Regime shift by an exotic nitrogen-fixing shrub mediates plant facilitation in primary succession

Abstract

Ecosystem invasion by non-native, nitrogen-fixing species is a global phenomenon with serious ecological consequences. However, in the Mediterranean basin few studies addressed the impact of invasion by nitrogen-fixing shrubs on soil quality and hydrological properties at local scale, and the possible effects on succession dynamics and ecosystem invasibility by further species. In this multidisciplinary study we investigated the impact of Genista aetnensis (Biv.) DC., an exotic nitrogen-fixing shrub, on the Vesuvius Grand Cone (Southern Italy). Specifically, we tested the hypotheses that the invasion of G. aetnensis has a significant impact on soil quality, soil hydrological regime, local microclimate and plant community structure, and that its impact increases during the plant ontogenetic cycle. We showed that G. aetnensis, in a relatively short time-span (i.e. ~ 40 years), has been able to build-up an island of fertility under its canopy, by accumulating considerable stocks of C, N, and P in the soil, and by also improving the soil hydrological properties. Moreover, G. aetnensis mitigates the daily range of soil temperature, reducing the exposure of coexisting plants to extremely high temperatures and water loss by soil evaporation, particularly during the growing season. Such amelioration of soil quality, coupled with the mitigation of below-canopy microclimatic conditions, has enhanced plant colonization of the barren Grand Cone slopes, by both herbaceous and woody species. These results suggest that the invasion of G. aetnensis could eventually drive to the spread of other, more resource-demanding exotic species, promoting alternative successional trajectories that may dramatically affect the local landscape. Our study is the first record of the invasion of G. aetnensis, an additional example of the regime shifts driven by N-fixing shrubs in Mediterranean region. Further studies are needed to identity specific management practices that can limit the spread and impacts of this species.

Fig 1. Genista aetnensis invasion of the Vesuvius Grand Cone.

Changing landscape at the Vesuvius Grand Cone following Genista aetnensis invasion. Pictures have been taken from the West side of the Grand Cone in 1880 (Raccolte Museali Fratelli Alinari, Firenze, Italy) and in 2013 (Picture by Stinca A.).

Fig 2. Results of the litter decomposition experiment.

Dynamics of litter mass (% of initial value) in litterbags decomposing for 360 days under (IN) and outside (OUT) the canopy of adult Genista aetnensis individuals, and corresponding changes of cellulose and lignin percent content (top), C-to-N and lignin-to-N ratios (bottom) and N percent content (inset). Data refer to mean and standard deviation of 10 replicates for each harvesting date. Data of chemical variables (cellulose, lignin, N, C-to-N and lignin-to-N ratios) are pooled for IN and OUT areas, since such factor did not affect significantly litter decomposition in the field (S6 Table).

Fig 3. Plant growth in the greenhouse bioassay.

Plant dry biomass of six target species pot-grown on soil collected at the Vesuvius Grand Cone, outside and under the canopy of either living (OUT_S3 and IN_S3, respectively) or dead (OUT_D and IN_D, respectively) Genista aetnensis adult individuals. For each species and within each treatment, data refer to mean and 95% confidence interval of single plant dry mass (g) from 15 replicated pots. Different small letters indicate statistically significant difference among soil types (Post-hoc Duncan test at p<0.05, from two-way ANOVA in S7 Table).

Fig 4. Time series of microclimate variables.

Daily values of cumulated rainfall, average air temperature and relative humidity, soil temperature and water content measured at both 5 cm and 20 cm depths outside (OUT—red lines) and under the canopy of living (IN_S3—black lines) Genista aetnensis adult individuals. Data refer to 1 year of monitoring (January 2012 – January 2013).

Fig 5. Effects of Genista aetnensis canopy on light regime.

Photosynthetic active radiation (PAR) attenuation along the vertical profile under (IN) and outside (OUT) the canopy of Genista aetnensis individuals at different ontogenetic stage (S1, S2, S3, D) at the Vesuvius Grand Cone. Data refer to mean and s.e.m. of PAR, expressed as percentage of the maximum recorded value (full light, 1171 μmol m² s^-1). See S8 Table for statistical analysis.

Fig 6. Yearly effects of Genista aetnensis on vegetation.

Time-dependency of the effects of Genista aetnensis ontogenetic stage on plant living biomass (top) and species richness (bottom) under (left) or outside (right) the canopy of Genista individuals. Data refer to mean and 95% confidence interval of data recorded in two surveys in the years 2010 and 2011 (N = 60 for each bar). Significantly higher time-dependent values within each ontogenetic stage are marked with an asterisk (Post-hoc Duncan test at p<0.05, interactions of year and ontogenetic stage from GLMs in S10 Table).