Plant invasion in forest ecosystems is a serious ecological and economic issue, deserving attention by researchers, managers and policy-makers worldwide. Many invasive plants have been reported as early successional species able to colonize disturbed areas following abrupt changes in microhabitat and resource availability. We investigated disturbance effects of a severe windstorm generated by a wet microburst (hail and rain at 160 mm h-1) remarkably affecting the canopy cover of an old-growth
Invasive, non-native species are regarded as one of the most serious issues from both an ecological and economic perspectives (
In forest ecosystems, plant invasion has drawn the attention of researchers, managers and policy-makers worldwide (
The fluctuating resource hypothesis states that an increase in unused resources enhances plant community susceptibility to biological invasion (
The availability of unused resources, such as soil nutrients, may be ascribed to either a decreased uptake by native species after disturbance events (
Natural disturbances such as windstorms, fires, floods and landslides play an important role in the structure and function of forest ecosystems (
Evidence of windstorm damages to forest ecosystems is widely reported for North America (
In this study, we investigated the disturbance effects of a stand-replacing windstorm generated by an extreme wet microburst in an old-growth, urban
The Gussone Park of the Royal Palace of Portici (40° 48′ 40.3″ N, 14° 20′ 33.8″ E, elevation 75 m a.s.l.; about 1 km distant from the coast line) hosts a 16.4 ha, even-aged old-growth evergreen holm oak Mediterranean forest, surrounded by a densely urbanized metropolitan area. Small preexisting canopy gaps and newly storm-generated gaps suggest that the dynamic of stand structure will shift from a monocohort to a more complex multi-cohort stand. The study site is located at the base of the south-western slopes of Mt. Vesuvius volcano at an elevation of 84 m a.s.l., facing the sea of the Gulf of Naples.
The holm oak (
A shallow soil with andic properties lays over pyroclastic deposits from eruptions of the Mount Vesuvius dated 1631 CE. The climate is Mediterranean, with humid winter and dry summer, total yearly rainfall of 929 mm (290, 200, 89 and 348 mm in winter, spring, summer, and fall, respectively), and mean monthly temperatures ranging between 11 °C (January) and 26 °C (August).
On 16 June 2014 at ~13:30 (CEST), a wet microburst, part of a large front of severe thunderstorms hitting the Tyrrhenian coastline of Southern Italy, moved from the Gulf of Naples towards the study site. The microburst generated irregular wind patterns with local speeds exceeding 100 km h-1 and hail and rain precipitations with intensity above 160 mm h-1.
Few days after the event, a field survey was carried out in the whole Gussone Park to assess the tree damage occurred in the forest. For all damaged trees (
In June 2015, one year after the windstorm event, we randomly selected 5 locations where disturbance occurred. A location consisted in a disturbed area with canopy gap and a control area under closed canopy. In each location, we estimated vascular species abundance within two paired adjacent plots of 10 × 10 m, one in the control area and the other in the disturbed one. Then, in each selected location two paired adjacent plots, the first under closed canopy and the other within the canopy gap (hereafter referred to as “control” and “disturbed area”, respectively). Plant species cover was visually assessed based on the following abundance scores: (1) rare; (2) <1%; (3) 1-5%; (4) 6-15%; (5) 16 -25%; (6) 26-50%; (7) 51-75%; (8) 76-100%. Plant specimens were identified according to
In mid-June 2015, we collected from the forest floor leaf litter using randomly positioned squared frames (10 × 10 cm). A total of 20 litter samples were collected, 2 in each of the previously selected area (5 disturbed and 5 control). Litter samples were placed in plastic bags, transported to the laboratory, and dried at 80 °C until reaching constant weight.
In the same areas, to assess the effects of disturbance on mineral nitrogen (N) availability, a total of 40 soil samples were randomly collected, away from uprooted trees, in summer (July) and autumn (October) 2015 (10 areas × 2 seasons × 2 samples). All samples (~1 kg each) were collected from the topsoil layer (0-20 cm), after removing the litter layer. Samples were packed in polyethylene bags, transferred to the laboratory within the sampling day and sieved at 2 mm, with subsequent quantification of the coarse (diameter >2 mm) and fine (diameter <2 mm) particle fractions. Soil samples for determination of nitrate (NO3-) and ammonium (NH4+) content were prepared by mixing 1 g of dry pulverized soil with 1 ml of distilled water in 2 ml Eppendorf tube. This mixture was shaken for 20 min and subsequently centrifuged for 5 min at 13.000 rpm. The samples were analyzed with a DR 3900 Spectrophotometer (Hach, Loveland, CO, USA) by using the manufacturer kits LCK 340 for NO3- and LCK 303 for NH4+.
Microclimate and soil moisture were monitored for one year (from December 9th, 2014 to December 9th, 2015) using two monitoring stations in either disturbed and control areas. Each station was equipped with an Em 50 data logger, two 5TM sensors for soil moisture content and temperature and one VP3 sensor for air temperature and relative humidity (all instruments from Decagon, Pullman, WA, USA). Air temperature/humidity sensors, protected by a radiation shield, were placed 10 cm above the ground. The two soil moisture and temperature probes were diagonally buried into the soil at -5 cm and -20 cm depths, respectively. No specific direct gravimetric measurements were performed for calibrating the relation between 5TM sensor responses and actual moisture content, because the sensors were installed for comparing relative changes over time by meteorological forcing in disturbed and control areas, rather than for retrieving absolute soil moisture values. Volumetric water content data were estimated according to the standard relation proposed by the manufacturer, certifying an accuracy of ± 3% for soils. The data loggers were programmed to store sensor data every 30 minutes over the whole monitoring period.
Photosynthetic photon flux density (PPFD, λ = 400-700 nm) was measured using a LI-250A light meter as quantum sensor (Li-Cor Inc. Environmental, Lincoln, Nebraska, USA), located at 0, 0.5, 1.0, and 2.0 m above the ground of 10 locations randomly selected within disturbed and control areas. Instantaneous measurements averaged every 15 seconds were taken during bright, sunny days in July 2014.
Tree data from disturbed and control areas were used to estimate tree density, above-ground biomass, basal area and mean height of standing and damaged trees, the latter separately assessed for uprooted and snapped trees. Gap data from aerial imagery were used to calculate gap-size frequency distribution. Species abundance scores were transformed in percent cover data, using the mean percent value for each ordinal class, and submitted to two-way factorial ANOVA including species, area (either disturbed or control) and their interaction as fixed factors. Species-specific differences between disturbed and control area were assessed by means of Duncan’s
Litter data were tested for significant differences between disturbed and control areas fitting a Generalized Linear Mixed Model (GLMM) with gaussian error distribution and identity link function, considering area and location as fixed and random factors, respectively. Further GLMMs were fitted to test differences of soil mineral N content, either NO3- or NH4+, between disturbed and control areas in summer and autumn, including fixed effects of area and season, and random effect of location where soil samples were collected. In all GLMMs, pairwise differences were tested by Duncan’s
Damages produced by the windstorm on the forest canopy were highly variable in space, as related to high spatial variability of the wind pattern generated by the microburst. Windstorm was stand-replacing on 1.53 ha (
Tab. S2 (Supplementary material) reports the number, dry biomass, basal area and quadratic mean diameter of the trees growing in the disturbed area selected for the vegetation analysis, before and after the windstorm. After the windstorm, about 65% of trees were uprooted in disturbed areas (Tab. S2). Above-ground dry biomass declined by ~87%. The quadratic mean diameter of the trees before the storm was 33.1 cm, while after windstorm it became 34.3 cm and 30.8 cm for uprooted and snapped trees, respectively.
Plant species cover was significantly affected by disturbance, with effects differing for different species (Tab. S3). Unconstrained ordination by PCA showed a distinct segregation of the plots according to disturbance (Fig. S1 in Supplementary material), with disturbed and control plots being positively and negatively correlated to the first ordination axis, respectively, and all invasive plant species showing positive scores on the same axis. Thirty-nine plant species were recorded in the plots surveyed, with 14 life forms overall representing 32 families (Tab. S4). Among these, 10 alien invasive plant species were recorded in the disturbed area, while the control area was not subject to plant invasion.
The amount of litter was significantly lower in disturbed areas compared to control ones (1745.31 ± 17.28 and 2496.88 ± 47.05 g m-2, respectively;
Microclimate, in terms of temperatures and moisture, exhibited a strong seasonality. Soil temperature was slightly warmer in the control area during winter months. Differently, from April to September mean daily temperature in the soil under the intact forest canopy was largely lower than that observed in the disturbed area (
Soil moisture exhibited a wet stage from October to May, followed by a relatively dry stage from June to September (
Expectedly, PPFD within the disturbed area was significantly higher than the control, with maximum relative difference recorded at ground level, where the PPFD exceeded that of the control area by one order of magnitude (
Abrupt environmental shifts produced by uprooted trees affected plant community recovery from the disturbance and recolonization within the gaps. In medium and large gaps, early colonizer species prevailed over pre-existing established herbs, lianas and tree seedlings. Noteworthy, one of the most obvious windstorm effects was the invasion of non-native species that occurred only in the disturbed plots. At the community level, the windstorm acted as a disturbance removing previously established vegetation and releasing space for new pioneer species. Such alien species spreading can be explained by two complementary factors: the increase of community invasibility and the high propagule pressure at the study site. With regard to the first factor, one year after the disturbance, micro-environmental conditions within the gaps showed higher temperature with larger diurnal and seasonal fluctuations, higher light flux-density at ground level, and higher soil moisture and nitrate nitrogen content compared to undisturbed understory. As a consequence, fast-growing, early colonizer species rooted in the gaps could benefit from favorable microclimatic conditions, at least during spring and early summer seasons, as well as from improved resource availability, compared to pre-disturbance conditions. Our data are consistent with the fluctuating resource hypothesis, which states that an increase in quantity of unused resources will enhance the susceptibility of a plant community to biological invasion (
The increased community invasibility, alone, cannot explain the increased abundance and diversity of alien species recorded in forest gaps after the windstorm. The burst of several herbaceous species (
The catastrophic windstorm of 16 June 2014 produced many gaps in the forest canopy caused by individual or neighborhood groups of tree falls, with gap size ranging from few square meters to more than 1600 m2. According to previous studies, gaps formed by the windstorm are characterized by greater light availability at ground level compared to closed canopy (
Among the possible environmental modifications induced by the windstorm, we showed a systematic modification of soil moisture regime within the gaps. The study area is characterized by a Mediterranean climate with alternation of cold-wet (autumn-winter) and hot-dry (spring-summer) seasons, with very short wet-to-dry and dry-to-wet transition stages. Several studies highlighted that Mediterranean summer drought establishes microclimatic conditions particularly severe for the regeneration of shrub and tree species (
The soil in gaps, in addition to higher moisture content, had higher nitrate nitrogen content compared to undisturbed areas. Our results are apparently contrasting with previous findings by
We showed that extreme windstorm events affect forest structure driving to sudden environmental shifts, such as modifications of micro-climatic conditions and soil resources. At the community level, windstorms can foster the spread of several invasive species, likely by removing the dominant evergreen tree
Plant cover percentage of native and invasive plant species within disturbed and control areas of the Gussone Park forest in June 2015, one year after the windstorm. Asterisks indicate significant difference for each species between disturbed and control areas (
Mineral nitrogen NO3- (upper panel) and NH4+ (lower panel) content in disturbed and control areas in summer (June) and autumn (October) 2015, following the windstorm of 16 June 2014. Values are average ± standard error of five replicates. Within each panel, different letters indicate significantly different groups (Duncan’s
Canopy effects on below-ground microclimate assessed by monitoring soil temperature and moisture from December 9, 2014 to December 9, 2015 in disturbed (red line) and control (black line) areas. Panels show daily soil temperature at -5 cm (A) and -20 cm (B) depths and soil moisture at the same depths (C and D, respectively). Grey shaded areas (bounded by red lines) highlight daily temperature ranges in the disturbed areas as compared to observations under the canopy in control areas (bounded by black lines).
Photosynthetic photon flux density (PPFD) in disturbed and control areas. Values are average ± standard error of ten replicates.
Fig. S1 - PCA biplot of species and plots.
Fig. S2 - Canopy effects on above-ground microclimate assessed by monitoring air temperature and relative humidity from December 9 2014 to December 9 2015 in disturbed and control areas.
Tab. S1 - Gap-size distribution in the study forest following the windstorm of 16 June 2014.
Tab. S2 - Forest stand attributes before and after (June 2015) the windstorm.
Tab. S3 - Results of two-way factorial ANOVA (F statistics and associated
Tab. S4 - List of plant species recorded in the disturbed and control areas.
Tab. S5 - Results of the GLMM testing for effects of the sampling area and location and their interaction on the amount of litter collected at the sampling site.
Tab. S6 - Results of the GLMM testing for the effects of sampling area , location and collection season on NO3- and NH4+ content in soil samples collected at the sampling site.