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Article

The Effectiveness of Natura 2000 Network in Conserving Salix alba and Populus alba Galleries against Invasive Species: A Case Study of Mureșul Mijlociu—Cugir Site, Romania

by
Cristina Maria Avram
1,
Marian Proorocu
1,*,
Anamaria Mălinaș
2 and
Cristian Mălinaș
1
1
Department of Engineering and Environmental Protection, Faculty of Agriculture, University of Agricultural Sciences and Veterinary Medicine, 400372 Cluj-Napoca, Romania
2
Department of Plant Culture, Faculty of Agriculture, University of Agricultural Sciences and Veterinary Medicine, 400372 Cluj-Napoca, Romania
*
Author to whom correspondence should be addressed.
Forests 2023, 14(1), 112; https://doi.org/10.3390/f14010112
Submission received: 1 December 2022 / Revised: 22 December 2022 / Accepted: 4 January 2023 / Published: 6 January 2023
(This article belongs to the Section Forest Biodiversity)
Browse Figures
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Abstract

:
There is currently a lack of knowledge regarding the effectiveness of the Natura 2000 (N2000) network in providing protection against biological invasion by invasive alien species (IAS). In this study, we analyzed two Salix alba and Populus alba riparian habitats located both inside and outside a N2000 site from Romania in order to assess the efficacy of N2000 network in conserving this type of ecosystem against IAS. Field investigations were conducted both using polygon method for vegetation study and semi-structured interviews focusing on the local people knowledge and their contribution to biological invasion. We found that the research area located within the N2000 network is highly exposed to biological invasion by IAS, the major threat to this type of habitat being expressed by Acer negundo, which occupied more than half of the vegetation cover. It seems that not only the management strategy should be blamed for this situation, but rather its failure in popularization and application. As such, in our opinion, future management plans developed by N2000 network should rely on the intertwined co-evolutionary mechanisms existing between poplar and willow stands diversity and cultural diversity, by integrating aspects related to local traditional knowledge.

1. Introduction

Biodiversity is the key indicator of the health of an ecosystem, which ultimately constitutes the foundation of human civilization [1]. Despite its invaluable contribution to our long-term survival, well-being, prosperity, and security [2], biodiversity is threatened nowadays by several direct and indirect drivers, including habitat conversion, climate change, overexploitation, pollution, and invasive alien species (IAS) [3,4,5]. The major tool for counteracting the negative impacts associated with biodiversity loss is the setting aside of large-scale, functional networks of protected areas (Pas) [6,7]. The Natura 2000 Network (N2000) is the largest network of Pas in the world, designed and implemented by the EU, and having as main objective to protect the biodiversity in all of its forms. The N2000 includes Special Areas of Conservation (SACs) designated under the Habitats Directive [8], and Special Protection Areas (SPAs) designated under the Birds Directive [9]. The Habitats Directive is aiming to enhance a good conservation status for the European habitats, and, to this end, the N2000 network makes an important contribution. Recent studies demonstrate the contribution of the habitats rated to be at “favorable conservation status” in providing higher biodiversity and ecosystem services (especially regulating and cultural ones), but the actual contribution of N2000 in achieving this status is still undefined [10]. The N2000 regime is quite permissive and includes human activities as a relevant part of the ecosystems functioning [11,12]. Considering that humans are the main driver of biological invasion, the PAs comprised in this network could be probably more exposed to biological invasions than other PAs with no human activities at all [13]. In this regard, Pyšek et al. [14] pointed out that humans could greatly impact ecosystem functioning by interfering and affecting the nutrient and contaminant cycling, hydrology, habitat structure, and disturbance regimes. Consistence evidence already exist regarding the high exposure of riparian forests to IAS threats as a result of periodical flood pulses that occurred within this type of habitat. These events could constitute an important vector for IAS propagation [15]. Yet, few studies addressed the issue of IAS occurrence and impact on riparian habitats located within N2000 network. Some examples of such a habitat are Salix alba and Populus alba galleries (with the N2000 identification code 92A0), each defined as a riparian forest dominated by poplar and willow species [16]. This type of habitat is largely spread among riverbanks from EUs countries, including Romania. Poplar (Populus alba) and willow (Salix alba) galleries hold an outstanding value, translated through a variety of ecosystem services [17], from provisioning services through biomass production, up to regulating and maintenance services (such as the stabilization of riverbanks, water filtering animal sheltering, etc.), and cultural services (aesthetic and recreation). Thus, studies aiming to evaluate the conservation status and identify potential threats for this habitat are greatly required. This research aimed to assess the efficacy of N2000 network in conserving Salix alba and Populus alba (here poplar and willow) galleries against IAS. We specifically aimed to evaluate: (1) species diversity inside and outside the N2000 site; (2) the effectiveness of N2000 network in conserving poplar and willow galleries against biological invasion by IAS; and (3) local peoples’ knowledge and contribution to the IAS occurrence, and to which extent their local ecological knowledge could contribute to a better conservation status of this type of ecosystem in face of biological invasion.

2. Materials and Methods

2.1. Research Area Description

The study area encompassed two Salix alba and Populus alba habitats, one inside (A1) and one outside (A2) the N2000 network. The two research areas were selected based on a preliminary field investigation using the DJI Mavic Mini Fly More Combo Drone. The aerial images acquired (at a flying altitude of 200 m) allowed us to identify the research areas relevant for the objectives of our study. As such, two research areas (one inside and one outside the N2000 site) were selected based on a visual appreciation of the vegetation representativeness (meaning that each area selected was representative for the habitats explored through drone aerial images). Both land surfaces (A1 and A2) are subjected to short-term periodical floods, and both plant and animal species in the areas are well adapted to this flooding regime [18].
The N2000 site consisted in ROSCI0419 Mureșul Mijlociu–Cugir, located in Romania (N 45.952333°, E 23.360433°), on an area of 356.6 ha and approx. 23 km mostly along the Mures and Cugir rivers (Figure 1). According to the Management Plan [18], this habitat is placed on a fertile alluvial soil, with vegetation typical for river floodplains, and a temperate continental climate (annual average temperature of 8 °C and annual sum of rainfalls of 500–600 mm). The land is mainly used as pasture, but also as agricultural land, cultivated with wheat (Triticum aestivum), barley (Hordeum vulgare), rye (Secale cereale), and oats (Avena sativa), or maize (Zea mays), potatoes (Solanum tuberosum), beets (Beta vulgaris), sunflowers (Helianthus annuus), and even vineyards (Vitis vinifera) on the sunny slopes [18].
The river floodplains included in the N2000 site extends up to 2 km width or even more in some places, favoring the development of valuable floodplain vegetation that can harbor an increased diversity of avifauna species [18]. The site was confirmed as SCI in the year 2018, with the main purpose in conserving the 6 ha poplar and willow galleries included (Figure 1), and ten mammals and fish species of community importance (2 mammals—Castor fiber, Lutra lutra; 8 fish species—Aspius aspius, Gobio albipinnatus, Gobio kessleri, Rhodeus sericeus amarus, Sabanejewia aurata, Cobitis taenia, Zingel streber, and Zingel zingel). Despite its recognized ecological value, some areas within the ROSCI0419 Mureșul Mijlociu Cugir are highly degraded, such that they can no longer provide suitable conditions for a number of fauna species of community importance, such as Cobitis taenia, Zingel streber, and Zingel zingel [18].
The research area inside the N2000 site is located in Sibot municipality, Alba County, Romania (45°56′07″ N 23°20′02″ E), along the Mures and Cugir rivers. This municipality includes four villages (Băcăniți, Șibot, Balomiru de Câmp, and Tărtăria), and experienced a drastic decrease in the number of inhabitants during the last 50 years, from 3399 inhabitants in the year 1850, down to 2236 inhabitants in the year 2011 [19].
The research area outside the N2000 network is located in Alba County, Romania, along the Mures River (Figure 1). This research area consists of a populous and willow riparian forest, nowadays surrounded by agricultural fields. The A2 area is located in Rădești (46°14′46″ N 23°44′38″ E), a municipality with four villages included (Leorinț, Meșcreac, Rădești and Șoimuș), which showed a similar trend of depopulation similar to that described for Șibot. According to the last published data it seems that the number of inhabitants from Rădești showed a drastic decrease from 2325 inhabitants in the year 1930, down to 1200 inhabitants in the year 2011 [19].
The latest official data shows that, generally, the population from Alba County is decreasing and is dominated by elderly people [19].

2.2. Tree Species Diversity

Field investigations were conducted between April 2020 and November 2021. The polygon method was used for tree study, in order to evaluate tree species richness for each experimental area (both A1 and A2). Polygons could be simple defined as homogenous areas of vegetation structure and type [20] and represent the first stage involved in a forest inventory. Following the delineation of these homogenous areas, the polygons are stratified in sub-samples which allow a more detailed investigation of specific forest attributes (species, height, diameters, and age) [20].
The research areas (both A1 and A2; represented in Figure 2a,b) were divided into 18 polygons with a radius of 10 m (9 polygons for A1, and 9 for A2), with three sites per polygon (after Manning et al. [21]). Thus, vegetation was recorded in 27 representative plots (0.6–0.8 ha/each) for each research area, resulting in a total of 54 plots. Species richness was expressed as the average number of tree species, and families inventoried. The number of trunks per plot (both for native and IAS trees) was recorded within each plot.
On the basis of the data collected during vegetation studies the following attributes of tree species diversity were calculated: tree species richness (as the total number of tree species identified), the Shannon-Weiner index (H′), and the Evenness (J). These indices are able to provide us important information regarding the diversity in tree species of the research areas.
The Shannon–Wiener index (H′) is a diversity measure characterized by the number of individuals observed for each species in the sample plot [22]. Usually the H′ index reaches values greater than 1, such that in this index interpretation one should consider that species diversity grows proportionally with this index value [23]. This diversity measure was calculated after Shannon [22], based on the following Formula (1):
H′ = −∑[(pi) × log(pi)]
where: H′—the Shannon–Wiener index; pi—the proportion of individuals of i-th species in a whole community (pi = n/N)—where n–individuals of a given type/species; N—total number of individuals in a community.
We also calculated the evenness index which gives us an idea about the degree to which individuals are split among species [23]. In the interpretation of evenness, we have to consider that low J values indicate the dominance of a certain species, while high values indicate that relatively equal numbers of individuals belong to each species [23]. This diversity index, with values ranging between 0 and 1, was calculated after Pielou [24], based on the following Formula (2):
J = H′/Hmax
where: J—the evenness index; H′—Shannon–Wiener index; Hmax—the highest possible H′ and given by log(N), with the same log base as in the calculation of H′.

2.3. Effect of N2000 in Conserving Poplar and Willow Galleries against IAS

The effectiveness of N2000 network in providing protection for poplar and willow riparian forests against biological invasion by IAS was evaluated based on the results obtained through tree inventories (according to the method described previously in Section 2.2). In this regard, tree density was assessed, expressed as the number of trunks per plot (both for native and IAS), and some of the most relevant dendrometric measurements (tree average height, diameter, and age). For each tree, diameter at breast height (DBH) at 1.3 m above the ground was recorded using a tree caliper. Two measurements were made for each tree trunk, and the average of the two measures was recorded. Tree height was measured for each tree trunk inventoried using a dendrometer. The age of the trees was measured for each tree trunk inventoried using an Increment borer, a specialized tool commonly used for this type of assessment. This tool enables users to extract a section of core sample from a living tree, and count the rings found in the wood tissue.
All dendrometric measurements were further validated by measurements performed to several downed trees found during field investigations.

2.4. Local People Knowledge and Contribution to IAS Occurrence and Overall Conservation of Poplar and Willow Forests

An ethnobotanical field investigation was conducted in Alba County, Romania (covering both A1 and A2 research area) between July 2020 and November 2021. The snowballing method [25] was used for the selection of informants, in order to determine the most representative persons for the topic researched (in particular landowners). This is a non-probability sampling techniques that assists researchers in their approach to subjectively select unit that represents the population under study. A total of 93 inhabitants from A1 and 121 from A2 were interviewed in-person. The semi-structured questionnaire was divided into four parts (detailed in Table 1): (1) general information regarding age, gender, place of residency, education level, and job/study field; (2) awareness about Natura 2000 network; (3) knowledge regarding the invasive alien species; and (4) local ecological knowledge regarding the management applied to poplar and willow riparian forests. Generally, if the answer to the first question from Section 2 and Section 3 is “No” (i.e., meaning that the respondent did not know about the N2000 network, and/or IAS meaning), then we proceeded to the other sections, and did not address the questions about the unknown topic in further detailed.

2.5. Data Statistical Analysis

The data recorded during field investigations were processed using descriptive statistics by Statistica vs. 10 (developed by StatSoft in the year 2010), two sample t-tests and Hutcheson/diversity t-tests for the two diversity indices calculated, using Past free software for scientific data analysis [26]. Effects were accepted as statistically significant if p ≤ 0.05.

3. Results

3.1. Tree Species Diversity

The results recorded showed that the two research areas were almost similar in terms of tree species composition, including two native species: willow (Salix alba) and poplar (Populus alba), and two IAS, namely the box elder (Acer negundo) and false indigo-bush (Amorpha fructicosa; Figure 3 and Figure 4; Table 2). The only difference concerning tree species composition was the presence of common alder (Alnus glutinosa) in A2, species which was not identified in the plots inventoried in A1 research area. Generally, the average number of tree species per plot inventoried were higher in A1 compared to A2 (Figure 4). Additionally, significant differences were recorded which only concerned the box elder and common alder (p < 0.01).
As illustrated in Table 2, the A2 research area showed a lower number of trunks per plot compared to A1, and a higher diversity (highlighted through H′ index, which scored the highest value in A2). Moreover, A2 included an even population distribution of species (highlighted by J value, which was 0.76 for A2, compared to 0.68 for A1). Significant difference in Shannon–Wiener (p < 0.00) and Evenness (p < 0.01) diversity indices were recorded among the two research areas.

3.2. Effect of N2000 in Conserving Poplar and Willow Galleries against IAS

The forest stands found in the investigated areas showed relatively small differences in the share of indigenous species and their respective dendrometric measurements (p > 0.05). Willow was the dominant native species in both the A1 and A2 research areas (Table 3), scoring an insignificant higher density in A2, compared to A1 (p > 0.05).
Additionally, the composition of the poplar and willow galleries found in the two research areas showed to be affected by IAS. Both research areas were to a various extent invaded by two IAS (Table 3), such that the dominant tree species were the IAS box elder and false indigo-bush. These two IAS tree species occupied 74% from the overall tree vegetation in A1, and 56% in A2. The box elder was more abundant in the area located inside the N2000 network (62%), compared to the research area outside the PA (48%). According to the dendrometric measurements, the box elder invasion was higher in the forests stands which comprised younger willow stands (average age per plot in A1 of 23 years), compared to older willow stands (average age per plot in A2 of 29 years). The dominant IAS box elder showed generally higher values of the dendrometric indices in A1, significant differences were recorded concerning this species age, such that the average age per plot recorded in A1 was higher with approx. 4 years compared to that reached in A2.

3.3. Local People Knowledge and Contribution to IAS Occurrence and Overall Conservation of Poplar and Willow Forests

Overall, 214 individuals from A1 (n = 93) and A2 (n = 121) research areas participated to the semi-structured interviews, most respondents were females aged between 20 and 85 years (64%; n = 137). Generally, the individuals from both research areas were retirees (68%; n = 146), unemployed (14%; n = 30), or students (8%; n = 17), with the major source of income resulting from extensive agriculture and animal breeding. Few respondents hold a bachelor’s degree (11%; n = 24), which was the highest academic degree among the respondents.
A majority of the respondents had never heard of N2000 network. Thus, 75% (n = 68) individuals from A1 research area and 82% (n = 99) from A2 had no knowledge about the meaning of N2000 network (Figure 5). Among the other 25% individuals from A1, which claimed to have heard about N2000 network, only 10% were able to correctly identify the existence of some N2000 sites around their residential area. Most of them were individuals holding a bachelor’s degree (n = 5), which was the highest academic degree among the respondents. The same respondents were able to correctly specify the major purpose of N2000 network; however, only three individuals knew little information regarding the specific management of such a PA (Figure 5). The respondents from Rădești, the municipality where A2 research area is located, seemed to know even less information regarding the existence and management of N2000 sites. As such, only 9% were able to identify correctly the existence of some N2000 sites around their residential area, all of them being individuals holding a bachelor’s degree (n = 2). The same respondents were able to correctly specify the major purpose of N2000 network, but none of them knew any information regarding the specific management of such a protected area.
Generally, the respondents did not heard about the term “invasive alien species” (A1: 88%; n = 80; S2: 84%; n = 102). After a brief clarification of the meaning of IAS made by the interviewer, the respondents were able to give more information on this topic (Figure 6). Thus, a total of 40 respondents from Șibot (the municipality where A1 research area is located) and 62 individuals from Rădești claimed to have noticed some IAS around their residential area/agricultural fields. These respondents were able to correctly name the false indigo-bush, one of the two IAS identified by us through the tree field investigation (detailed in Section 3.1). Same respondents identified the box elder as an aggressive, invaluable tree, with negative effects on native vegetation, but they did not know how to name it, thus they called it just “tree”. Most of the respondents who knew some information regarding IAS were male (A1: 68% with n = 27; A2: 71% with n = 44). Generally, the individuals recognized that they have learned about IAS during their work in the agricultural fields, located in the proximity of the riparian areas.
The results recorded during the fourth section of the interview (Figure 7) showed that most of the respondents were able to identify the major ecosystem services provided by this type of habitat (A1: 78% with n = 71; A2: 83% with n = 100). Among the most commonly mentioned functions were: the important role of poplar and willow forests in providing protection against erosion and flood (A1: 78% with n = 71; A2: 83% with n = 100), regulating climate (A1: 36% with n = 26; A2: 21% with n = 26), filtering the water (A1: 39% with n = 28; A2: 48% with n = 58), and recreation (A1: 78% with n = 71; A2: 85% with n = 103). Most of the respondents which were able to share their knowledge regarding the value of poplar and willow riparian forests were males (A1: 82% with n = 52; A2: 73% with n = 84) aged between 44 and 82 years old (A1: 67% with n = 35; A2: 54% with n = 65). Among the 71 respondents from A1 who were able to correctly identify the functions of the riparian forests, approximately 53% (n = 48) claimed to be notice some changes in poplar and willow species composition. A higher percentage of individuals from the A2 research area observed some changes in poplar and willow species composition (78%; n = 94). Most of them were able to correlate these changes with the impact of the two IAS discussed on Section 3 of the interview (66%; n = 38; as a total from both research areas).
Furthermore, when the 171 individuals who recognized the value of the riparian forests investigated were asked to describe the management applied to these forests stands, a total of 42% individuals from A1 research area (n = 38) and 54% (n = 65) from A2, with ages between 62–84 years old, told us that, until approx. 10–15 years ago, they usually pruned the willows in late winter-early spring (through pollarding and coppicing). The respondents recognized that they were stimulated to perform these management practices because in the past, poplar and willow forests were integrated into local people daily lives. As such, the most commonly utilizations of poplar and willow listed by the respondents were: as raw material for kitchen tools and basket manufacturing, medicinal uses, divine protection against diseases, and symbol for rebirth, chastity, and fertility.

4. Discussion

Despite the large number of Pas implemented through N2000 network, biodiversity is currently threatened by invasive alien species [3]. Our results confirm these findings, as the research area located inside the N2000 network showed to be less rich in terms of tree species diversity, and comprised a higher percent of IAS, compared to the research area outside the N2000. As previously described (Section 3.1), the highest tree density was recorded by the IAS box elder, which scored 62% in the A1 research area, and 48% in A2 (Table 3).
The compound Indices calculated showed that the A2 research area has more diversity (highlighted through H′ index which had the highest value in A2). Moreover, this research area includes an even population distribution of species (highlighted by J value, which is 0.83 for A2, compared to 0.76 for A1). These findings are supported by previous research, which also highlighted that higher levels of biological invasion may reduce diversity [27]. In addition, Mendoza-Fernández et al. [28,29] notes that the Natura 2000 network does not always collect the best samples from different habitats, as there are great conservation value species or habitats outside this protection. However, there are some studies which showed that IAS can increase the number of species locally [30,31], highlighting the need to conduct more research aimed at evaluating the impact of IAS on native diversity.
According to the dendrometric measurements presented in Table 3, there were no significant differences in willow occurrence in A1 compared to A2, while the other two native species (poplar and the black alder) showed a lower tree density found in the research area inside N2000, where the two IAS occupied 74%. Both of the invasive tree species identified show to be older in the N2000 site (16.6 years in A1 and 12.68 years in A2 for box elder, respectively, and 9.25 years in A1 and 6.83 years in A2 for false indigo-bush, respectively), highlighting that it is probable that the invasion is coming from downstream to upstream of Mures river (from inside the N2000 site into the direction of A2). A similar mention was made also in the Management Plan of the research area A1 [18], where it is specified that the invasion of Acer negundo is likely coming from downstream of Mures river. As pointed out by the results recorded during this study, and supported through previous research conducted so far, the differences in tree dimensions are an effect of stand age, more than a result of N2000 management. In this regard, Marziliano et al. [32] highlighted that the growth of trees continues for years by continuously increasing both diameter and height, such that the tallest trees are often the oldest ones [33].
Overall, the data acquired through tree inventories showed that the two research areas were more or less similar in terms of tree species composition, the differences noted previously are insignificant from statistic point of view. Considering these findings, it is of outstanding importance to find out which are the major causes that produced this high percentage of IAS on both research areas, and especially in the research area located inside the N2000 network. As such, the main question that arises is whether the management specific to N2000 network “is sufficient” enough to provide protection for poplar and willow galleries. Or maybe, could be other factors contributing to this high level of invasion within N2000 site?
It is increasingly recognized nowadays that any plan involving nature conservation should include aspects regarding the mutual interdependence between human culture, heritage and history, and nature expressed as ecology or biodiversity [34]. According to Uprety et al. [35], traditional knowledge and science are complementary and should be used in conjunction in ecological restoration projects. The results from the semi-structured interviews showed that most of the respondents from both research areas did not have much knowledge about the N2000 network, and thus they were in total ignorance on the specific management which should be applied within such a PA. This finding should not be surprising since other research has already pointed out the same disappointing conclusion for other countries included in the N2000 network. Oliveira et al. [36] pointed out that most respondents from Portugal which participated to their study had never heard of N2000. Moreover, according to a survey conducted by the European Commission in the year 2018, only 11% of Europeans claimed to know what N2000 is [37].
Generally, the respondents did not recognized the term “invasive species” (A1: 88%; n = 80; A2: 84%; n = 102). After they found out about the meaning of IAS (provided by the interviewers), some of them (40 respondents from A1, and 62 individuals from A2) were able to name some IAS noticed around their residential area/agricultural fields. These respondents were able to correctly name the false indigo-bush, one of the two IAS identified by us through tree field investigation. Furthermore, the respondents identified the box elder, but they did not know to name it, and thus they simply called it “tree”. This species was described by local people as an aggressive, invaluable tree, with negative effects on native vegetation. This is an example of the phenomenon called “plant blindness” [38].
Despite the respondents not having the knowledge regarding the traditional management applied to IAS, they were able to provide us important and valuable information regarding the intertwined co-existence between the poplar and willow stands diversity and cultural diversity. As such, the answers recorded during the semi-structured interviews highlighted that, during ancient times, these forest stands were closed related to community life through several practices and believes. Overall, these uses and believes not only enhanced a sustainable management of poplar and willow stands (through pollarding and coppicing), but they also strengthened them to face threats, such as diseases, pests and IAS, since pollarding and coppicing in the spring are two essential practices for these species growth and harmonized development [39]. Most of the respondents revealed us that these practices were somehow supported through several traditions, which have mostly disappeared in modern times. As such, we found out that during ancient times these areas were closed related to community life through several practices and believes, which integrated poplar and willow forests into local people daily lives and provided them a special protection and care. Thus, according to traditional ecological knowledge, it seems that the willow had more functions in ancient times. This species was used not only as firewood (on a lower percentage, especially the old branches fallen to the ground), but was also as an important raw material used for kitchen tools manufacturing (wood spoons, scoops, bottoms, and other such objects), fences, and for baskets making. These objects were made from willow branches, resulted after pollarding and coppicing. Thus, according to the responses recorded during the semi-structured interviews, every year, the willow rods were cut as close as possible to the stool, which provided not only the raw material for the tools mentioned above, but also a better growth and sustainable development of this species. The respondents remembered that, in the past, some areas around these riparian forests were used as pastures (with an increased percent found in A2 research area). The extensive animal raising approach, which chose the times that the pollard willow and poplar trees were above the grazing height of livestock (most commonly cattle). This practice not only allowed animals to graze the woody-pastures, but also had some important sustainability benefits for these two species, encouraging new growth at the top of the tree. Furthermore, it seems that the willow is associated with some ancient rituals. Thus, the willow is considered by inhabitants as the emblem for “The flower Sunday”, an orthodox religious celebration occurring during the sixth week of Lent. According to the traditional knowledge, during this religious celebration, people must go to the church service holding a willow branch in their hands, which will be sanctified by the priest during the religious ceremony. Further, the tradition says that this sanctified willow branch will provide protection for those who touch it or live around it. As a result, often people introduced some parts of this branch in animals’ shelters and to the vegetable garden, to provide protection against diseases and pests. Interestingly, this religious celebration overlaps with the optimal stages in vegetation growth when it is recommended to coppice willow. Willow bark was also used in ancient times as medicine, both for people and animals. Another cultural event closed related to willow (mentioned by the respondents) was the ancient ceremony according to which every young pregnant women was led to a willow or poplar fence by two older women; hereafter, they braid the pregnant women’s hair similar to a bride’s traditional hairstyle and dress her up, they circle around her, saying three times the following poem: “Please marry the women of God “the name of the pregnant women” with the fence, with the poplar or with willow”. It seems that this ceremony symbolized rebirth, chastity, and fertility.
The respondents concluded that according to their own opinion and experience, the application of these management practices resulted in “clean poplar and willow forest stands”, meaning that no other IAS were allowed to reproduce and propagate describing the ancient poplar and willow stands as “pure and robust”. However, somewhere in this partnership between man and poplar and willow, the partnership was broken; some of the reasons why this happened include the drastic depopulation of the entire Alba County (not only of the two research areas), followed by population aging. This factor, together with the low speed in the implementation of the reforms that shifted land ownership from the collective back to individual users, resulting in a high rate of agricultural land abandonment. In sum, these factors and the loss of traditions (both related to their cultural believes, and concerning the extensive agricultural practices), contributed to a high vulnerability of poplar and willow stands, leaving them “unguarded” in face of biological invasion by IAS. This local ecological knowledge is a cultural heritage that is risk of extinction due to rural depopulation and people aging. In addition, the loss of traditional management can lead, as pointed out by Dömpke and Succow [40], to a biodiversity loss.
In addition, it seems that the N2000 network, along with this site managers, failed in safeguarding these riparian forests strips by not providing sufficient popularization about the specific management, which should be applied in these areas. Although this individual category (N2000 managers) were not included in our interviews, it is clear that if the managers would have taken any actions in protecting these forests stands against IAS: (1) we would not find this magnitude of invasion in the N2000 site; (2) local people and landowners would possess more knowledge and awareness regarding the impact of IAS on native trees, and the specific management which should be applied.
Considering that the PAs included in the N2000 network allow for a broad range of human activities, we genuinely believe that the success of the N2000 network stands in developing a close partnership with the inhabitants’ residents to these areas. However, this partnership could also create a solution where everyone benefits, since, as pointed out previously, some respondents from both research areas have important knowledge regarding the practices which could be applied to these riparian forests management in order to ensure their favorable conservation status.
It was previously reported that in the initial phase of their invasion some IAS species, such as the box elder, occur in riparian localities and subsequently spread into adjacent non-riparian habitats [41]. This is generally attributed to the efficient transport of alien species’ propagules due to regular flooding [41]; such that, despite the forests strips investigated were periodically and in the short-term subjected to flooding [18], we cannot exclude that the flooding regime could have a certain contribution to this species occurrence. Still, box elder was found in higher percentage of participation into adjacent habitats, not exposed to river flooding, such that further research aimedat this species’ occurrence and spread are highly required. Although this was not the objective of the present study, we do plan to expand our researches in these areas, in order to identify which were the major factors contributing to box elder occurrence and spread, and to which extend is this species invasion spread along the entire Mures river.

5. Conclusions

Despite the Salix alba and Populus alba galleries from ROSCI0419 Mureșul Mijlociu-Cugir, Romania are included in the N2000 network, thanks to their recognized multiple ecosystem services, it seems that the inclusion in the highest ecological network is failing in proving their conservation in face of biological invasion. As pointed out by our research, the research area inside the N2000 network is highly threatened by two IAS, namely the box elder and false indigo-bush. This situation seems to be caused by inhabitants’ lack of knowledge regarding the specific management which should be applied within N2000 sites, and also by N2000 network failure in integrating aspects related to local ecological knowledge in their conservation program. Additionally, the drastic depopulation of the entire Alba County (not only of the two research areas), followed by population aging, agricultural land abandonment, and loss of traditions (both related to their cultural believes, and also concerning the extensive agricultural practices) seemed to have contributed to a high vulnerability of poplar and willow stands, leaving them “unguarded” in face of biological invasion by IAS. Based on these findings, we believe that future management plans developed by N2000 network should rely on the intertwined co-existence of poplar and willow stands diversity and cultural diversity, by integrating aspects related to local traditional knowledge. This kind of approach could result in a more efficient management against IAS and other threats, and in an increase popularization of the conservation/restoration programs. Although it was not considered in this study, based on previous studies, we recognize that other factors may have contributed to box elder invasion, such as the flooding regime and wind. For this reason, we plan to expand our research in these areas in order to identify to which extend the Mures river plain is exposed to IAS (especially by box elder), and which are the major factors contributing to this invasion phenomenon.

Author Contributions

Conceptualization, M.P., A.M. and C.M.A.; methodology, M.P. and A.M.; software, C.M. and C.M.A.; validation, M.P. and A.M.; formal analysis, C.M.A.; investigation, C.M.A., M.P., A.M. and C.M.; resources, M.P.; data curation, C.M.A.; writing—original draft preparation, C.M.A. and A.M.; writing—review and editing, M.P. and C.M.; visualization, C.M.; supervision, M.P.; project administration, C.M.A.; funding acquisition, M.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Not applicable.

Acknowledgments

The authors thank all the participants involved in this study, and for taking the time to participate to the semi-structured interviews.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 00112 g001 550
Figure 1. Location of the research areas (Source: Original).
Figure 1. Location of the research areas (Source: Original).
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Figure 2. Sampling design: (a) A1—Research area inside the N2000 network. The area marked with a brown color line represents the delineation of the N2000 site. The land surface colored with brown represents the research area inside the N2000 site (A1). (b) A2—Research area outside the N2000 network. The circles found within the two research areas represent the 9 polygons/research area investigated, while the small quadrats found inside the circles represent the 27 plots/research area inventoried. (Source: Original).
Figure 2. Sampling design: (a) A1—Research area inside the N2000 network. The area marked with a brown color line represents the delineation of the N2000 site. The land surface colored with brown represents the research area inside the N2000 site (A1). (b) A2—Research area outside the N2000 network. The circles found within the two research areas represent the 9 polygons/research area investigated, while the small quadrats found inside the circles represent the 27 plots/research area inventoried. (Source: Original).
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Figure 3. Overview presenting the vegetation characteristic for the investigated riparian forest strips (aerial images acquired using the drone): (a) Research area inside the N2000 network; (b) Research area outside the N2000 network.
Figure 3. Overview presenting the vegetation characteristic for the investigated riparian forest strips (aerial images acquired using the drone): (a) Research area inside the N2000 network; (b) Research area outside the N2000 network.
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Figure 4. Mean species richness per plot inventoried. Notes: Values are given as average ± standard error. Effects were accepted as statistically significant if p ≤ 0.05, as follows: ns—p > 0.05—not significantly different. **—p < 0.01—significant from statistical point of view (S, confidence 99%).
Figure 4. Mean species richness per plot inventoried. Notes: Values are given as average ± standard error. Effects were accepted as statistically significant if p ≤ 0.05, as follows: ns—p > 0.05—not significantly different. **—p < 0.01—significant from statistical point of view (S, confidence 99%).
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Figure 5. Awareness about Natura 2000 network. The number of respondents comprises those individuals which answered “Yes” to the question addressed.
Figure 5. Awareness about Natura 2000 network. The number of respondents comprises those individuals which answered “Yes” to the question addressed.
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Figure 6. Knowledge regarding the invasive alien species. The number of respondents comprises of those individuals which answered “Yes” to the question addressed.
Figure 6. Knowledge regarding the invasive alien species. The number of respondents comprises of those individuals which answered “Yes” to the question addressed.
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Figure 7. Local ecological knowledge regarding the ecosystem services provided by poplar and willow riparian forests.
Figure 7. Local ecological knowledge regarding the ecosystem services provided by poplar and willow riparian forests.
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Table
Table 1. The questions addressed through semi-structured interviews.
Table 1. The questions addressed through semi-structured interviews.
SectionsQuestions
1. General informationWhat is your age and gender?
Which is your last degree in education?
What is your occupation?
2. Awareness about Natura 2000 networkHave you heard about the N2000 network?
Have you noticed the existence of some N2000 sites around your residential area?
Which is the major purpose of a N2000 site from your knowledge/point of view?
Have you know about the management strategies specific to N2000 sites? If yes, which one/do you apply?
3. Knowledge regarding the invasive alien speciesDid you heard about invasive alien species?
Have you noticed any invasive alien species in your residential area? If yes, please name some examples.
How do you appreciate the impact of invasive alien species on native vegetation?
Have you applied any management strategies to reduce/increase invasive alien species occurrence?
4. Local ecological knowledge regarding the management applied to poplar and willow riparian forestsHow do you appreciate the value of poplar and willow riparian forests?
Have you benefit of these areas (uses)/how?
Have you noticed any change in species composition of the poplar and willow riparian forests located in the neighborhood of your residential area? If yes, which is the reason of this change, from your perspective?
Have you apply any management strategies to these forests stands?
Table
Table 2. Diversity indices for the research areas inside and outside the N2000 network. Values are given as average ± standard deviation. Values within the same column followed by a common letter are not significantly different according to t-test (for the mean number of trunks per plot) and Hutcheson t-test (for the diversity indices).
Table 2. Diversity indices for the research areas inside and outside the N2000 network. Values are given as average ± standard deviation. Values within the same column followed by a common letter are not significantly different according to t-test (for the mean number of trunks per plot) and Hutcheson t-test (for the diversity indices).
Research AreaMean Number of Trunks per PlotDiversity Indices
Shannon–Wiener Index (H′)Evenness Index
(J)
A1 Research area inside the N2000 network68 ± 7.48 a1.02 ± 0.04 b0.68 ± 0.30 b
A2 Research area outside the N2000 network52 ± 3.55 b1.34 ± 0.13 a0.76 ± 0.07 a
p-value0.008310.00160.0050
Notes. Effects were accepted as statistically significant if p ≤ 0.05 (more detailed definition can be found in Figure 4 notes).
Table
Table 3. Cover and allometric measurements of tree species in the two research areas. Values are given as average ± standard deviation. Effects were accepted as statistically significant if p ≤ 0.05. Values within the same column followed by a common letter are not significantly different according to t-test.
Table 3. Cover and allometric measurements of tree species in the two research areas. Values are given as average ± standard deviation. Effects were accepted as statistically significant if p ≤ 0.05. Values within the same column followed by a common letter are not significantly different according to t-test.
Research AreaTree SpeciesMean Percent Tree Species per Plot (%)Dendrometric Measurements
Height (m)Diameter (cm)Age (Years)
A1NativeSalix alba22 ± 40 b22.5 ± 10.60 b26 ± 6 b23 ± 4 b
Populus alba4 ± 1.91 c31.66 ± 15.27 a47 ± 21 a32 ± 11 a
InvasiveAcer negundo62 ± 6.20 a11.43 ± 4.21 c17 ± 4 c16 ± 4 c
Amorpha fructicosa12 ± 1.81 c1.75 ± 0.70 d1 ± 0 d9 ± 2 d
A2NativeSalix alba25± 3.55 b23.38 ± 4.11 a28 ± 7 a29 ± 7 a
Populus alba8 ± 2.16 c19.5 ± 1.91 a11 ± 1 b19 ± 2 b
Alnus glutinosa11 ± 3.55 c11.15 ± 2.23 b9 ± 2 b11 ± 1 d
InvasiveAcer negundo48 ± 1.63 a11.15 ± 1.13 b12 ± 3 b12 ± 5 c
Amorpha fructicosa8 ± 1.63 c1.66 ± 0.81 c1 ± 0 c6 ± 1 d
p-value
(A1 vs. A2)		Native 0.4360.3030.0800.186
Invasive 0.4020.4900.4100.263
p-value
(A1 vs. A2)		Overall 0.3680.3210.1580.242
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Avram, C.M.; Proorocu, M.; Mălinaș, A.; Mălinaș, C. The Effectiveness of Natura 2000 Network in Conserving Salix alba and Populus alba Galleries against Invasive Species: A Case Study of Mureșul Mijlociu—Cugir Site, Romania. Forests 2023, 14, 112. https://doi.org/10.3390/f14010112

AMA Style

Avram CM, Proorocu M, Mălinaș A, Mălinaș C. The Effectiveness of Natura 2000 Network in Conserving Salix alba and Populus alba Galleries against Invasive Species: A Case Study of Mureșul Mijlociu—Cugir Site, Romania. Forests. 2023; 14(1):112. https://doi.org/10.3390/f14010112

Chicago/Turabian Style

Avram, Cristina Maria, Marian Proorocu, Anamaria Mălinaș, and Cristian Mălinaș. 2023. "The Effectiveness of Natura 2000 Network in Conserving Salix alba and Populus alba Galleries against Invasive Species: A Case Study of Mureșul Mijlociu—Cugir Site, Romania" Forests 14, no. 1: 112. https://doi.org/10.3390/f14010112

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