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Biogeographia – The Journal of Integrative
Biogeography
UC Merced
Peer Reviewed
Title:
Monitoring Natura 2000 habitats: habitat 92A0 in central Italy as an example
Journal Issue:
Biogeographia – The Journal of Integrative Biogeography, 31
Author:
Carli, Emanuela
D'Alessandro, Evelina
Di Marzio, Piera
Giancola, Carmen
Paura, Bruno
Salerno, Giovanni
Blasi, Carlo
Publication Date:
2016
Permalink:
http://escholarship.org/uc/item/83f7v7t4
DOI:
http://dx.doi.org/10.21426/B631132735
Keywords:
alien species, Article 17, conservations status, plant community indicators, plant species
indicators, riparian forests
Local Identifier:
biogeographia_32735
Abstract:
The evaluation and the subsequent monitoring of the conservation status of habitats is one
of the key steps in nature protection. While some European countries have tested suitable
methodologies, others, including Italy, lack procedures tested at the national level. The aim of this
work is to propose a method to assess the conservation status of habitat 92A0 (Salix alba and
Populus alba galleries) in central Italy, and to test the method using data from the Molise region.
We selected parameters that highlight the conservation status of the flora and vegetation in order
to assess habitat structures and functions at the site level. After selecting the parameters, we
tested them on a training dataset of 22 unpublished phytosociological relevés taken from the whole
dataset, which consists of 119 relevés (49 unpublished relevés for the study area, and 70 published
relevés for central Italy). We detected the most serious conservation problems in the middle and
lower course of the Biferno river: the past use of river terraces for agriculture and continual human
eScholarship provides open access, scholarly publishing
services to the University of California and delivers a dynamic
research platform to scholars worldwide.
interventions on the river water flow have drastically reduced the riparian forests of Molise. Our
results show that in areas in which forest structure and floristic composition have been substantially
modified, certain alien plant species, particularly Robinia pseudoacacia, Amorpha fruticosa and
Erigeron canadensis, have spread extensively along rivers. In the management of riparian forests,
actions aimed at maintaining the stratification of the forest, its uneven-agedness and tree species
richness may help to ensure the conservation status, as well as favour the restoration, of habitat
92A0.
Copyright Information:
Copyright 2016 by the article author(s). This work is made available under the terms of the Creative
Commons Attribution4.0 license, http://creativecommons.org/licenses/by/4.0/
Biogeographia – The Journal of Integrative Biogeography 31 (2016): 7–25
Monitoring Natura 2000 habitats:
habitat 92A0 in central Italy as an example
EMANUELA CARLI1,*, EVELINA D’ALESSANDRO2,
PIERA DI MARZIO3, CARMEN GIANCOLA3, BRUNO PAURA2,
GIOVANNI SALERNO4, CARLO BLASI1
1 Dipartimento di Biologia Ambientale, ‘Sapienza’ Università di Roma (Italy)
2 Dipartimento di Agricoltura, Ambiente e Alimenti, Università del Molise (Italy)
3 Dipartimento di Bioscienze e Territorio, Università del Molise (Italy)
4 Dipartimento di Scienze per la Biologia, la Geologia e l’Ambiente, Università degli Studi del Sannio (Italy)
* e-mail corresponding author: piera.dimarzio@unimol.it
Keywords: alien species, Article 17, conservations status, plant community indicators, plant species
indicators, riparian forests.
SUMMARY
The evaluation and the subsequent monitoring of the conservation status of habitats is one of the key
steps in nature protection. While some European countries have tested suitable methodologies, others,
including Italy, lack procedures tested at the national level. The aim of this work is to propose a method
to assess the conservation status of habitat 92A0 (Salix alba and Populus alba galleries) in central Italy,
and to test the method using data from the Molise region. We selected parameters that highlight the
conservation status of the flora and vegetation in order to assess habitat structures and functions at the
site level. After selecting the parameters, we tested them on a training dataset of 22 unpublished
phytosociological relevés taken from the whole dataset, which consists of 119 relevés (49 unpublished
relevés for the study area, and 70 published relevés for central Italy). We detected the most serious
conservation problems in the middle and lower course of the Biferno river: the past use of river terraces
for agriculture and continual human interventions on the river water flow have drastically reduced the
riparian forests of Molise. Our results show that in areas in which forest structure and floristic
composition have been substantially modified, certain alien plant species, particularly Robinia
pseudoacacia, Amorpha fruticosa and Erigeron canadensis, have spread extensively along rivers. In
the management of riparian forests, actions aimed at maintaining the stratification of the forest, its
uneven-agedness and tree species richness may help to ensure the conservation status, as well as favour
the restoration, of habitat 92A0.
Biogeographia 31: 7–25 Carli et al., 2016
8
Abbreviations: FV = favourable; SCI = Site of Community Importance; SPA = Special Protection
Area; U1 = unfavourable inadequate; U2 = unfavourable bad.
INTRODUCTION
According to European Directive 92/43/EEC, better known as the Habitat Directive, member states are
required to preserve, or restore to a favourable conservation status, habitats within the Natura 2000
Network, that is Sites of Community Importance (SCIs) and Special Protection Areas (SPAs). The
conservation of such habitats can only be guaranteed by effective monitoring. The Habitat Directive
requires the identification and evaluation of the defining characteristics of the habitats, as well as the
threats that affect their current status or that may damage them in the future. According to Article 17 of
the Directive, the conservation status of a natural habitat is considered favourable when its area of
natural distribution is stable or expanding, when the structure and functions specific to its long-term
maintenance exist and are not exposed to future threats, and when the conservation status of its typical
species is favourable. While some European countries (JNCC 2004, BfN 2006, Calleja 2009, Carnino
2009) have already designed appropriate methods to monitor the conservation status of habitats, others
have yet to introduce standard procedures adopted on a national level. The latter group of countries
includes Italy, even though evaluations of Italian habitats, based on expert knowledge, have been
performed and were published in the 3rd National Report ex-art. 17 Habitat Directive (92/43/EC)
(www.sinanet.isprambiente.it/Reporting_Dir_Habitat).
Riparian habitats represent one of the ecosystems threatened most by human activities,
particularly by changes in water regimes, the management of riparian vegetation and pollution (Allan
& Flecker 1993, Liendo et al. 2015), as recently highlighted also in central Italy by Viciani et al.
(2014). Indeed, nearly 20% of the research projects that have been conducted in recent years have
focused on freshwater habitats, as highlighted by the EuMon database on monitoring methods and
systems of surveillance for species and habitats of community interest
(http://eumon.ckff.si/index1.php).
Changes in water regimes, as well as other types of human disturbance, can facilitate the spread
of invasive alien species (Liendo et al. 2015). Indeed, riparian environments are, owing to their
inherent predisposition to disturbance, among the environments most prone to invasions of non-native
species (Stohlgren et al. 1998, Chytrý et al. 2008). Since the publication of the Italian checklist of non-
native flora (Celesti-Grapow et al. 2009, 2010), which raised considerable interest in plant invasions
among local botanists, an increasing amount of attention has been paid to alien plant species in Italy.
Despite this, the amount of information available in Italy is still incomplete, as highlighted by Assini
(2000) for wet areas, and the experience limited, particularly for riparian habitats, if compared with
other European and non-European countries (Pyšek and Prach 1993, Richardson et al. 2007, Schnitzler
et al. 2007).
Forests dominated by Salix alba or Populus alba are widespread in the majority of
Mediterranean EU member states, though their distribution is scattered
(http://natura2000.eea.europa.eu/) owing to their ecological requirements. A specific monitoring
strategy for Salix alba and Populus alba forests based on plant species and community indicators may
prove useful to other member states in the Mediterranean area insofar as such forests are azonal. The
aim of this study is to help fill this gap by proposing a suitable method to assess the conservation status
of habitat 92A0 (Salix alba and Populus alba galleries) by testing field data from the Molise region,
Carli et al., 2016 Biogeographia 31: 7–25
9
and to shed light on the reasons underlying the expansion of invasive plant species in these
environments.
We believe that our case study may be considered a useful example of conservation status
assessment of fresh water habitats in central Italy.
MATERIALS AND METHODS
In Table 1, we list the Natura 2000 sites (SCI/SPAs) included in the study area (Fig. 1), together with
the area of the sites and the area covered by the study habitat in each site, derived from the Natura 2000
database (update 2012) (http://www.eea.europa.eu/data-and-maps/data/natura-2000). Although the
majority of the sample plots were selected from Natura 2000 sites, some fall within the Biferno river
basin and are located outside of the Natura 2000 Network. Owing to the scattered distribution of
residual areas with riparian forests belonging to habitat 92A0, for the sampling design, we identified
the sites for the sample plots after selecting potential areas referred to these forests by integrating the
map of the Natura 2000 habitats in Molise
(http://www3.regione.molise.it/flex/cm/pages/ServeBLOB.php/L/IT/IDPagina/657) and the map of the
Nature (http://www.isprambiente.gov.it/en/environmental-services/map-of-the-nature-
system?set_language=en). Although the number of relevés is not particularly high, we believe that this
selection process yields a fairly accurate representation of the current situation of riparian forests in the
Molise region.
The vegetation sampling was performed mainly by means of the phytosociological method
(Braun-Blanquet 1931, Dengler et al. 2008, Biondi 2011). This method, based on relevés conducted in
areas with homogeneous vegetation, records the species and their coverage (as of percentage of the
relevé area) and describes the local environment (Mucina et al. 2000). These relevés are aimed at
characterising plant communities and identifying the habitat (Biondi et al. 2009).
We first carried out 22 relevés, with a mean area of 70 m2, located in the courses of the all the
main rivers in the region except the Volturno and Fortore rivers. A vegetation database was created in
Turboveg 2.0 (Hennekens 1995), starting from these 22 original relevés, which were then integrated
using a further 27 unpublished relevés conducted along the Biferno river (B. Paura and collaborators,
unpublished data), and 70 from the Adriatic side of the Apennines in central and southern Italy, derived
from literature (Pedrotti 1970, 1984, Pedrotti and Cortini-Pedrotti 1978, Pirone 1981, 2000, Pirone et
al. 1997, Manzi 1988, 1993, Biondi et al. 2002, Baldoni and Biondi 1993, CUM 2002, Allegrezza
2003, Allegrezza et al. 2006).
The 49 unpublished relevés were classified by means of cluster analysis using Past 2.1
(algorithm UPGMA, and Ochiai distance on species cover/presence) (Hammer et al. 2001).
The conservation status was assessed in each site by estimating the characteristics of the habitat
and the threats it was exposed to. We focused on the type of data that can be collected from flora and
vegetation surveys, adopting those parameters proposed in other member states (JNCC 2004, BfN
2006, Calleja 2009, Carnino 2009) that we considered to apply most to our study area. We then
obtained the threshold values for the parameters by using our whole dataset (119 relevés), classifying
them according to natural breaks (Jenks 1967). We decided to use natural breaks for classification
purposes because we considered them to be more representative of the variation of our data. Table 2
summarizes the three types of parameters and the threshold values of the corresponding indicators used
to assess the conservation status.
Biogeographia 31: 7–25 Carli et al., 2016
10
To assess the structure of the forest vegetation, we selected the following indicators: (i) the
cover of the native tree layer and of the shrub layer (h 2-5 m) to highlight the stratification of the
vegetation (JNCC 2004, Calleja 2009); (ii) the number of diameter classes of the tree trunks, which
provide information on the uneven-agedness of the forest and the presence and type of forest
management (BfN 2006, Carnino 2009); (iii) the presence of dead wood (relative cover in each relevé
of woody debris and/or standing dead wood, and the presence of fallen old trees), to highlight the
absence of management or natural forest management (BfN 2006, Carnino 2009).
FIGURE 1. Study area showing the location of the 22 relevés (white stars) assessed and the selected
Natura 2000 sites in Molise region (grey areas). The inlet shows the position of Molise in Italy.
TABLE 1. List of Natura 2000 sites included in the study area, showing the area covered by each site and the
area covered by habitat 92A0 (including other habitat types that may form a mosaic of riparian vegetation with
habitat 92A0) (http://www.eea.europa.eu/data-and-maps/data/natura-4).
Carli et al., 2016 Biogeographia 31: 7–25
11
Site_code
Site_name
Habitat_code
Site_area
Habitat_cover_ha
IT7211120
Torrente Verrino
92A0, 3280
93
34.41
IT7212124
Bosco Monte di Mezzo - Monte Miglio - Pennataro
- Monte Capraro - Monte Cavallerizzo
3954
IT7212126
Pantano Zittola - Feudo Valcocchiara
92A0, 3260
1246
14.95
IT7212134
Bosco di Collemeluccio - Selvapiana - Castiglione -
La Cocozza
6239
62.39
IT7218213
Isola della Fonte della Luna
92A0
867
86.7
IT7222247
Valle Biferno da confluenza Torrente Quirino al
Lago Guardalfiera - Torrente Rio
92A0, 3260
368
228.16
IT7222249
Lago di Guardialfiera - M. Peloso
92A0
2848
56.96
IT7222287
La Gallinola - Monte Miletto - Monti del Matese
92A0
25002
50
IT7228229
Valle Biferno dalla diga a Guglionesi
92A0, 3260, 3280
356
106.8
IT7222237
Fiume Biferno (confluenza Cigno - alla foce
esclusa)
92A0, 3280
133
42.56
IT7228230
Lago di Guardialfiera - Foce fiume Biferno
28724
TABLE 2. Parameters used in the study to assess the conservation status and their relative indicator values. List
of the abbreviations: tree_cov = tree cover; sh_cov = shrub cover; ages = number of diameter classes; dead =
dead wood; FC = floristic consistency; tree-rich = tree species richness; alien = presence of alien species; interest
= presence of species of interest; FV = favourable; U1 = unfavourable inadequate; U2 = unfavourable bad.
Parameters
Threshold value
Assessment
tree_cov
≥ 60%
F
U1
< 30%
U2
sh_cov
≥ 60%
F
U1
< 20%
U2
ages
≥ 3
F
U1
1
U2
dead
fallen old trees
F
woody debris and standing dead wood
F
woody debris and standing dead wood
U1
absent
U2
FC
≥ 40%
F
U1
< 15%
U2
weed_alien
absent
F
< 5%
U1
> 5%
U2
tree_rich
≥ 3
F
U1
< 3
U2
interest
present
F
absent
-
We selected the following floristic and vegetation indicators: (i) the floristic consistency of the
communities detected (JNCC 2004, BfN 2006, Calleja 2009, Carnino 2009) with the vegetation of
reference, by comparing the presence of diagnostic and frequent species for the alliances (Biondi et al.
Biogeographia 31: 7–25 Carli et al., 2016
12
2014; http://www.prodromo-vegetazione-italia.org/); (ii) the presence and cover of exotic species,
which reduce the degree of naturalness (JNCC 2004, Carnino 2009); (ii) the native tree species
richness, which is particularly marked in Italian old-growth forests (Burrascano et al. 2009), and known
to be a good proxy for the total richness (Abbate et al. 2015); (iv) the presence of species of
biogeographic or conservation interest, selected from Red Lists and other lists of protected or rare
species (Table 3), which highlight the peculiarities of the site (BfN 2006).
TABLE 3. List of species of biogeographic or conservation interest selected from Red Lists (Conti et
al. 1992, 1997, Rossi et al. 2013) and other lists of protected or rare species (Directive 92/43/EC,
http://www.societabotanicaitaliana.it/cites/index.asp, Lucchese 1995, 1996, Regione Molise 1999,
Fortini e Viscosi 2008); List of abbreviations: CR = Critically Endangered; EN = Endangered; LR =
Low Risk; NT = Near Threatened; VU = Vulnerable.; HD = Council Directive 92/43/EEC; CITES =
Council Regulation (EC) No 338/97; Reg. = Regione Molise, Legge Regionale 23 febbraio 1999 n°9.
Species
Conti et al. 1992 or
Rossi et al. 2013
Conti et al. 1997
Protected species
Rare species
Acer cappadocicum Gled. subsp.
lobelii (Ten.) A.E.Murray (≡ Acer
lobelii Ten.)
LR
LR
Alopecurus bulbosus Gouan
EN
Reg.
x
Anacamptis palustris (Jacq.) R.M.
Bateman, Pridgeon & M.W.Chase (≡
Orchis palustris Jacq.)
EN
CR
Reg.
x
Asparagus acutifolius L.
LR
Caltha palustris L.
EN
Reg.
x
Carex paniculata L. subsp.
paniculata
CR
Reg.
x
Carex pseudocyperus L.
CR
Reg.
x
Cicuta virosa L.
EN
Clematis viticella L.
EN
Cucubalus baccifer L.
LR
Dactylorhiza incarnata (L.) Soó
subsp. incarnata
EN
Reg.
x
Dactylorhiza maculata (L.) Soó (≡
Orchis maculata L.)
HD, CITES
Dichoropetalum schottii (Besser ex
DC.) Pimenov & Kljuykov (≡
Peucedanum schottii Besser ex DC.)
CR
Reg.
x
Epilobium palustre L.
CR
Epipactis palustris (L.) Crantz
NT
CR
Reg.
x
Euphorbia palustris L.
CR
Reg.
x
Helosciadium inundatum (L.)
W.D.J.Koch (≡ Apium inundatum
(L.) Rchb. f.)
EN
Reg.
x
Isoëtes durieui Bory
CR
Reg.
x
Limniris pseudacorus (L.) Fuss (≡
Iris pseudacorus L.)
VU
Lomelosia graminifolia (L.) Greuter
& Burdet (≡ Scabiosa graminifolia
LR
Carli et al., 2016 Biogeographia 31: 7–25
13
Species
Conti et al. 1992 or
Rossi et al. 2013
Conti et al. 1997
Protected species
Rare species
L.)
Menyanthes trifoliata L.
CR
Reg.
x
Myosurus minimus L.
EN
Reg.
x
Ophioglossum vulgatum L.
EN
Reg.
x
Orobanche flava Mart. ex F.W.
Schultz
EN
Reg.
x
Persicaria amphibia (L.) Delarbre (≡
Polygonum amphibium L.)
CR
Reg.
x
Peucedanum officinale L. subsp.
officinale
CR
Reg.
x
Ranunculus flammula L.
VU
EN
Reg.
x
Ranunculus lingua L.
VU
CR
Reg.
x
Ruscus aculeatus L.
HD
Salix cinerea L.
LR
Salix fragilis L.
VU
Salix pentandra L.
EN
CR
Reg.
x
Sparganium emersum Rehmann
CR
Reg.
x
Thelypteris palustris Schott
EN
Reg.
x
Triglochin bulbosum L. subsp.
barrelieri (Loisel.) Rouy
EN
Reg.
x
Trollius europaeus L. subsp.
europaeus
EN
Reg.
x
Utricularia vulgaris L.
CR
x
We tested the parameters we selected on a training dataset, i.e. 22 relevés that we carried out in
the Molise Region. In this way, we only considered the most recent relevés, for conservation status
assessment purposes.
When assessing the conservation status of forests in the Mediterranean area, it should be noticed
that, owing to the impact of man over the millennia, forest habitats that have either never been used by
humans or were only used in very ancient times are extremely rare. We cannot consequently expect the
best-preserved context to be represented by a primeval forest (Carnino 2009). This is why we decided
to determine the threshold values of the parameters for the best-conserved situations based on our
whole dataset.
The resulting synthetic assessment for each relevé is determined by the condition of the worst
parameter, as suggested by Article 17 of the Habitat Directive (92/43/EEC).
RESULTS
Biogeographia 31: 7–25 Carli et al., 2016
14
The cluster analysis led to the identification of two main types of riparian forests, referred to Salicion
albae Soó 1930 (55% of the 49 unpublished relevés) and to Populion albae Br.-Bl. ex Tchou 1948
(45%).
The species recorded in more than 40% of the relevés are Salix alba, Rubus ulmifolius,
Brachypodium sylvaticum, Salix purpurea, Populus nigra, Cornus sanguinea and Urtica dioica (see
Supplementary Table S1 for the complete list).
Fourteen of the 22 relevés were found to have an Unfavourable-Bad (U2) conservation status.
The worst parameters, indicating a bad conservation status, were mainly richness of the native trees
species and shrub cover.
TABLE 4. Assessment of the conservation status of habitat 92A0 in our study area. List of the abbreviations:
tree_cov = tree cover; sh_cov = shrub cover; ages = number of diameter classes of the tree trunks; dead = dead
wood; FC = floristic consistency; tree-rich = tree species richness; alien = presence of alien species; interest =
presence of species of interest; FV = favourable; U1 = unfavourable inadequate; U2 = unfavourable bad.
relevé
type of vegetation
tree_
cov
sh_ cov
ages
dead
char_ab
u
tree_
rich
weed_a
lien
interest
general
assessment
1
forest of Salix alba
FV
FV
FV
FV
FV
FV
FV
FV
FV
2
forest of Populus alba
FV
FV
FV
FV
FV
FV
FV
-
FV
3
forest of Populus alba
FV
FV
FV
FV
FV
FV
FV
-
FV
4
forest of Populus alba
U1
FV
FV
FV
FV
U1
FV
-
U1
5
forest of Populus alba
FV
FV
FV
U1
FV
U1
FV
-
U1
6
forest of Salix alba
FV
FV
FV
U1
FV
U1
FV
FV
U1
7
forest of Populus alba
FV
FV
FV
U1
FV
U1
FV
-
U1
8
forest of Populus alba
FV
FV
FV
U1
FV
U1
U2
-
U2
9
forest of Populus alba
FV
FV
U1
U2
FV
FV
U2
-
U2
10
forest of Populus alba
FV
FV
FV
FV
FV
U2
U2
-
U2
11
forest of Populus alba
U1
FV
FV
-
FV
FV
U2
-
U2
12
forest of Populus alba
FV
FV
U1
FV
FV
U2
U2
-
U2
13
forest of Populus alba
FV
FV
FV
FV
U2
U2
U2
-
U2
14
forest of Salix alba
FV
FV
U1
U1
FV
U2
U2
-
U2
15
forest of Salix alba
U1
FV
FV
U1
U2
FV
U2
-
U2
16
forest of Populus alba
FV
U2
U1
U2
U1
FV
U2
-
U2
17
forest of Populus alba
U2
U2
U1
FV
FV
U2
U2
-
U2
18
forest of Salix alba
FV
U2
U1
U2
U2
U2
U2
-
U2
19
shrub veg. (Salix sp. pl.)
-
-
-
-
FV
-
FV
FV
U1
20
shrub veg. (Salix sp. pl.)
-
-
-
-
FV
-
U2
-
U2
21
shrub veg. (Salix sp. pl.)
-
-
-
-
2
-
U2
-
U2
22
shrub veg. (Salix sp. pl.)
-
-
-
-
-1
-
U2
-
U2
We detected a marked difference between the western and eastern parts of the region (relevés n°
1 and 2 in Table 4). The site with the best conservation status was located in SCI IT7218213, where the
native tree species richness and the presence of woody debris, two surrogates for the natural or semi-
Carli et al., 2016 Biogeographia 31: 7–25
15
natural evolution of the forest, are very good. The majority of the relevés in the Campobasso province
(in the east) were found to have an unfavourable conservation status. In the surroundings of IT7222287
lies the only riparian forest in which we found a favourable conservation status (relevé n° 3),
particularly as regards the native tree species richness and the presence of woody debris, which were
comparable to those detected in the aforementioned site n° 2.
DISCUSSION
The Molise region is characterized by a strong altitudinal gradient and by the presence of large river
valleys (e.g. Volturno and Biferno) that connect the two sides of the Apennines. These valleys have
always allowed the migration of plant species (Lucchese 1995, Paura et al. 2010b). These migrations
are now represented by invasive exotic species. Indeed, it is along the rivers that the greatest spread of
invasive species has been witnessed in the region (Lucchese 2010). Rivers play an important role in the
invasion of plant species insofar as their waters act as important agents of propagule dispersal, just as
aquatic birds do. In addition, periodic disturbance events, due to floods, create openings in plant cover
that can easily be colonized by alien plant species thanks to the availability of nutrients. Low water
periods also provide areas that are exposed to colonization by pioneer annual plants. Lastly, the rivers
are subject to anthropogenic disturbance (agriculture, urbanization, water regimentations, etc.), which
also promotes the spread of invasive species (Stohlgren et al. 1998, Schnitzler et al. 2007).
Riparian forests are known to be azonal formations that are conditioned mainly by the water
level and water regime (Pedrotti and Gafta 1996). Although such forests are very dynamic owing to the
natural disturbance to which they are subjected, they remain relatively stable if the hydrogeological
conditions do not change. Riparian forests belonging to habitat 92A0 can be divided in two types, as
described in the national interpretation manual (Biondi et al. 2012). They differ in dominant tree
species and from an ecological point of view. Willow groves are located on the lower terraces, which
are affected regularly by the ordinary flooding of the river, while poplar forests colonize the upper
terraces, which are only sporadically affected by extraordinary flooding. The aforementioned manual
recognized two different alliances of reference: Populion albae Br.-Bl. ex Tchou 1948 and Salicion
albae Soó 1930 (Biondi et al. 2014).
The most recent European Interpretation Manual describes habitat 92A0 as "Riparian forests of
the Mediterranean basin dominated by Salix alba, Salix fragilis or their relatives. Mediterranean and
Central Eurasian multi-layered riverine forests with Populus spp. [...]" (European Commission 2007).
The name of the habitat makes explicit reference to gallery forests, sometimes generating difficulty in
recognizing the habitat where riparian forest conservation does not preserve this aspect. In Spain,
Calleja (2009) has proposed extending the definition to include the intermediate stages of vegetation
dominated by shrubby willows with sparse trees of Salix alba and Populus alba. We agree with this
proposal and have included forests of Populus alba, Populus nigra and Salix alba and shore vegetation
dominated by shrubby willows, with some willow trees or poplars, in this study.
Our study identified two types of riparian forests, as expected for habitat 92A0: Salicion albae
and Populion albae (Biondi et al. 2009, 2014). The main difference between these two types of forest
lies in the dominant tree species (Salix or Populus species), there being little difference in the
understory flora. Our findings are confirmed by data in the literature. Indeed, as shown in previous
works on riparian vegetation (Pirone 1981, 2000, Pedrotti 1984, Manzi 1988, 1993), the general
impoverishment of the flora of poplar forests in central Italy, due to the past use of this habitat by
humans for agricultural purposes, makes it somewhat difficult to distinguish them from willow forests.
Furthermore, the forests of Populus alba, which are affected to a lesser extent by river flooding, are
Biogeographia 31: 7–25 Carli et al., 2016
16
also characterized by species that belong to oak forests, as highlighted in Molise by Paura et al.
(2010a). It is likely that ISPRA (Institute for Environmental Protection and Research) included the
Mediterranean tall willow galleries (EUNIS code 44.41) in the Italian poplar galleries (EUNIS code
44.614) on account of the floristic similarity between poplars and willows forests in the Apennines (for
more information see http://www.isprambiente.gov.it/files/carta-della-natura/catalogo-habitat.pdf).
The rivers in central and southern Italy do not tend to create large floodplains that lend
themselves to intensive agriculture. Human activities in these two regions have resulted in substantial
changes in the flora and vegetation, particularly as a result of works related to riverbank reinforcement
and to the production of electricity. These changes have often promoted the establishment and spread
of exotic plant species (Lucchese 2010). The riparian forests of willows and poplars examined in this
study revealed a peculiar susceptibility to human intervention and displayed considerably different
features if compared with the past (Pedrotti and Cortini-Pedrotti 1978, Pedrotti 1984).
The most serious conservation problems were detected along the lower course of the Biferno
river, in the Campobasso province. The past land use of river terraces and the continual human
interventions have led to only small portions of what was once likely to have been the richest lowland
forest in Molise being left, such as that near Colle d'Anchise, which lies out of the Natura 2000
Network (relevés n° 3 in Table 3), and where a well-preserved forest still exists. This area has not yet
been included as a Natura 2000 site. It is a very rich poplar forest that is well stratified and contains a
large amount of woody debris, standing dead wood and fallen old trees. In order to promote the natural
evolution of this forest and its conservation, the boundaries of SCI IT7222247 "Valle Biferno da
confluenza Torrente Quirino al Lago Guardalfiera - Torrente Rio" should be redrawn in such a way as
to include the forest of Colle d'Anchise in the Natura 2000 network.
A better state of preservation is found in the areas that lie in the upper course of the rivers,
where human impact is less marked and there are few exotic species. The site with the best
conservation status is SCI IT7218213 "Isola Fonte della Luna" (relevés n°2 in Table 4), which has been
unmanaged for approximately 30 years. As shown in Table 4, the structure of the forest is fairly well
preserved and nine tree species were been found, which is the highest number recorded in the study
area.
Exotic species tend to be promoted in areas in which the structure and floristic composition of
the forest are substantially compromised. This is particularly evident in relevés n°17 in the Biferno
valley (in the proximity of Morgia dell’Eremita), where the poplar layer has been completely replaced
by Robinia pseudoacacia. The poor conservation status of the poplar forests in the lower course of the
Biferno river may have been caused by the overall reduction in the size of this habitat, following the
replacement in many areas of riparian forests by cultivated fields, a trend first observed in the 1970s in
central and southern Italy (Pedrotti 1970, 1984, Manzi 1988, 1993). It is in the woods in this area that
we observed the greatest spread of alien plant species such as Robinia pseudoacacia, Amorpha
fruticosa and Erigeron canadensis. A similar trend has been observed for the willow forests in the Po
Plain (Poldini et al. 2011). We should not forget that the success of invasive plant species is often the
result of a poor conservation status of riparian habitats (Stohlgren et al. 1998, Chytrý et al. 2009,
Liendo et al. 2015).
The introduction and spread of these invasive species appear to be promoted in areas in which
trees and shrub layers are not well developed. Indeed, alien species were not recorded in sites with a
favourable conservation status, particularly as regards the structure. In conclusion, we believe that
forest management should focus on maintaining the stratification of the forest, its uneven-agedness and
Carli et al., 2016 Biogeographia 31: 7–25
17
tree species richness because a forest can withstand the invasion of alien species only as long as its
structure is well preserved and strong.
ACKNOWLEDGEMENTS
This study is a part of “Management Plan of 10 SCI/SPAs in Molise”, a research project conducted in
the years 2010-2013 funded by the Italian Ministry for the Environment, Land and Sea Protection.
Thanks to Luisa Battista for the help in the field sampling.
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Edited by Lorenzo Peruzzi
Carli et al., 2016 Biogeographia 31: 7–25
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SUPPLEMENTARY TABLE S1. List of species, number of relevés in which they are present,
and relative frequency.
Species
N° relevés
frequency
Acer campestre L.
9
0.41
Acer cappadocicum Gled. subsp. lobelii (Ten.) A.E.Murray
2
0.09
Acer opalus Mill. subsp. obtusatum (Waldst. & Kit. ex Willd.) Gams
2
0.09
Acer pseudoplatanus L.
7
0.32
Aegopodium podagraria L.
2
0.09
Agrostis stolonifera L.
7
0.32
Alisma plantago-aquatica L.
7
0.32
Alnus glutinosa (L.) Gaertn.
4
0.18
Alopecurus myosuroides Huds.
5
0.23
Alopecurus utriculatus (L.) Pers.
5
0.23
Amorpha fruticosa L.
11
0.50
Anisantha diandra (Roth) Tutin ex Tzvelev
6
0.27
Anisantha sterilis (L.) Nevski
3
0.14
Anthoxanthum odoratum L.
5
0.23
Artemisia verlotorum Lamotte
5
0.23
Artemisia vulgaris L.
5
0.23
Arum italicum Miller
2
0.09
Arundo pliniana Turra
7
0.32
Berula erecta (Huds.) Coville
9
0.41
Bidens frondosa L.
11
0.50
Bolboschoenus maritimus (L.) Palla
2
0.09
Brachypodium sylvaticum (Huds.) P.Beauv.
18
0.82
Bromopsis benekenii (Lange) Holub
2
0.09
Bromus hordeaceus L.
6
0.27
Bryonia dioica Jacq.
7
0.32
Calystegia sepium (L.) R.Br.
7
0.32
Carex hirta L.
5
0.23
Carex otrubae Podp.
7
0.32
Carex pendula Huds.
8
0.36
Cerastium holosteoides Fr.
5
0.23
Chenopodium album L.
3
0.14
Cirsium creticum (Lam.) d’Urv.
5
0.23
Clematis vitalba L.
11
0.50
Convolvulus arvensis L.
5
0.23
Cornus mas L.
6
0.27
Cornus sanguinea L.
16
0.73
Corylus avellana L.
3
0.14
Cota tinctoria (L.) J.Gay
2
0.09
Crataegus monogyna Jacq.
15
0.68
Biogeographia 31: 7–25 Carli et al., 2016
22
Species
N° relevés
frequency
Crepis vesicaria L.
5
0.23
Cucubalus baccifer L.
6
0.27
Cynosurus cristatus L.
5
0.23
Dactylis glomerata L.
6
0.27
Dactylorhiza incarnata (L.) Soó
5
0.23
Daphne laureola L.
2
0.09
Daucus carota L.
4
0.18
Digitalis micrantha Roth
2
0.09
Dioscorea communis (L.) Caddick & Wilkin
2
0.09
Dipsacus laciniatus L.
3
0.14
Dittrichia viscosa (L.) Greuter
3
0.14
Doronicum orientale Hoffm.
2
0.09
Eleocharis palustris (L.) Roem. & Schult.
5
0.23
Epilobium hirsutum L.
10
0.45
Equisetum arvense L.
3
0.14
Equisetum ramosissimum Desf.
3
0.14
Equisetum telmateja Ehrh.
7
0.32
Erigeron canadense L.
8
0.36
Euonymus europaeus L.
13
0.59
Eupatorium cannabinum L.
4
0.18
Euphorbia amygdaloides L.
5
0.23
Euphorbia helioscopia L.
2
0.09
Foeniculum vulgare Mill.
2
0.09
Fraxinus ornus L.
3
0.14
Galium aparine L.
5
0.23
Galium palustre L.
5
0.23
Geranium robertianum L.
9
0.41
Geranium versicolor L.
5
0.23
Geum urbanum L.
11
0.50
Glyceria plicata Fries
5
0.23
Hedera helix L.
10
0.45
Helianthus tuberosus L.
2
0.09
Helleborus foetidus L.
3
0.14
Helminthotheca echioides (L.) Holub
2
0.09
Heracleum sphondylium L.
6
0.27
Holcus lanatus L.
9
0.41
Hordeum bulbosum L.
5
0.23
Humulus lupulus L.
6
0.27
Hypericum tetrapterum Fries
7
0.32
Juglans regia L.
2
0.09
Juncus articulatus L.
5
0.23
Carli et al., 2016 Biogeographia 31: 7–25
23
Species
N° relevés
frequency
Juniperus communis L.
2
0.09
Lactuca muralis (L.) Gaertn.
3
0.14
Lactuca serriola L.
3
0.14
Lapsana communis L.
7
0.32
Lepidium campestre (L.) R.Br.
2
0.09
Ligustrum vulgare L.
11
0.50
Lycium europaeum L.
2
0.09
Lycopus europaeus L.
14
0.64
Lysimachia vulgaris L.
3
0.14
Lythrum salicaria L.
7
0.32
Malus sylvestris Mill.
5
0.23
Melica uniflora Retz.
2
0.09
Melilotus alba Medicus
3
0.14
Mentha aquatica L.
8
0.36
Mentha longifolia (L.) Huds.
8
0.36
Mentha pulegium L.
5
0.23
Muscari comosum (L.) Mill.
5
0.23
Myosotis scorpioides L.
5
0.23
Oenanthe pimpinelloides L.
5
0.23
Paspalum paspaloides (Michx.) Scribner
10
0.45
Persicaria amphibia (L.) Delarbre
7
0.32
Persicaria hydropiper (L.) Delarbre
2
0.09
Petasites hybridus (L.) G.Gaertn., B.Mey. & Scherb.
6
0.27
Petasites pyrenaicus (L.) G.López
3
0.14
Phalaris paradoxa L.
2
0.09
Phragmites australis (Cav.) Trin.
7
0.32
Picris hieracioides L.
4
0.18
Pimpinella peregrina L.
2
0.09
Plantago lanceolata L.
6
0.27
Plantago major L.
4
0.18
Poa trivialis L.
11
0.50
Populus alba L.
14
0.64
Populus nigra L.
17
0.77
Potentilla reptans L.
6
0.27
Prunus spinosa L.
9
0.41
Pulmonaria apennina Cristof. & Puppi
4
0.18
Pyrus communis L. subsp. pyraster (L.) Ehrh.
5
0.23
Quercus cerris L.
2
0.09
Quercus pubescens Willd.
6
0.27
Ranunculus lanuginosus L.
3
0.14
Ranunculus repens L.
8
0.36
Biogeographia 31: 7–25 Carli et al., 2016
24
Species
N° relevés
frequency
Ranunculus sardous Crantz
5
0.23
Ranunculus serpens Schrank
2
0.09
Ranunculus trichophyllus Chaix
6
0.27
Rhinanthus alectorolophus (Scop.) Pollich
5
0.23
Robinia pseudoacacia L.
9
0.41
Rorippa sylvestris (L.) Besser
5
0.23
Rosa arvensis Huds.
2
0.09
Rubus caesius L.
6
0.27
Rubus ulmifolius Schott
20
0.91
Rumex conglomeratus Murray
3
0.14
Rumex crispus L.
5
0.23
Salix alba L.
22
1.00
Salix eleagnos Scop.
5
0.23
Salix fragilis L.
5
0.23
Salix pentandra L.
5
0.23
Salix purpurea L.
17
0.77
Salix triandra L.
4
0.18
Salvia glutinosa L.
2
0.09
Sambucus nigra L.
11
0.50
Saponaria officinalis L.
3
0.14
Scirpoides holoschoenus (L.) Soják
4
0.18
Scrophularia umbrosa Dumort.
7
0.32
Sherardia arvensis L.
2
0.09
Sinapis alba L.
4
0.18
Solanum dulcamara L.
4
0.18
Sonchus asper (L.) Hill
6
0.27
Sparganium erectum L.
6
0.27
Stachys sylvatica L.
10
0.45
Stellaria media (L.) Vill.
2
0.09
Symphyotrichum squamatum (Spreng.) G.L.Nesom
5
0.23
Taraxacum F.H.Wigg. sect. Taraxacum
5
0.23
Tordylium maximum L.
9
0.41
Torilis nodosa (L.) Gaertn.
2
0.09
Trifolium brutium Ten.
5
0.23
Trifolium pratense L.
6
0.27
Trifolium repens L.
7
0.32
Trifolium resupinatum L.
5
0.23
Typha angustifolia L.
2
0.09
Typha latifolia L.
8
0.36
Ulmus minor Mill.
9
0.41
Urtica dioica L.
16
0.73
Carli et al., 2016 Biogeographia 31: 7–25
25
Species
N° relevés
frequency
Valeriana officinalis L.
5
0.23
Veronica anagallis-aquatica L.
2
0.09
Veronica beccabunga L.
4
0.18
Veronica catenata Pennell
5
0.23
Vicia sepium L.
2
0.09
Viola alba Besser
5
0.23
Xanthium italicum Moretti
4
0.18
Xanthium spinosum L.
2
0.09