrease in total nickel concentration in the soil, via mobilization of the metal caused by lowering of pH induced by the conifer litter. The nickel-hyperaccumulator O. bertolonii was able to maintain high metal concentrations in the shoots despite a decrease in root concentration, resulting in a higher shoot/root ratio in the pine stands (~ 20). Conversely, shoot/root ratio in the non-accumulator Plantago holosteum was < 1 and not affected by the conifer, as well as its abundance in this anthropogenic habitat. Contrasting responses of the two species were likely due to their different sensitivity to modified light and soil conditions, whereas stability of shoot nickel-concentration in O. bertolonii did not support increased predation by natural enemies as one of the causes for its decline under the conifer.

Progressive thinning of these stands is advocated to limit soil nickel mobilization and to restore a unique ecosystem with its endemic metallophytes.

Introduction

One of the major threats to biodiversity and integrity of natural habitats is the spread of invasive plant species (Pauchard and Shea, 2006). The introduction of non-native trees forming monospecific stands can result in the long-term alteration of the structure and functioning of the invaded ecosystems with consequent shifts in plant species composition (Jose et al., 2008). Several studies have shown that such woody species can significantly reduce local species richness and alter floristic assemblages via changes in soil conditions (González-Muñoz et al., 2012, Lorenzo et al., 2012, Benesperi et al., 2012). Among the many habitat types that are prone to invasions there are also those typical to the outcrops of ultramafic soils (Burgess et al., 2015), especially serpentine. Here, tree colonization is often a consequence of past introductions of conifers made with the intent of improving soil protection and increasing vegetation cover of the low and sparse communities characteristic of these sites (Barton and Wallenstein, 1997, Cumming and Kelly, 2007). Indeed, serpentine outcrops are severely stressful habitats for plant life because of factors such as the very low Ca/Mg ratio, the elevated concentrations of heavy metals, especially Ni, Cr and Co, and the deficiency of nutrients (Brooks, 1987, Brady et al., 2005, Alexander, 2006, Gonnelli and Renella, 2012). In addition, the usually high rock fragment content, the slow weathering and the dark color cause a marked heating and scarcity of available water under sunny conditions, further contributing to the often stunted vegetation (Proctor, 1999). Wherever they occur on Earth, serpentine outcrops represent ecological “islands” inhabited by a relatively small number of specialized “metallophytes”, often locally restricted (Baker et al., 1992, Anacker, 2014). Communities formed by these plants are strongly characterized in terms of structure and floristic composition, providing an outstanding contribution to the overall biological diversity of the territories where they occur. Hence, in-situ conservation of these ecosystems is increasingly recognized as a major target of biological conservation, due to their scientific interest and the numerous potential applications of the constituent metallophytes (Baker et al., 2010, Thorne et al., 2011, Baumbach, 2012). However, introductions of non-native trees and consequent invasions are usually not included among the threats to these sites (Whiting et al., 2004), explaining why the responses of serpentine vegetation and plants to such anthropogenic disturbance are neglected and still poorly understood.

Since the mid-20th Century, several outcrops in central Italy have been planted with Pinus sp., especially the maritime pine (Pinus pinaster Ait.), due to its pioneer characteristics, resistance to drought and adaptation to low levels of soil nutrients. This conifer has been widely employed for afforestation purposes in the Mediterranean (Andrés and Ojeda, 2002, Selvi et al., 2016) and in the southern Hemisphere (Richardson et al., 1994). However, it often shows an invasive nature and represents a threat to the integrity of natural ecosystems, due to its fast growing capacity and regeneration ability under a variety of environmental conditions, especially after fires (Fernandes and Rigolot, 2007). Spread of non-native P. pinaster stands also occurs in Italian serpentine environments, where it may lead to potentially significant alterations of the natural soil-vegetation dynamics. In fact, it is well-documented that the thick layer of needle-litter of pines and other conifers has chemical and physical effects on soil, such as acidification and loss of fertility (Augusto et al., 2002, Binkley and Giardina, 1998). A significant decrease of pH and other effects on soil conditions were observed in pine-invaded serpentine grasslands in the eastern United States (Barton and Wallenstein, 1997, Cumming and Kelly, 2007, Burgess et al., 2015) and in a metalliferous area in Poland (Kapusta et al., 2015), whereas studies at an Italian ultramafic site (Chiarucci and De Dominicis, 1995, Chiarucci, 1996) mainly focused on changes in species richness and vegetation structure caused by pine afforestation. However, the overall impact of the conifer on the plant community still remain to be investigated on a wider spatial scale, to account for the geographic and floristic variations among the regional serpentine outcrops (Selvi, 2007). A first aim of the present investigation was, therefore, to test the hypothesis that artificial pine cover is able to cause changes in terms of α- and β-diversity, taxonomic distinctness and composition of the vegetation on geographically isolated outcrops.

Previous studies also indicated that pine afforestation can cause changes in metal concentrations in the soil (Chiarucci and De Dominicis, 1995, Cumming and Kelly, 2007), but whether and how these changes affect, in turn, the concentrations of heavy metals in the organs of the serpentine plants is still unknown. Understanding these effects is especially relevant to address some of the ecological and conservation aspects regarding the nickel-hyperaccumulating taxa, e.g. those plants that can accumulate this metal in concentrations higher than 1000 μg g^− 1 of leaf d.w. (van der Ent et al., 2013). This rare trait is supposed to have evolved as a defense strategy against natural enemies, especially herbivores, because of the toxic and deterrent effect of the high metal concentration in shoots (Martens and Boyd, 2002, Palomino et al., 2007, Boyd, 2012). Hence, the competitive ability of these species might decrease if, specifically, the lowering of soil pH induced by the conifer litter resulted in a drop of nickel content in their aboveground parts, thus increasing plant vulnerability to natural enemies. Together with the possible impact of canopy shading and other direct effects of soil, this may be an additional detrimental factor for the long-term persistence of nickel-hyperaccumulating species in a scenario of increasing invasion by the pine.

Accordingly, we used Odontarrhena bertolonii (Desv.) L. Cecchi & Selvi (syn. Alyssum bertolonii Desv.) as a model species to investigate the effects of artificial pine canopy on the concentration of nickel in roots and above-ground parts. This crucifer is the most typical obligate endemic of the sparse vegetation of the serpentine outcrops in Tuscany and southeast Liguria (Cecchi et al., 2013); it is the first nickel-hyperaccumulator discovered (Minguzzi and Vergnano, 1948, Galardi et al., 2007) and the only one found in this region. Responses of O. bertolonii were compared to those of a second species, Plantago holosteum Scop. to understand the possible consequences of pine invasion on a typical preferential serpentinophyte without nickel-accumulation capacity (Pandolfini and Pancaro, 1992). This approach allowed to test a second hypothesis, e.g. that the responses to possible conifer-induced changes in the soil nickel concentration, in terms of metal accumulation pattern, are different between species with hyperaccumulating and excluding strategies. Resulting evidence provides helpful insights into the management strategies to be adopted to favor the long-term conservation of a specialized ecosystem and its unique plant species.