UNIVERSITÀ DEGLI STUDI DI TRIESTE
XXXIII CICLO DEL DOTTORATO DI RICERCA IN
AMBIENTE E VITA
Global changes in harsh environments:
effects on plant species and communities from a
trait-analysis perspective.
Settore scientifico-disciplinare: BIO/03
DOTTORANDO
STEFANO VITTI
COORDINATORE
PROF. GIORGIO ALBERTI
SUPERVISORE DI TESI
DOTT. VALENTINO CASOLO
CO-SUPERVISORE DI TESI
STATEMENT OF ORIGINAL CONTRIBUTION
This research thesis is an original contribution to the field of ecology and it is submitted as the final outcome of my Ph.D. project.
It focused on linking plant responses to global climate changes to harsh environmental conditions, which determine remarkable species responses, from cell to community level, by means of physiological and morphological plant responses.
I joined the Plant Biology Laboratory, Dipartimento di Scienze AgroAlimentari, Ambientali ed Animali (DI4A), University of Udine, Italy. My supervisor, Dr. Valentino Casolo, and co-supervisor Dr. Francesco Boscutti, always care for my work professionally, and their participation is revealed to be of fundamental relevance.
This dissertation contains the papers, and other related works, I produced during my Ph.D. program. According to my academic discipline (BIO/03 - ENVIRONMENTAL AND APPLIED BOTANY), it is divided into main works (Chapter 1, 2, 3, 4) and other minor works (n.2), as follow:
Chapter 1 Vitti, S., Pellegrini, E., Casolo, V., Trotta, G., & Boscutti, F. (2020). Contrasting responses of native and alien plant species to soil properties shed new light on the invasion of dune systems. Journal of Plant Ecology, rtaa052. doi: 10.1093/jpe/rtaa052;
Chapter 2 Boscutti, F., Vitti, S., Casolo, V., Roppa, F., Tamburlin,
ecosystem of the northern Adriatic Sea. Ecological Research, 34(2), 320– 327. doi: 10.1111/1440-1703.1070;
Chapter 3 Population density modulates the response of
morphological traits and non-structural carbohydrates in Vaccinum myrtillus when exposed to different rain regimes. Original draft, not submitted.
Chapter 4 Trifilò, P., Kiorapostolou, N., Petruzzellis, F., Vitti, S.,
Petit, G., Lo Gullo, M.A., Nardini, A. and Casolo, V. (2019). Hydraulic recovery from xylem embolism in excised branches of twelve woody species: Relationships with parenchyma cells and non-structural carbohydrates. Plant Physiology and Biochemistry, 139, 513–520. doi: 10.1016/j.plaphy.2019.04.013.
In addition to the above manuscripts, as previously said, other outputs have been presented at national - international conferences (for details see Appendix):
• Vitti, S., Boscutti, F., Pellegrini, E., & Casolo, V. (2018). Study of plant traits, soil features and plant invasion in sandy beach of Grado and Marano lagoon (northern Adriatic Sea). 113° Congresso della Società Botanica Italiana - V International Plant Science Conference (IPSC). abstracts keynote lectures, communications, posters. Università di Salerno, Fisciano (SA). 978-88-85915-22-0. abstracts keynote lectures, communications, posters. Fisciano (SA): Università di Salerno.
ACKNOWLEDGEMENTS
My most important thank goes to my supervisor, Dr. Valentino Casolo, and my co-supervisor, Dr. Francesco Boscutti, for being always helpful, professional, respectful, and full of wise advice, giving me a warm welcome to their research group.
They taught me much about botany and ecology, also permitting me to discover fantastic unknown places during field activities.
I thank the staff of Friuli Venezia Giulia Region for the administrative support, Dr. Glauco Vicario, and Dr. Stefano Sponza for field logistic support.
I thank my office-mate, Antonio and Marco, particularly for recreational moments. They are really funny guys.
FOREWORD
Climate is the average of the weather conditions at a particular point on the Earth, and it is expressed in terms of expected temperature, rainfall, and wind conditions based on historical observations (Riedy 2016).
The Earth’s climate has always changed and the history of life on Earth is closely associated with environmental change on multiple spatial and temporal scales (Davis 2001).
The success of human societies depends mainly on the living components of systems (Pecl et al. 2017). In the case of environmental conditions changes, for marine, freshwater, and terrestrial species, the first response is often a shift in location, to stay within ecologically optimal environmental conditions (Chen et al. 2011; Lenoir and Svenning 2015). At the cooler extremes of their distributions, species are moving poleward, whereas range limits are contracting at the warmer range edge, where temperatures are no longer tolerable. On land, species are also moving to cooler, higher elevations; in the ocean, they are moving to colder water at greater depths (Pecl et al. 2017).
Species are affected by climate in many ways, including range shifts, changes in relative abundance, and changes in activity timing and microhabitat use (Williams et al. 2008; Bates et al. 2014) and the geographic distribution of any species depends upon its environmental tolerance, dispersal constraints, and biological interactions with other species (Peterson
et al. 2011).
TABLE OF CONTENT
STATEMENT OF ORIGINAL CONTRIBUTION _________________________ - 3 - AKNOLEDGEMENTS _______________________________________________ - 6 - FOREWORD _______________________________________________________ - 8 - INTRODUCTION __________________________________________________ - 13 -
Climate change and effects of plants in a changing precipitation scenario ________ 13 Biological invasion: invasion mechanisms in harsh environments _______________ 15 Effects of biological interactions ___________________________________________ 17
-THESIS’ AIMS ____________________________________________________ - 19 - THESIS’S STRUCTURE ____________________________________________ - 20 - CHAPTER 1_______________________________________________________ - 23 -
Contrasting responses of native and alien plant species to soil properties shed new light on the invasion of dune systems ___________________________________________ 23
-CHAPTER 2_______________________________________________________ - 61 -
Seagrass meadow cover and species composition drive the abundance of Eurasian wigeon (Mareca penelope L.) in a lagoon ecosystem of the northern Adriatic Sea ___ 61
-CHAPTER 3_______________________________________________________ - 87 -
Population density modulates the response of morphological traits and non-structural carbohydrates in Vaccinum myrtillus when exposed to different rain regimes _____ 87
-CHAPTER 4______________________________________________________ - 120 -
Hydraulic recovery from xylem embolism in excised branches of twelve woody species: relationships with parenchyma cells and nonstructural carbohydrates _________ 120
-CONCLUSIONS __________________________________________________ - 155 - APPENDIX ______________________________________________________ - 159 -
Study of plant traits, soil features and plant invasion in sandy beach of Grado and Marano lagoon (Northern Adriatic Sea) ___________________________________ 160 -Seagrass - waterbirds interactions in a lagoon ecosystem of the Northern Adriatic Sea_ - 164
“It is not the strongest of the species that survives,
nor the most intelligent that survives.
It is the one that is the most adaptable to change.”
Charles Robert Darwin
INTRODUCTION
Climate change and the effects of plants in a changing precipitation scenario
Although it appeared on Earth relatively recently, man has affected most of the biosphere by means of its activities.
Since the beginning of the industrial revolution, in England in the late 18th
century, pollution due to human activities has been steadily increasing across the world. After the Second World War, there was an acceleration of this phenomenon: technological development has led to the introduction of new materials and production processes, and many of which have led to new eco-toxicological risks.
Climate change is the persistent change in the weather pattern, and one of the major drivers of climate change is global warming (Mgbemene 2011), mainly caused by the emission of greenhouse gases such as carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O), chlorofluorocarbons and
other chemicals into the atmosphere (Hecht 2007). Climate change is widely acknowledged as a primary environmental problem of the Planet (Zhai and Helman 2019).
Arctic snow and ice have contributed to the Arctic amplification, which corresponds to a warming rate more than twice that in the other regions (Manabe and Wetherald 1975); in the Amazon region, more than 20% of the rainforests has been destroyed in the past decades (Davidson et al. 2012), causing changes in hydroclimatic regimes (von Randow et al. 2004; D’Almeida et al. 2007; Lawrence and Vandecar 2015). In the ‘80s deforestation caused thermally triggered atmospheric circulations(Roy 2002), with an increase in regional cloudiness (Negri et al. 2004) and precipitation frequency (Chagnon 2005); in West Africa (Niger, Senegal, and Gambia) climate changes influenced evapotranspiration rates, temperatures and rainfall regimes (Abdelkrim 2013), with a consequent impact on water availability given by a reduction in rainfall (Mahé and Olivry 1995).
In Europe, the Mediterranean basin is one of the most vulnerable climate change hotspots (Giorgi 2006), indeed it responds quickly to atmospheric forcings (Lionello 2012). In terms of the thermal regime, according to the IPCC’s model, the base scenario from 1980-2000 was used to estimate an increase in average surface temperatures (2.2-5.1 °C) in this century (2080-2100). For the same period, the models indicate rainfall regime and estimate that precipitation over lands might vary between -4% and -27%.
Many studies existing on the consequences that climate change could produce on species distribution and habitat. All this research indicates that a serious alteration of biological and ecological patterns in both marine and terrestrial biomes is already taking.
As above reported, the Arctic region has warmed, in the last decades and the warming ratio is more than twice of the rest of the Earth (IPCC 2013; Post
et al. 2019): as the Arctic warms, vegetation is responding. One of the most
et al. 2015) state that, tundra vegetation changes in response to the warming
effect, and this change (called ‘greening of the Arctic’) was recognized as the world’s most important ecological responses to global climate change, on large-scale (Myers-Smith et al. 2020).
Arctic vegetation is mainly composed of life forms more adapted to harsh conditions, e.g. dwarf shrubs, that replaced trees at high latitudes or high elevations. This vegetation replacement is highlighted by the treeline; it can be interpreted as the boundary of the forest, although it is usually not a distinct line (Grace 2002). It is so ecologically relevant to be monitored in every part of the Earth (Tranquillini 1979; Beneke and Davis 1980; Alden et
al. 1993; Holtmeier 2000).
In consideration of this, the study of plant response, both from a morphological and physiological point of view, to several and extreme environmental stresses may be crucial in forecasting further climate scenarios (Filippi et al. 2020).
Biological invasion: invasion mechanisms in harsh environments
Plant invasions are known to be favored by humans, both directly (species introductions) and indirectly (anthropogenic alterations of the environment) (Thuiller et al. 2006; Pysek et al. 2010). In Europe, the increase of human activities, especially in coastal areas, caused habitat loss (Heslenfeld et al. 2008) and also the introduction of many alien plants (Campos et al. 2004a; Carboni et al. 2010).
In terms of biodiversity of species and habitat, coastal areas are globally considered among the most valuable but endangered environments, due to their susceptibility to global changes (Defeo et al. 2009).
Open sandy coasts comprise up to 40% of the world's coastline (Bird 1996) which is subject to a very high level of human utilization. Sandy coasts can be divided into mainland and barrier island coasts, with some operating physical processes being common to both types of coasts (e.g. storm erosion, coastline recession, spit/barrier breaching due to elevated water levels) and some others being specific to one coast type or the other (e.g. seasonal closure of small tidal inlets on mainland sandy coasts; barrier rollover on barrier island coasts) (Ranasinghe 2016).
Among coastal systems, dune has been already proved to be particularly prone to biological invasion (Campos et al. 2004a; Giulio et al. 2020), which leads to major shifts in biodiversity, ecosystem integrity, functions, and services (Vilà et al. 2011; Simberloff et al. 2013).
scale (Kron 2013; Hinkel et al. 2013; Johnson et al. 2015; Brown et al. 2016).
Coastal dunes, occupying transition zones between terrestrial and marine ecosystems, constitute one of the most dynamic landscapes on earth (Carranza et al. 2008; Carboni et al. 2009). In particular, Mediterranean coastal dunes host a highly specialized flora (European Commission. Directorate General for the Environment. 2016) along a well-known vegetation zonation which is similar to the Mediterranean coastline (Acosta
et al. 2009). During recent decades along the Mediterranean basin, outbound
tourism, the expansion of urban areas, and the spread of agriculture have strongly shaped coastal landscapes (Hesp and Martínez 2007; Malavasi et al. 2013).
Effects of biological interactions
To predict an ecological response to climate change we base our studies on direct climatic effects on species (Suttle et al. 2007) and the impacts of recent climate change on life on Earth are already evident.
Both biotic factors, i.e. species properties and interactions, and abiotic factors, i.e. climate and soil characteristics, may affect ecosystem structure and their processes (Loreau 2001) and shape community composition (Bray
et al. 2019). Global warming can lead to a modification in abiotic conditions
that influence plant performance, with a particular inclination of alpine and arctic ecosystems to be affected (Callaghan and Jonasson 1995) and it may alter soil moisture and nutrient availability.
THESIS’ AIMS
This Ph.D. work aimed to investigate the effects of global changes, analyzing the effects of changing climatic factors, to plant ecosystems achieving precise information to understand and better explain global changes in harsh environments, searching for a link between plant metabolism and communities. Another aim was to add knowledge on how plants respond to extreme climatic treatments.
The contribution of the following reported article gives help in understanding how changing climatic factors and environmental parameters can affect plant ecosystems.
Two different approaches were applied: i) morphological and physiological plant traits analysis, ii) and plant communities’ analysis
THESIS’S STRUCTURE
This dissertation is composed of 4 chapters:
Chapter 1 Vitti, S., Pellegrini, E., Casolo, V., Trotta, G., & Boscutti, F. (2020). Contrasting responses of native and alien plant species to soil properties shed new light on the invasion of dune systems. Journal of Plant Ecology, rtaa052. doi: 10.1093/jpe/rtaa052; this is the last submitted contribute to plant ecology and alien species. Plant communities mainly, and also soil cores, were analyzed along the sea – inland - saltmarsh gradient.
Chapter 2 Boscutti, F., Vitti, S., Casolo, V., Roppa, F., Tamburlin,
D., & Sponza, S. (2019). Seagrass meadow cover and species composition drive the abundance of Eurasian wigeon (Mareca penelope L.) in a lagoon ecosystem of the northern Adriatic Sea. Ecological Research, 34(2), 320– 327. doi: 10.1111/1440-1703.1070; this is a contribution to plant – animal interaction, where we studied the interactions between primary producers and consumers, which plays an important role in the conservation of sensitive ecosystems such as lagoons.
Chapter 3 Population density modulates the response of
morphological traits and non-structural carbohydrates in Vaccinum myrtillus when exposed to different rain regimes. Original draft, not submitted. We analyzed the relationships between NSC, plant traits, rain exclusion, and shrub density to determine the response of alpine Vaccinium myrtillus stands to climate variation.
Chapter 4 Trifilò, P., Kiorapostolou, N., Petruzzellis, F., Vitti, S.,
carbohydrates. Plant Physiology and Biochemistry, 139, 513–520. doi: 10.1016/j.plaphy.2019.04.013; the last one is a contribution to plant physiology, from a collaboration between Prof. Patrizia Tifilò, University of Messina, and my supervisor, Dr. Valentino Casolo. We investigated the embolism repairation ability on 12 broadleaved species differing in vulnerability to xylem embolism.
CHAPTER 1
Contrasting responses of native and alien plant species to soil
properties shed new light on the invasion of dune systems
Stefano Vitti1,2,*, , Elisa Pellegrini2,3, Valentino Casolo2, Giacomo Trotta2 and
Francesco Boscutti2,
1Department of Life Sciences, University of Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy, 2Department of Agricultural, Food,
Environmental and Animal Sciences, University of Udine, via delle Scienze 91, Udine 33100, Italy,
3Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 København Ø, Denmark
*Corresponding author. E-mail: stefano.vitti@phd.units.it
Handling Editor: Bin Zhu
Citation: Vitti S, Pellegrini E, Casolo V, et al. (2020) Contrasting responses
of native and alien plant species to soil properties shed new light on the invasion of dune
systems. J Plant Ecol XX:XX–XX. https://doi.org/10.1093/jpe/rtaa052
Abstract
Aims Among terrestrial ecosystems, coastal sandy dunes are particularly
focusing on the interplay between soil nutrients, soil salinity and plant functional traits.
Methods Study sites were sandy barrier islands of the Marano and Grado
lagoon (northern Adriatic Sea). One hundred plots of 16 m2 have been
randomly selected in three habitats (foredune, backdune and saltmarsh). In each plot, we recorded all plant species occurrence and abundance and we collected a soil core. For each soil sample, soil texture, conductivity (as proxy of soil salinity), organic carbon and nitrogen content were analysed and related to the species number and cover of native and alien plants. Variation of main reproductive and vegetative functional traits among habitats was also analysed for both alien and native species.
Important Findings Soil properties were strongly related to overall plant
diversity, by differently affecting alien and native species pools. In backdune, the most invaded habitat, a high soil conductivity limited the number of alien species, whereas the content of soil organic carbon increased along with alien plant abundance, suggesting also the occurrence of potential feedback processes between plant invasion and soil. We found a significant convergence between native and alien plant functional trait spectra only in backdune habitat, where environmental conditions ameliorate and plant competition increases. Our findings suggest that in harsh conditions only native specialized plants can thrive while at intermediate conditions, soil properties gradient acts in synergy with plant traits to curb/facilitate alien plant richness.
Keywords: invasive alien species, functional traits, soil nutrients, plant
Introduction
Coastal areas are globally considered among the most valuable but endangered habitats due to their susceptibility to global changes (Defeo et al., 2009). Among coastal systems, dune has been already proved to be particularly prone to biological invasion (Campos et al., 2004; Giulio et al., 2020), which leads to major shifts in biodiversity, ecosystem integrity, functions and services (Vilà et al., 2010; Simberloff et al., 2013).
In dune systems, many studies focused on the relationships between invasive plants and regional environmental variables (Marcantonio et al., 2014; Malavasi et al., 2014; Tordoni et al., 2018; Marzialetti et al., 2019). However, while land-use and climate are considered pivotal at large-scale (i.e. landscape), variations of soil and stand structure might prevail when considering the local spread of alien species in semi-natural habitat (Ohlemüller et al., 2006). Soil features are supposed to directly affect the success of exotic plants in introduced habitats (Carvalho et al., 2010). Among soil properties, nutrient content and organic matter are known as important determinants of plant community diversity (Chapin III et al., 1986). For instance, high levels of soil nitrogen increase the abundance of invasive alien plants and decrease plant diversity (Vitousek et al., 1997). On the other hand, some invaders can trigger cascading effects on ecosystem proprieties by altering nutrient cycles (Boscutti et al., 2020). In coastal systems, soil salinity is the major driver of species distribution (Donnelly and Pammenter, 1983; Gorham, 1992; Lortie and Cushman, 2007). Nonetheless, the effect of salinity on the distribution of invasive species was studied only for few specific alien taxa, focusing on their phenotypic response to salt stress (Ishikawa et al., 1991; Caño et al., 2016).
functional response of plants (Boscutti et al., 2018a; Pellegrini et al., 2018; Bu et al., 2019). In turn, the range of functions provided by a plant community is thought to largely depend on the diversity of functional traits (Dı́az and Cabido, 2001), expressed as global variability of functional traits (functional spectrum). For these reasons, plant functional traits have been proved to be pivotal in elucidating plant invasion success (Rejmanek and Richardson, 1996; Boscutti et al., 2018b). In particular, plasticity of plant traits are supposed to affect the success of alien plants (Davidson et al., 2011) by producing a divergence/convergence of plant traits in response to the invaded habitat conditions (e.g. Marchini et al. 2019). In fact, invasive species are supposed to be more tolerant to environmental stresses (Alpert et al., 2000; Antunes et al., 2018), showing a general higher phenotypic plasticity than native species (Feng et al., 2007; Raizada et al., 2009).
In this observational study, we aimed at parsing the relationships between native and alien plants and soil properties (i.e. soil conductivity, soil nutrients) in three main habitats of coastal dune systems, i.e. foredune, backdune and saltmarsh. In addition, the variation of important reproductive and vegetative functional traits for both alien and native species were considered. In particular, we hypothesized that:
(i) low soil conductivity (i.e. less salt content) favours the abundance and richness of alien species in each considered habitat;
(ii) soil nutrients increase along with alien species abundance;
Materials and methods
Study site and plant communities
The study sites were the barrier islands of the Marano and Grado lagoon (from 45°42’10.5’’N 13°9’17.8’’ E to 45°40’49.8’’N 13°21’31.2’’ E), located in the northern part of the Adriatic Sea (Friuli Venezia Giulia region, Italy) (Fig. 1.1a-b). The lagoon is included in the Natura 2000 network, recognized both as Special Area of Conservation (SAC) and Special Protection Area (SPA). The mean annual rainfall is 974 mm. The driest month is July. The mean lowest temperature is in January; with a value of 3.1°C; the mean highest temperature is in July, with a value of 29.0°C. Wind average speed ranges from 7.8 to 10.4 km/h.
and consequently on soil nutrient availability. Despite many saltmarshes are estuarine, they can also be found associated with barrier islands, usually due to wash over events that brake the sand barrier and leads to the deposit of fine soil particles just behind dunes (Fontolan et al., 2012).
Sampling design
Along the islands shore we identified a total of 10 areas (ca. 5 ha each). Each area represented the described ecological gradient including the 3 main habitats of our interest (i.e. foredune, backdune and saltmarsh). Ten points were randomly selected within each of the 10 previously selected areas (see Fig. 1.1c as example), giving overall 100 points: 32 points for foredune, 40 for backdune and 28 for saltmarsh. In each point, plant communities and soil were surveyed.
Data collection Plant community
At each point, a sample area (plot) of 16 m2 (4x4 m) was established. Within
Soil
Within each plot, a soil sample was collected using a cylindrical tube (height: 12 cm, width: 3.5 cm, volume: 115.5 cm3), transported to the lab and stored
at 4°C. Soil samples (n=100) were afterwards homogenized and divided into two aliquots. The first aliquot was air-dried, sieved at 2 mm and ball-milled for the further chemical analysis of soil organic carbon (C) and nitrogen (N), while the second aliquot was stored at 4°C in plastic bags for the analyses of conductivity and granulometry.
Soil organic carbon and nitrogen content were measured on a set of subsamples using a CHNS Elemental Analyser (Vario Microcube © Elementar). Before analysis, all soil samples were treated with HCl to remove the carbonate fraction.
Conductivity was measured in 5:1 extract using about 10 g of dry soil and 50 mL of water. The solution was shacked for 2 hours and filtered using a Whatman n°42 filter paper. Conductivity was measured in the filtered solution using the CM35+ portable conductivity meter (Crison).
The Bouyoucos method was applied to determine granulometry. A small amount of soil was used to determine soil humidity. About 50 g of corresponding dry soil was treated with 100 ml of sodium hexametaphosphate (SHMP). The extract (1:2) was shacked for 2 hours and then pour in a Bouyoucos’ cylinder, where density was measured with the hydrometer ASTM 152H after 4 minutes and 2 hours (silt plus clay and only clay, respectively).
Data analysis
For each plot, we calculated species richness (number of species) and abundance (sum of species cover) of the overall, native and alien pools of species, respectively. Since the ranges of native and alien species richness and abundance were very different, we standardized species richness and abundance (z-scores) within each status level.
Differences between habitat in terms of overall and status-pooled species richness were tested using linear mixed-effects models (LMMs), considering the id of the 5 ha surveyed area (i.e. area id) and sub replicates for the status (i.e. plot id) as random effects. A Tukey pairwise test was then applied to detect significant differences between habitat and status (native or alien) interaction (p<0.05). LMMs were applied with the “nlme” package (Pinheiro et al., 2019), pairwise comparisons were performed with the ‘multcomp’ R package (Hothorn et al., 2008).
The random effects of the 5 ha surveyed area (i.e. area id) and sub replicates for the status (i.e. plot id) were included. Given the non-linear relationship between independent variable and dependent variables, the models were linearized by logarithmic transformation as best solution after considering the inclusion of a quadratic term. Multi-model inference compared the fit of all possible models obtained by the combination of the variables. We used Akaike’s information criterion (AIC) to choose the best fitting model. The best fit is indicated by the lowest AIC value (AIC MIN). In a set of models each model i can be ranked using its difference in AIC score to the best-fitting model (Δ AICi = AICi- AICi MIN). A model in the set can be considered plausible if its Δ AIC is below 2 (Burnham and Anderson 2002).The multi-model inference based on AIC was executed using the ‘MuMIn’ package (Barton, 2015). The LMMs were applied using the “nlme” package (Pinheiro et al., 2019).
Results
Plant diversity, habitat and alien plant invasion
The total number of species within the 100 surveyed plots was 97 (73 native and 24 alien) (Appendix S1.1). The most common native species were Cakile
maritima Scop., occurring in 38% of the overall number of plots, Elymus acutus (DC.) M.A. Thiébaud (29 %), Limonium narbonense Mill. (28 %) and Limbarda crithmoides (L.) Dumort. (28%). Among the alien species, the
most frequent were Sporobolus pumilus (Roth) P.M. Peterson & Saarela (50 %), Xanthium italicum Moretti (35 %), Ambrosia psilostachya DC. (34%) and Oenothera biennis L. aggr. (30 %).
The average species number found in each plot was 7.8 ± 3.1 (mean ± standard deviation). Species richness was significantly different among habitats (F2-88 = 8.34, p < 0.001), where foredune (7.7 ± 3.23) and backdune (9.2 ± 2.7) had significant higher values than saltmarsh (5.7 ± 2.3) (p < 0.05). A significant interaction was found between habitat and status (i.e. alien vs native) (F2-97 = 18.7, p < 0.001). Differences between native and alien standardized species richness (hereafter species richness) were significant in saltmarsh and backdune where native species showed higher values (Fig. 1.2).
Relationships between plant invasion and soil features
Multi-Model Inference analysis showed that species richness of alien and native plants were related to soil features by only one plausible model (Δ AIC < 2), which included soil conductivity, soil nitrogen content and the interactions with species status and habitat for the conductivity, and with habitat, for the soil nitrogen (Table 1.1; R2=0.51).
with soil conductivity, native species showed a stronger increase respect to aliens (Fig. 1.3a). In backdune, native species number increased when conductivity increased, whereas alien species number decreased (Fig. 1.3b). In saltmarsh, the number of specie was not correlated with soil conductivity (Fig. 1.3c).
High values of nitrogen content in the soil increased the overall number of species in foredune, while decreasing it in saltmarsh (Fig. 1.3d). Finally, in backdune, the number of both native and alien species was not affected by soil nitrogen (Fig. 1.3e).
We also analysed the effect of conductivity, soil organic carbon and total nitrogen on the abundance of species (species overall cover) in relation to each status and habitat. Multi-model inference analysis showed that only one model was plausible (Δ AIC < 2) and it included all considered interactions (Table 1.2), explaining the 48% of the total variation in species abundance. High soil conductivity favored native species abundance in both foredune and backdune (Fig. 1.4a, b), whereas plant cover was not related to soil conductivity in saltmarsh (Fig. 1.4c).
Soil organic carbon content was positively related to alien overall cover in both foredune and backdune, whereas native plant abundance decreased with increasing content of soil organic carbon, but only in backdune (Fig. 1.4e). In saltmarsh, species abundance was not affected by soil organic carbon content (Fig. 1.4f).
Functional convergence
We found a significant difference between native and alien plant functional trait spectrum (distance) (PERMANOVA: r2 = 0.09, p = 0.001), in different
habitats (r2 = 0.14, p = 0.001) and their interaction was significant as well (r2
= 0.06, p = 0.001). Interestingly, we found a functional convergence (similarity) between alien and native species pool only in backdune habitat, which was also the most invaded. On the other hand, functional traits variation (dispersion) did not differ between species status, habitat and their interactions (p > 0.05) (see online Supplementary Material, Fig. S1.2).
Discussion
Plant diversity, habitat and alien plant invasion
Alien species represented the 25% of the total species richness in the studied dune system, much higher than the frequency of alien taxa at regional (16%) and national (12%) scale (Galasso et al., 2018); hence confirming that coastal dunes are one of the most invaded habitat by neophytes at the European level (Chytrý et al., 2008).
Saltmarsh showed an overall low plant diversity, similar to what found by Kunza and Pennings (2008), but also harbored a low number of alien species. In this habitat, flooding, sediment anoxia and salt create extremely harsh conditions (Redelstein et al., 2018), difficult to cope for generalist plants. Only few adapted species thrive in this habitat and their response to the environment can indirectly ameliorate pant community condition and overall plant diversity (Redelstein et al., 2018; Pellegrini et al., 2018).
habitats such as inland agricultural land-use and semi-natural grasslands (Marcantonio et al., 2014).
Relationships between plant invasion and soil features
Among the analysed soil features, soil conductivity (i.e. salinity), organic carbon and nitrogen content showed significant relationships with plant species abundance and diversity, with contrasting trends between alien and native plants, especially in backdune habitat. Soil conductivity have been proved to affect plant distribution in coastal dunes (Ishikawa et al., 1995) and altering the interactions between native and alien species (Wang et al., 2006). Moreover, many alien species are supposed to be less competitive than native species in relation to salt stress (Mesléard et al., 1993; Borgnis and Boyer, 2016). Salt content create harsh condition principally by reducing water availability and increasing osmotic stress. On sandy soils, this is exacerbated by the high soil porosity and thus water drainage. In these conditions, native adapted species thrive better than alien (Antunes et al., 2018). In contrast, a previous study showed that alien species richness increased in sites with high rainfall, as a consequence of a higher soil water availability and salt leaching.
We found that nitrogen and organic carbon soil content (i.e. overall representing also organic matter content) were mainly involved in explaining plant abundance of alien and native species. The relationships between nitrogen and carbon soil content and species abundance were stronger in backdune, while in the harsher environments the other drivers (e.g. waterlogging, salinity, wave action, storms disturbance) seem to overrule on such effects. In backdune, a high content of nitrogen increased along with the abundance of native species, but not with the abundance of alien species. It is thought that plant invasion is favored by high content of nitrogen, triggering positive feedback between plant invasion and carbon and nitrogen cycles in invaded ecosystems (Liao et al., 2008). Our findings, instead, support the idea that in very poor soils native rather than alien species can intercept such nutrient resources and increase their abundance.
However, we cannot exclude the aftereffect of the overall plant abundance (biomass) accumulating in a more stable habitat less subjected to wash over events.
mechanism between soil and plants, opening future experimental perspectives.
Functional convergence
Plant trait analysis is a methodological approach to better understand the processes linked to alien species invasion (Richardson et al., 2000; Richardson and Pyšek, 2006). Stressed plant communities are mainly ruled by habitat filtering, whereas functional convergence is mainly related to this ecological process (Cornwell et al., 2006). When different plant species are co-existing in the same community, it is usual for species to show some morphological and functional similarities (Grime, 2006; de Bello et al., 2009). Environmental filtering can contribute to community’s similarity and the result of this process is functional redundancy for species traits inside a community (Cornwell et al., 2006). Our findings suggest the presence of an overlap of niche between native and alien species and a potential substitution of native species in the most invaded habitat, namely the backdune. Kowarik (2008) explains that changes in environmental factors can generate a more efficient niche invasion by alien species, rather than favor native species. In fact, this mechanism is known to be more effective where environmental conditions are not extremely harsh (Carboni et al., 2010). In these conditions, we can hypothesize that less specialized alien species are favored to invade dune ecosystem due to ecosystem characteristic which present a higher similarity to human-disturbed habitats (e.g. urban sites or agricultural) where the alien species commonly thrive (Kowarik, 2008).
evolved to specialized species and only few alien species are suitable to colonize these areas (Marcantonio et al., 2014).
Conclusions
Our findings suggest that main soil properties and plant functional traits are related to the plant invasion across the shore-saltmarsh gradient in barrier islands. The initial hypotheses were supported by our results, showing that soil conductivity curb both abundance and specific richness of alien species, favoring the presence of native species. Moreover, nitrogen and organic carbon in soil were related to plant with particular regard to plant abundance, underpinning plausible feedback mechanisms between plant and soil which understanding would need specific experimental approach. The magnitude of the effect is habitat specific: while backdune are the most sensitive habitat, foredune and saltmarsh were mostly unaffected by plant invasion and regardless to soil feature gradients. Finally, the higher invasion of backdune was consistent with a functional convergence between alien and native species pool.
Funding
This work was supported by Regione Autonoma Friuli Venezia Giulia and University of Udine [grant number Morphological and environmental study of the Marano and Grado Lagoon CUP D26D14000230002].
Acknowledgements
We thank the staff of Friuli Venezia Giulia Region, Marano Lagunare municipality for field logistic support and for their assistance. In particular Dr. Glauco Vicario and Dr. Stefano Sponza for the valuable logistic assistance. The authors have no conflicts of interest.
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Tables
Table 1.1: Results of the linear mixed-effects models relating standardized
species richness with habitat (i.e. foredune, backdune and saltmarsh), species status (i.e. alien and native), soil conductivity (cond), soil nitrogen content (N) and the interactions between species status, habitat and soil conductivity, nitrogen content and habitat type. Degrees of freedom (DF), F-value and p-value are reported. In bold are indicated the significant outcomes (p<0.05).
Table 1.2: Results of the linear mixed-effects models relating the
standardized species abundance with habitat (i.e. foredune, backdune and saltmarsh), species status (i.e. alien and native), soil conductivity (cond), soil nitrogen content (N), soil organic carbon (C) and the interactions between species status, habitat and soil conductivity, nitrogen content, organic carbon content and habitat type. Degrees of freedom (DF), F-value and p-value are reported. In bold are indicated the significant outcomes (p<0.05).
Figures
Figure 1.1: location of the study area in the lagoon of Marano and Grado in
Figure 1.2: differences in standardized species richness between status
Figure 1.3: effects of soil conductivity (a, b, c) and soil nitrogen (d, e, f) on
Figure 1.4: effects of soil conductivity (a, b, c), organic carbon content in
Supplementary Material
Figure S1.1: correlation plot between soil features. Statistically highly
Figure S1.2: Principal Coordinates Analysis (PCoA) applied to functional
Appendix S1.1: Species list. For each taxon the status (alien= A, native= N)
and relative frequency (in percentage) in each habitat and overall are reported.
Frequency (%)
Species Status Foredune Backdune Saltmarsh Overall
Abutilon theophrasti Medik. A 3.1 0 0 1
Ailanthus altissima (Mill.)
Swingle A 0 2.5 0 1
Amaranthus retroflexus L. A 3.1 0 0 1
Ambrosia psilostachya DC. A 25 62.5 3.6 34
Amorpha fruticosa L. A 3.1 27.5 0 12
Aristolochia rotunda subsp.
rotunda L. N 0 2.5 0 1
Arthrocaulon macrostachyum
(Moric) Piirainen & G.Kadereit N 0 0 17.9 5
Arundo donax L. A 0 5 0 2
Asparagus maritimus (L.) Mill. N 0 12.5 0 5
Atriplex patula L. N 9.4 2.5 0 4
Atriplex rosea L. N 40.6 10 7.1 19
Avena barbata Pott ex Link N 0 7.5 0 3
Bryonia dioica Jacq. N 0 2.5 0 1
Cakile maritima subsp.
maritima Scop. N 93.8 20 0 38
Calamagrostis arenaria (L.)
Roth N 12.5 2.5 0 5
Calamagrostis epigejos (L.)
Roth N 0 10 3.6 5
Carex extensa Gooden N 3.1 17.5 21.4 14
Cenchrus longispinus (Hack.)
Fernald A 3.1 0 0 1
Centaurea tommasinii A.Kern. N 0 5 0 2
Cerastium pumilum Curtis N 0 5 0 2
Chenopodium album L. N 21.9 2.5 0 8
Convolvulus sepium L. N 0 2.5 0 1
Convolvulus soldanella L. N 0 10 0 4
Crepis foetida L. subsp.
rhoeadifolia (M.Bieb.) Čelak. A 0 10 0 4
Cuscuta cesattiana Bertol. N 40.6 12.5 0 18
Cycloloma atriplicifolium
Frequency (%)
Species Status Foredune Backdune Saltmarsh Overall
Cynodon dactylon (L.) Pers. N 6.3 0 0 2
Cyperus capitatus Vand. N 9.4 7.5 0 6
Cyperus esculetus L. A 25 7.5 0 11
Dactylis glomerata L. N 3.1 30 0 13
Diplotaxis tenuifolia (L.) DC. N 0 2.5 0 1
Elymus acutus (DC.) M.A.
Thiébaud N 40.6 25 21.4 29
Elymus farctus (Viv.)
Runemark ex Melderis N 25 15 0 14
Erigeron annuus (L.) Desf. A 0 2.5 0 1
Erigeron canadensis L. A 12.5 42.5 0 21
Eryngium maritimum L. N 18.8 7.5 0 9
Festuca fasciculata Forssk. N 12.5 10 0 8
Fumaria officinalis L. N 0 2.5 0 1
Galatella pannonica (Jacq.)
Galasso, Bartolucci & Ardenghi
N 0 0 28.6 8
Helianthemum nummularium
(L.) Mill. N 0 2.5 0 1
Helianthus annuus subsp.
annuus L. A 6.3 0 0 2
Juncus acutus subsp. acutus L. N 3.1 7.5 17.9 9
Juncus littoralis C.A.Mey. N 0 2.5 3.6 2
Juncus maritimus Lam. N 0 5 32.1 11
Lagurus ovatus L. N 9.4 2.5 0 4
Lepidium virginicum subsp.
virginicum L. A 0 2.5 0 1
Limbarda crithmoides (L.)
Dumort. N 21.9 10 57.1 27
Limonium bellidifolium
(Gouan) Dumort. N 0 5 3.6 3
Limonium narbonense Mill. N 0 2.5 96.4 28
Limonium virgatum (Willd.)
Fourr. N 0 5 7.1 4
Medicago littoralis Loisel. N 0 2.5 0 1
Medicago marina L. N 3.1 0 0 1
Oenothera biennis L. aggr. A 18.8 60 0 30
Panicum capillare L. A 12.5 25 0 14
Parapholis incurva (L.)
C.E.Hubb. N 12.5 2.5 0 5
Frequency (%)
Species Status Foredune Backdune Saltmarsh Overall
Phleum arenarium L. subsp.
caesium H.Scholz N 9.4 10 0 7
Phragmites australis subsp.
australis (Cav.) Trin. ex Steud. N 3.1 10 17.9 10
Plantago coronopus L. N 0 12.5 0 5
Poa annua L. N 0 2.5 0 1
Poa trivialis L. N 0 5 0 2
Polypogon maritimus Willd. N 9.4 2.5 0 4
Polypogon viridis (Gouan)
Breistr. N 0 2.5 0 1
Portulaca oleracea L. N 3.1 0 0 1
Poterium sanguisorba L. N 6.3 25 0 12
Puccinellia festuciformis (Host)
Parl. N 0 2.5 32.1 10
Raphanus raphanistrum L. N 0 2.5 0 1
Robinia pseudoacacia L. A 0 2.5 0 1
Rubus ulmifolius Schott N 0 20 0 8
Salicornia fruticosa (L.) L. N 0 2.5 92.9 27
Salicornia perennans Willd. N 0 0 10.7 3
Salsola kali L. A 68.8 12.5 0 27 Sanguisorba officinalis L. N 0 7.5 0 3 Scabiosa triandra L. N 0 27.5 0 11 Scirpoides holoschoenus (L.) Soják N 0 10 0 4 Sedum sexangulare L. N 0 15 0 6 Senecio inaequidens DC. A 3.1 10 0 5
Setaria italica (L.) P.Beauv.
subsp. viridis (L.) Thell. N 0 2.5 0 1
Silene vulgaris subsp.
angustifolia (Moench) Garcke N 3.1 30 0 13
Soda inermis Fourr. N 18.8 10 0 10
Sorgum halepense (L.) Pers. A 0 2.5 0 1
Spergularia media (L.) C.Presl N 3.1 0 3.6 2
Sporobolus maritimus (Curtis)
P.M.Peterson & Saarela N 0 2.5 10.7 4
Sporobolus pumilus (Roth)
P.M.Peterson & Saarela A 56.3 62.5 25 50
Stachys recta L. N 0 2.5 0 1
Suaeda maritima (L.) Dumort. N 3.1 5 14.3 7
Symphyotrichum lanceolatum (Willd.)
G.L.Nesom
Frequency (%)
Species Status Foredune Backdune Saltmarsh Overall
Teucrium chamaedrys (L.) N 0 2.5 0 1
Trachomitum venetum (L.)
Woodson N 6.3 27.5 0 13
Trifolium repens L. N 0 0 3.6 1
Trigonella alba (Medik.)
Coulot & Rabaute N 0 17.5 0 7
Trigonella officinalis (L.)
Coulot & Rabaute N 0 2.5 0 1
Tripidium ravennae (L.)
H.Scholz N 0 2.5 0 1
Verbascum phlomoides L. N 0 5 0 2
Xanthium italicum Moretti A 75 27.5 0 35
CHAPTER 2
Seagrass meadow cover and species composition drive the
abundance of Eurasian wigeon (Mareca penelope L.) in a
lagoon ecosystem of the northern Adriatic Sea
Francesco Boscutti1 | Stefano Vitti1,2 | Valentino Casolo1 | Flavio Roppa3 | Daniel Tamburlin1 | Stefano Sponza4
1Department of Agricultural and Environmental Sciences, Plant Biology Unit, University of Udine, Udine, Italy
2Department of Life Sciences, University of Trieste, Trieste, Italy 3Via San Giovanni D'Antro 2/2, Udine, Italy
4Department of Mathematics and Geoscience, University of Trieste, Trieste, Italy
Correspondence
Stefano Vitti, Department of Life Sciences,
University of Trieste, Via Weiss 2, 34128 Trieste, Italy.
Email: stefano.vitti@phd.units.it
Abstract
distribution of three seagrass species (Cymodocea nodosa, Zoostera marina and Nanozostera noltei) occurring in the Marano and Grado lagoon (Northern Adriatic Sea). Twelve bird monitoring areas were monthly surveyed for 3 years whereas seagrass distribution data were collected for the whole lagoon in the following years. The overall number of individuals of M. penelope was related to seagrass meadow extension and species cover by using a multiscale approach in four circle buffers (with radius of 500, 750, 1,000 and 1,250 m). Among the considered scales, the 750 m radius scale showed the best performance. The overall number of M. penelope increased where the occupied area by seagrass meadows was larger. Results also showed that when C. nodosa mean percentage cover increased the number of M. penelope decreased, while if N. noltei mean percentage cover increased also M. penelope number increased. Z. marina showed a negligible influence for all the tested scales. Our findings demonstrate that M. penelope populations depend not only on the extension of seagrass meadows but also on their species assembly, evidencing that M. penelope seem to prefer N.
noltei stands, avoiding meadows with high abundance of C. nodosa.
KEYWORDS
herbivorous birds, lagoon, Mareca penelope, primary producers, seagrasses
Introduction
waters subjected to tide cycles (Marín-Guirao et al. 2005). Such ecological amplitude positively reverberates on the richness of the environmental mosaic, which is pivotal to harbor high levels of biodiversity for all biota (Sadoul 1997). In many lagoons the primary production is mainly sustained by seagrasses (Moncreiff et al. 1992; Erftemeijer et al. 1993; Ziegler and Benner 1999); therefore, maintaining biodiversity and biocomplexity of seagrass meadows, and other related coastal ecosystems, has important conservation and management implications (Duffy 2006). Although widely distributed, seagrasses have experienced a large-scale decrease in the last decades in most of worldwide populations (Borum et al. 2004; Waycott et al. 2009; Short et al. 2011). In fact, their distribution, productivity, and community composition has been altered by global changes such as variations in sea level, salinity, temperature, atmospheric CO2, and UV
radiation (Short and Neckles 1999; Orth, Carruthers, et al. 2006; Unsworth et al. 2014).
as prey, for higher levels, and, as primary consumer, transferring energy up the food web (Jiménez-Ramos et al. 2017).
Seagrasses are largely studied as primary source sustaining wigeon populations (Nacken and Reise 2000). Moreover, seagrasses are also fundamental in the frame of the overall marine biodiversity. Indeed, structure and species composition of seagrass beds are influent factors for other photosynthetic organisms (Orth, Harwell, et al. 2006) and animal communities (Orth et al. 1984; Somerfield et al. 2002).
Several authors already have studied the relationships between wigeon and seagrasses (Valentine and Heck Jr 1999; Nacken and Reise 2000; Borum et al. 2004; Bouchaala et al. 2017). For example, in Northern Sea, Vermaat and Verhagen (1996) showed that the rapid decline in biomass from mid-September onwards could be attributed to grazing by herbivorous migratory waterbirds and it was estimated that wigeon can remove 65 g Ash-Free Dry Weight (AFDW) per bird day−1.
Other studies correlated wigeon’s occurrence to seagrass meadow distribution, some of these performed in Mediterranean Sea (Orth et al. 1984; Vermaat and Verhagen 1996; Valentine and Heck Jr 1999; Nacken and Reise 2000). Nevertheless, such studies seldom explored the preferences of wigeon for seagrass meadows constituted by different species. We used an observational approach to verify the relationships between the wigeon abundance and the distribution/cover of three seagrass species occurring in a large lagoon ecosystem of the Northern Adriatic Sea. In particular, we hypothesized that:
(i) wigeon flock increased in relation to seagrasses overall cover;
Material and methods Study site
waterbird species, and of national value for 33 species (Regione Friuli Venezia Giulia 2018).
Study species and data collection
Eurasian wigeon
Wigeon is a surface feeding waterbird species; on the wintering ground it feeds mainly on submerged vegetation and sometimes it feeds in absence of water (Larsen 2008). However, it can also eat a larger proportion of benthic invertebrates (Dessborn et al. 2011). In Europe the species is evaluated as Least Concern. The species has an extremely large range and the world population trend appears to be stable. Differently in the EU27 the population is estimated to have decreased by 30-49% during the last 19.2 years (three generations), and it is therefore classified as Vulnerable (IUCN 2016). In the study area wigeon is one of the most common wintering waterbird species. During winter and fall seasons (from September to March) it feeds and rests in the study area with a population of ca. 22,000 individuals (Sponza et al. 2009). The wigeon is hunted in the whole lagoon except for the areas included in the natural reserves (Fig. 2.1b). Grado and Marano lagoon is of international importance for the species, as it hosts at least 1% of the total population of the reference flyway connecting the Western Siberia and the North-Eastern Europe to the Black Sea and Mediterranean regions (Regione Friuli Venezia Giulia 2018).
population was assessed on 12 areas within 3 transect each (Fig. 2.1b). Centroids points of observation areas were used due to the uncertainty of precisely georeferencing a mobile flock, often composed of thousands of birds. All the flocks observed were composed by wigeons only or in any case wigeon was the dominant species. Data were preliminary summarized as (i) the total number of individuals of wigeon per site and survey and (ii) the mean number of individuals of wigeon per site. For geographical coordinates and summarized counts data of each site, see Table 2.1.
Seagrasses
Monitoring of seagrasses was conducted in between spring and fall of the years 2009-2010. During the monitoring, a distribution map of seagrass meadows was realized for the whole Marano and Grado lagoon, with a cartographic scale of 1:5,000. Distribution map was realized via a photointerpretation using digital aerial photos with 0.5 X 0.5 m resolution (taken in 2007 – high tide) and digital aerial photos with 0.2 X 0.2 m resolution (taken in 2003 – low tide) (Boscutti et al. 2015). Single species abundance was recorded in 570 sample areas within a regular grid applied to the whole lagoon (Boscutti et al. 2015). While in Boscutti et al. 2015 the authors disregarded the inner lagoon and brackish water sample areas, we have here included all the sample areas from their original database, thus covering the whole lagoon. In each sample area, presence of each seagrass species and visual estimation of species cover were recorded. Three seagrass species were recorded, namely Zoostera marina L., Nanozostera noltei (Hornem.) Toml. & Posl. and Cymodocea nodosa (Ucria) Asch.
Data analysis
