Here to stay. Recent advances and perspectives about Acacia invasion in Mediterranean areas

Abstract

The above- and belowground impacts due to Acacia invasions have been described in detail over the last 25 years. Future research should focus on the earlyd etection and prevention of new Acacia introductions and on a cost-effective and sustainable management of the novel ecosystems resulting from invasions.

Full text

REVIEW PAPER
Here to stay. Recent advances and perspectives
about Acacia invasion in Mediterranean areas
Pablo Souza-Alonso
1
&Jonatan Rodríguez
1
&Luís González
1
&Paula Lorenzo
2
Received: 30 August 2016 /Accepted: 12 June 2017
#INRA and Springer-Verlag France SAS 2017
Abstract
•Key message The above- and belowground impacts due
to Acacia invasions have been described in detail over the
last 25 years. Future research should focus on the early
detection and prevention of new Acacia introductions and
on a cost-effective and sustainable management of the nov-
el ecosystems resulting from invasions.
•Context Invasive alien plants (IAPs) strongly alter ecosys-
tems reducing biodiversity, modifying ecosystem services and
increasing negative impacts at social and economic level.
Among invasive taxa, Acacia is a highly problematic genus
worldwide. In fact, almost 500 papers have been published on
several aspects of Acacia invasions for the last 25 years.
•Aims We aim at reviewing the current knowledge on the
consequences of the invasion by Acacia genus in
Mediterranean ecosystems. We also collect and propose dif-
ferent approaches for the management and recovery of invad-
ed areas and suggest future perspectives on Acacia research.
•Methods We compile, summarise and discuss recent find-
ings on physicochemical, ecological, microbiological and so-
cioeconomic aspects of invasion related to Australian acacias
(Acacia dealbata, Acacia longifolia, Acacia mearnsii, Acacia
saligna and Acacia melanoxylon) focusing on Mediterranean
areas.
•Results Acacia invasion generally entails soil physicochem-
ical alterations and changes in microbial function and struc-
ture. Consequences such as the decreased biodiversity, altered
ecosystem structure, larger seed banks dominated by invasive
species, new biotrophic relationships or alterations in water
availability and fire regimes suggest that acacias are locally
creating novel ecosystems.
•Conclusions Forecasting invasions, modelling and manag-
ing ecosystems dominated by acacias are challenging tasks
that should be addressed in the future, since climatic condi-
tions and intensification in land uses are increasing the likeli-
hood of Acacia invasions in Mediterranean areas.
Unsuccessful management actions suggest that restoration
should be meticulously monitored, but the magnitude of inva-
sion or the inconsistency of economic investment indicate that
eradication is often unfeasible. Alternatively, novel integrative
and cost-effective solutions including the collaboration of so-
ciety, politicians and stakeholders are necessary to prevent
new introductions and achieve sustainable control of acacias.
Thereisagrowinginterestinappliedresearchonthe
valorisation or novel uses for acacias and their residues that
result in economic benefits.
Handling Editor: Andreas Bolte
Contribution of the co-authors Pablo Souza-Alonso: conceived the
paper, obtained information, coordinate the review, wrote the first draft
and edited the manuscript.
Paula Lorenzo: obtained information, wrote different sections and
contributed to correct and organise the manuscript.
Jonatan Rodríguez: obtained information and contributed to correct
different sections.
Luís González: contributed to correct and organise the manuscript.
*Pablo Souza-Alonso
souzavigo@gmail.com
Jonatan Rodríguez
jonatan@uvigo.es
Luís González
luis@uvigo.es
Paula Lorenzo
paulalorenzo@uc.pt
1
Plant Biology and Soil Science Department, University of Vigo,
36310 Vigo, Spain
2
Centro de Ecologia Funcional - CEF, Departamento de Ciências da
Vida, Faculdade de Ciências e Tecnologia, Universidade de Coimbra,
3000-456 Coimbra, Portugal
Annals of Forest Science (2017) 74:55
DOI 10.1007/s13595-017-0651-0

Keywords Invasive alien plants .Biodiversity .Ecosystem
changes .Seed production .Soil microorganisms .Acacia
management
1 Introduction
Humans induce rapid changes to the environment, including
the alteration of major biogeochemical cycles, land surface
transformation, changed atmospheric composition and evolu-
tion patterns. Such changes are currently taking place at un-
precedented rates in the period recently defined as the
Anthropocene (Steffen et al. 2007; Lewis and Maslin 2015).
Numerous human activities act as driving forces of environ-
mental change by removing physical, biotic and geographical
barriers that facilitate plant species movement, which is a main
risk factor for biodiversity. Invasive alien plants (IAPs), de-
fined as plant species producing large reproductive progeny
that spread over considerable distances from parent plants
(Richardson et al. 2000a), are currently a priority research
objective of the European Commission (EC Regulation
1143/2014).
Along the wide range of genera containing species classi-
fied as invaders, Acacia is one of the most controversial and
studied genus across the world (Murphy 2008). Currently, 24
Acacia species are confirmed as invasive worldwide
(Richardson and Rejmánek 2011; Lorenzo and Rodríguez-
Echeverría 2015). Acacia sensu lato is a cosmopolitan genus
with polyphyletic origin, but in this paper, we exclusively
focusontheAustralianAcaciasubgenusPhyllodineae -
Acacia s.s.- (Kyalangalilwa et al. 2013) due to their invasive-
ness. The movement of acacias to other continents began in
the late 1700s (Carruthers et al. 2011), but unprecedented
dispersal rates have occurred in the latest two centuries.
Albeit Australian acacias are now occurring worldwide, they
are more frequently invasive in Mediterranean areas (Fig. 1).
Studies on Acacia invasions were compiled in a special issue
covering not only biological and ecological but also social,
economic and ethical perspectives (human-mediated introduc-
tions of Australian acacias—a global experiment in biogeog-
raphy, Diversity and Distributions 2011). At the same time,
Lorenzo et al. (2010a) published a review mainly focused on
hypotheses explaining the invasive success of Acacia
dealbata in Europe. These authors suggest that A. dealbata
not only takes advantage from environmental disturbances,
but also possesses high clonal growth and allelopathic ability
that reduce native biodiversity in the understory. However,
due to the increasing number of studies recently conducted
in Mediterranean areas (see also Fig. 1), we consider that an
update of the current knowledge on the consequences of
Acacia invasion at these regions is required. Here, our objec-
tive is to not only summarise recent findings (including bio-
logical, ecological, physicochemical, microbiological or so-
cioeconomic aspects of invasion) but also to complement
2016-2011 2010-2005 2004-1999 1999-1980
Chile
2016-2011 2010-2005 2004-1999 1999-1980
South America
2016-2011 2010-2005 2004-1999 1999-1980
South Africa
2016-2011 2010-2005 2004-1999 1999-1980
Australia and N.Zealand
2016-2011 2010-2005 2004-1999 1999-1980
Asia
2016-2011 2010-2005 2004-1999 1999-1980
Africa
Regions with Mediterranean-typeclimate
1-3 papers
3-5 papers
5-10 papers
10-20 papers
20-30 papers
> 30 papers
No published papers
2016-2011 2010-2005 2004-1999 1999-1980
Europe
Fig. 1 Scheme representing the number of papers including highly
invasive acacias considered: Acacia dealbata, A. longifolia, A.
mearnsii, A. saligna and A. melanoxylon, through different areas across
the world. Map is created based on information (n= 214 manuscripts)
after the search in SCOPUS by using the key terms Acacia and plant and
invas* (TITLE-ABS-KEY)+ and “Acacia dealbata”or “Acacia
longifolia”or “Acacia saligna”or “Acacia melanoxylon”or “Acacia
mearnsii”. Systematical reviews on the Acacia invasive process were
not included unless they were strictly focused on a specific area. Note
the different scale for the last interval (1999–1980)
55 Page 2 of 20 Annals of Forest Science (2017) 74:55

and extend previous information related to the most problem-
atic acacias in Mediterranean areas. We also discuss future
perspectives on research, management and recovery of invad-
ed areas.
1.1 Major problematic acacia species, introduction
and current distribution
Although there is an important number of invasive species
within Acacia genus, we focused on Acacia dealbata Link,
Acacia longifolia (Andrews) Willd., Acacia mearnsii De
Wild., Acacia saligna (Labill) H. L. Wendl. and Acacia
melanoxylon R. Br. due to their impacts worldwide
(Richardson and Rejmánek, 2011; Lorenzo and Rodríguez-
Echeverría 2015). Acacia cyclops,alsoconsideredasanIAP,
was not included since available data is almost exclusively
based on information from the Cape Region, South Africa
(Higgins et al. 1999,2001).
Specific characteristics of these acacias, such as adaptabil-
ity to many environmental conditions, easy germination and
growth, good survival and rapid growth rates, ornamental val-
ue or wood quality, have determined their current distribution
(Maslin and McDonald, 2004). In Europe and other
Mediterranean areas, some uses of acacias as wood and timber
production (Griffin et al. 2011), the perfume industry (Perriot
et al. 2010;Kulletal.2011), stabilisation of dunes and avoid-
ance of sand erosion (Marchante et al. 2003; Cohen et al.
2008;DelVecchioetal.2013) or to stabilise slopes derived
from the railway construction (Kull et al. 2007), played a
significant role in their introduction. Consequently, a wide
range of Mediterranean biomes are currently threatened by
acacias, such as riparian habitats, shrublands, fynbos,
sclerophyllous forests, mixed forests, grasslands and prairies,
coastal areas and sand dunes, riverlands and watercourses,
islands, agricultural fields or tree plantations (Le Maitre
et al. 2000; Marchante et al. 2003; Rodríguez-Echeverría
et al. 2009; Lorenzo et al. 2010a,b; Crous et al. 2012;
Boudiaf et al. 2013; Hernández et al. 2014; Lazzaro et al.
2014; Celesti-Grapow et al. 2016). In fact, invasive acacias
have been also defined as transformers, those species that
“substantially change the character, condition, form or nature
of ecosystems, becoming active agents in region-forming pro-
cesses”(Richardson et al. 2000a; Marchante et al. 2011a).
1.2 Human perception of invasive acacias
“A fascinating story to be told regarding what transpires when
an environmental scientist’s problem is a rural community’s
livelihood”is how Kull et al. (2011) summarises the contra-
dictory perception of exotic acacias when they represent an
economic resource and, at the same time, an ecological threat
in the introduced ranges. Human perception of invasive aca-
cias is strongly influenced by biophysical, familiarity, social
variables and socioeconomic circumstances (Tassin et al.
2009a;Kulletal.2011,2007). In many countries, large parts
of the population have positive perceptions about invasive
acacias that are largely cultivated with profitable uses such
as construction materials, heat source or medicinal com-
pounds for rural communities (de Neergaard et al. 2005;
Wintola et al. 2017). For example, A. dealbata is highly val-
ued by local communities of Spain, Portugal and France,
where festivals have been celebrated in its honour for almost
50 years (Afonso 2012). In France, some villages such as
Mandelieu-la-Napoule or Biot, both at the Côte d’Azur, have
celebrations of A. dealbata that have continued for more than
80 and 60 years, respectively. On the other hand, when eco-
nomic activities are affected by Acacia invasion, such as for-
estry or citrus cultivation (Kull et al. 2011), these species are
being recognised as problematic.
2 New insights into traits that promote invasion
2.1 Genetics, phenotype and physiology
The size of the genomic pool has been suggested as a factor
promoting invasion (Grotkopp et al. 2004;Kubešová et al.
2010). However, univariate analyses comparing the genome
size of 92 acacias introduced outside their native range—21
invasive, 71 non-invasive—did not detect any difference be-
tween the genome size based on their invasive character
(Gallagher et al. 2011). In addition, low levels of genetic di-
versity in the introduced areas compared to native areas are
not necessarily related to a reduction in the invasion success
and vice versa (Harris et al. 2012).
The amplitude of the native range is generally considered
as an important predictor of invasiveness as it reveals the
adaptation to a wide range of environmental conditions and
leads to a large risk of propagation and dispersal by humans
(Goodwin et al. 1999). Life history traits, such as tree height
and sprouting ability, have an important weight in invasive-
ness predictive models (Gallagher et al. 2011;Gibsonetal.
2011). However, their importance decreases when human fac-
tors are included. In fact, human use is one of the most impor-
tant predictors of Acacia invasiveness (Castro-Díez et al.
2011).
Ecophysiological traits can be as important as morpholog-
ical traits in explaining invasiveness. Once seeds reach the
soil, acacias are provided with mechanisms to outcompete
native species. For example, in saline water-stressed environ-
ments, A. longifolia seeds and seedlings present increased
intracellular ion concentrations, efficient nitrogen uptake, de-
fence against superoxide radicals and high tolerance to a wide
range of salt concentrations compared to native species
(Morais et al. 2012; Morais and Freitas 2012). Godoy et al.
(2011) indicated that the photosystem II (PSII) activity of
Annals of Forest Science (2017) 74:55 Page 3 of 20 55

A. melanoxylon performs better with higher leaf temperature
than that of natives under water stress. This fact could reflect a
higher thermostability of the PSII or, on the contrary, a better
acclimation and thus, efficiency of the entire photosynthetic
process in arid or Mediterranean-type ecosystems. Under ex-
perimental conditions, an increase in CO
2
has been related to
higher growth rates, final weight and increased N-fixation
rates of A. melanoxylon (Schortemeyer et al. 2002).
Consequently, if N supply is also increased, dry biomass,
CO
2
assimilation, foliage thickness and density are signifi-
cantly enhanced (Schortemeyer et al. 1999). In a expected
global warming scenario with higher temperatures and CO
2
levels (IPCC 2013), with acacias growing at higher rates and
producing canopies with denser foliage, reducing light avail-
ability for understory species, the invasiveness of these spe-
cies could be severely increased. However, the benefit from
new climatic conditions is not clear, at least for A. dealbata.
González-Muñoz et al. (2014) predicted a decline of its
growth in the Iberian Peninsula based on climate-growth
patterns and climatic models. Conversely, using species
distribution models, habitat connectivity and protected areas
layers, Vicente et al. (2016)forecastedanincreasinglandex-
position and connectivity between suitable areas for
A. dealbata due to climate change.
2.2 Reproductive features
Reproduction by sprouting facilitates the establishment of
clonal populations (Lorenzo et al. 2010a; Fuentes-Ramírez
et al. 2011; Rodríguez et al. 2017). In fact, the proportion
of sprouting species is higher among invasive than non-
invasive acacias (Gibson et al. 2011). Invasive acacias also
reach reproductive maturity earlier (<2 years) than non-
invaders (Gibson et al. 2011). Acacia dealbata and
A. mearnsii tend to have higher levels of self-compatibility,
suggesting that the ability to self-fertilise may favour its
invasiveness (Gibson et al. 2011). Indeed, A. dealbata has
the capacity to produce progeny by autonomous self-polli-
nation (Rodger and Johnson, 2013). Besides A. dealbata,
also A. longifolia and A. melanoxylon showed low level of
spontaneous self-pollination allowing them to produce vi-
able offspring in Portugal (Correia et al. 2014).
Nevertheless, in the native range of A. dealbata,there
was little evidence of elevated inbreeding influencing its
progeny (Broadhurst et al. 2008). In addition, A. saligna
has a mixed mating system, preferential outcrossing, but
also with a certain level of selfing (George et al. 2008). The
ecological function of self-pollination and its role in inva-
siveness is highly dependent on the trade-off between the
benefits of the absence of compatible mates and costs, such
as the inbreeding depression (characterised by a reduction
in growth and progeny survival). Self-pollination could be
a valuable tool to produce offspring under circumstances
that severely constrain plant survival (e.g. isolated areas,
absence of pollinators, mate limitation). Interestingly,
A. mearnsii showed both sexual and asexual reproduction
depending on the environmental conditions in the non-
native range, showing preference for sprouting in disturbed
areas and seed-based reproduction in undisturbed sites
(Eilu and Obua 2005).
Acacias and pollinators Despite their ability to self-
fertilisation, acacias are pollinated by generalist insects and
they usually require the presence of pollination vectors to
achieve significant seed production (Correia et al. 2014). In
fact, low pollen/ovule ratio supports the compatibility with
dependence on animal pollen vectors (Gibson et al. 2011).
Reproductive success is often maximised by the synchronised
and massive opening of flowers both within a single individ-
ual and local populations (Stone et al. 2003), which may in-
terfere with the normal relationship between native species
and their pollinators. In South Africa, Gibson et al. (2013)
indicated that flower visitation to native plants was reduced
due to the presence of A. saligna. Nevertheless, despite the
massive flowering of A. dealbata and A. longifolia, native
plant species attained similar or even higher visitation rates
in Portugal (Montesinos et al. 2016). Complementary low
temperatures and high relative humidity during winters in
the Northern hemisphere favour polyad viability and pollen
tube development (Beck-Pay 2012).
Seed production, dispersal and germination Seed produc-
tion is suggested as a factor promoting the invasion of acacias
(Castro-Díez et al. 2011). In the introduced range, A. dealbata
and A. longifolia escape pre-dispersal predation and display a
higher production of fully developed seeds per fruit
(A. longifolia) or per tree (A. dealbata), accompanied with
larger size of individual seeds (Correia et al. 2016).
However, rare and widespread acacias have similar levels of
seed production (quantitatively and qualitatively), indicating
that, in some cases, the level of seed development and release
does not necessarily determine plant abundance (Buist 2003).
Nevertheless, massive seed production and accumulation is
highly variable within acacias (Gibson et al. 2011). Once re-
leased, seeds can be dispersed by water or wind, but also
through myrmecochory (seeds with elaiosomes) or
ornithochory (seeds with arils) (French and Major 2001;
Richardson and Kluge 2008; Marchante et al. 2010;
Montesinos et al. 2012), remaining viable for up to 150–200
years (Daws et al. 2007; Leino and Edqvist 2010).
Fire stimulates seed germination of several invasive acacias
such as A. melanoxylon,A. dealbata and A. saligna (García
et al. 2007; Lorenzo et al. 2010a;Wilsonetal.2011).
Additionally, butenolide, a chemical compound isolated from
smoke, may have a significant positive effect on the post-fire
seedling ecology of A. mearnsii (Kulkarni et al. 2007). The
55 Page 4 of 20 Annals of Forest Science (2017) 74:55

stimulating effect of fire has important ecological implications
since fire may eliminate native seeds from the surface layer,
favouring the germination of resistant acacia seeds and thus,
the success of the invasion (Richardson and Kluge 2008;Le
Maitre et al. 2011; Hernández et al. 2014). This is particularly
relevant for Mediterranean ecosystems that are characterised
by frequent fires, which might contribute to explain the suc-
cess of acacias such as A. saligna (Wilson et al. 2011)or
A. melanoxylon (García et al. 2007). Moreover, under a cli-
mate change scenario, extreme and more frequent wildfires
are expected in these ecosystems (IPCC 2013), which could
effectively expand the distribution area of invasive acacias.
2.3 Symbiotic associations
As legumes, acacias are highly reliant on symbiotic associa-
tions with compatible microbes. In a new habitat, access to
compatible rhizobia is a critical factor conditioning the inva-
sive ability of legumes since mutualisms play a key role dur-
ing their establishment (Parker 2001). Symbiotic promiscui-
ty—low specificity for building up associations with compat-
ible rhizobia—has been considered a characteristic trait of
invasive legumes (Richardson et al. 2000b;Parker2001).
Invasive acacias can associate with a wide range of N-fixing
bacteria (Lorenzo and Rodríguez-Echeverría, 2015). The in-
vasive ability of acacias might be primarily determined by the
capacity to form nodules profusely and more efficiently than
native N-fixing legumes (Rodríguez-Echeverría et al. 2009,
2010). Acacias usually establish symbiotic relationships with
the genus Bradyrhizobium, more specifically with
Bradyrhizobium japonicum (Lafay and Burdon 2001;
Rodríguez-Echeverría et al. 2007), in both native and non-
native ranges (Birnbaum et al. 2012; Boudiaf et al. 2014).
However, symbiotic interactions with new mutualists have
also been reported in non-native ranges for Australian acacias
(mainly Bradyrhizobium and Rhizobium,butalso
Mesorhizobium,Ochrobactrum and Ensifer meliloti)
(Rodríguez-Echeverría et al. 2011; Birnbaum et al. 2012).
For example, A. saligna may effectively associate with differ-
ent rhizobial communities in non-native and native ranges
(Birnbaum et al. 2012).
Nevertheless, A. longifolia,A. dealbata and
A. melanoxylon preferentially associate with co-introduced
symbionts in non-native ranges (Rodríguez-Echeverría et al.
2011;Lorenzo and Rodríguez-Echeverría, 2015), discarding
symbiotic promiscuity as an invasive trait. In fact, Le Roux
et al. (2016) have recently indicated that native and invasive
legumes (Acacia within them) interact with distinct rhizobial
lineages in South Africa. They found that instead of the classic
vision of disrupting invasions, acacias and their symbionts
form novel modules which are largely unconnected to highly
modular native legume–rhizobium networks. Genetic analysis
of symbiotic bacteria from root nodules of A. saligna from
Portugal indicated that obtained sequences mainly clustered
with Australian sequences, suggesting the co-introduction of
symbiotic partners (Crisostomo et al. 2013). Consequently,
the rapid expansion and great nodulation ability of
A. longifolia could enlarge the population and spread of the
associated exotic Bradyrhizobium through the establishment
of positive feedbacks (Rodríguez-Echeverría et al. 2009). The
establishment of positive soil feedbacks has been also sug-
gested when A. dealbata grows in previously invaded soils
(Lorenzo and Rodríguez-Echeverría 2012;Rodríguez-
Echeverría et al. 2013). This fact illustrates the ecological risk
of the voluntary and involuntary introduction of exotic mutu-
alistic microorganisms in reforestation projects. Invasion by
acacia species may be favouring a second invasion by their
associated exotic soil microbes. As a consequence, such syn-
ergistic interaction could accelerate impacts on ecosystems in
the introduced ranges (Invasional meltdown hypothesis,
Simberloff and Von Holle, 1999).
2.4 A clear role of allelopathy?
The release of allelochemicals by invasive plants has been
postulated as a factor influencing the surrounding environ-
ment and favouring invasion (Inderjit et al. 2011).
Allelopathy occurs because some IAPs bring novel chemicals
that affect native species (Callaway and Aschehoug 2000).
The allelopathic phenomenon has been broadly studied in
A. dealbata. In the invaded ranges, extracts of A. dealbata
containing natural or close to natural concentrations affected
germination, seedling growth, net photosynthetic rate, respi-
ration rate and biomass of agricultural and native understory
plants (Carballeira and Reigosa 1999; Lorenzo et al. 2010b,
2011,2012; Aguilera et al. 2015a) and functional diversity of
soil microbes (Lorenzo et al. 2013a). Studying the release of
allelochemicals along the different phenological stages of
A. dealbata, Lorenzo et al. (2010c) found that allelopathic
interactions were higher during the flowering period and
depended on target species. A recent study showed that alle-
lopathic effects mainly take place at root level, causing anom-
alous growth and morphology and leading to seedling mortal-
ity (Aguilera et al. 2015b). Interestingly, in vitro experiments
with natural leachates obtained from adult A. dealbata plants
increase the radicle length of its own seedlings, suggesting
self-stimulation (Lorenzo et al. 2010c). However, the stimula-
tory effect disappeared when A. dealbata seedlings were
grown on native soils (Lorenzo and Rodríguez-Echeverría
2012). In, volatile organic compounds (VOCs) released by
A. dealbata flowers reduced germination and growth of its
own seedlings (Souza-Alonso et al. 2014a). Despite the evi-
dence of allelopathy under controlled conditions, the allelo-
pathic effect was not detected at field scale, suggesting a neg-
ligible role of allelopathy during the invasive process of
Annals of Forest Science (2017) 74:55 Page 5 of 20 55

A. dealbata, at least in the European range (Lorenzo et al.
2016a; Souza-Alonso et al. under review).
Much less information is available on the allelopathic poten-
tial of other acacias. Litter at different stages of decomposition
and soils of A. melanoxylon have shown negative effects on the
germination and growth of native plant species (González et al.
1995;Soutoetal.2001). Stem and bark aqueous extracts of
A. melanoxylon reduced the growth of the aquatic plant Lemna
aequinoctialis (Allan and Adkins 2007), whereas extracts from
phyllodes and flowers of this species inhibited biometrical and
physiological parameters of native and model species (Hussain
et al. 2011a,b). Residues of A. mearnsii also showed a moderate
allelopathic effect on the growth of dicotyledons and grasses
(Schumann et al. 1995). Finally, Ens et al. (2009a,b) suggested
that allelopathy plays an important role in ecological interactions
of A. longifolia in their native range. However, these studies only
constitute evidence of potential allelopathy since bioassays were
conducted under controlled conditions. In fact, the effect of alle-
lopathic compounds depends on bioassay conditions as the
solvent, soil matrix or pH used and the presence/absence of soil
microbes (Inderjit and van der Putten 2010; Lorenzo et al.
2016b). Therefore, experiments mimicking natural conditions
are necessary to clearly identify the role of allelopathy in the
invasive process. Otherwise, the allelopathic picture of the
above-mentioned acacias will remain unclear and incomplete.
3 Effects on ecosystems
Invasive acacias affect both above- and belowground com-
partments as well as ecosystem services such as soil forma-
tion, water flow, nutrient cycling, wood or fibre production
and recreation or educational opportunities that sustain human
well-being (Le Maitre et al. 2011). The main characteristics of
Acacia invasions are represented in Fig. 2. Nevertheless, the
invasion of acacias presents geographical differences across
Mediterranean regions.
Fig. 2 Schematic representation of the main processes that take place under Acacia invasion and links to the main sections and references included in the
manuscript
55 Page 6 of 20 Annals of Forest Science (2017) 74:55

3.1 Aboveground effects
3.1.1 Structural changes
Invasive acacias create homogeneous and dense-vegetation
formations (Le Maitre et al. 2011), which drastically decrease
light availability for understory plants hindering their estab-
lishment (Lorenzo et al. 2010a; Rascher et al. 2011a;Lorenzo
et al. 2016a). In fact, Fuentes-Ramírez et al. (2011)founda
lower survival of light-demanding native forest species vs.
shade-tolerant species under A. dealbata. The reduced light
availability also leads to lower grass productivity through the
reduction of specific leaf area index (LAI) thresholds (Gwate
et al. 2016). However, A. dealbata did not reduce the light
availability in broad-leaf native forests (González-Muñoz
et al. 2012). This fact reveals that the influence of A. dealbata
on light conditions is severe in native open canopies, but with
slight effect in closed-canopy ecosystems.
Changes in the dominant tree species entail subsidiary con-
sequences. Dense Acacia canopies lead to the accumulation of
high quantity of biomass and litter, which increases the occur-
rence and intensity of fires in invaded ranges. Fires, in turn,
stimulate the germination of acacia seeds and reduce the via-
bility of native seeds favouring the invasive process
(Richardson and Kluge 2008; Le Maitre et al. 2011).
However, this fact has more ecological relevance in ecosys-
tems without dominant species reliant on fire to germinate. In
some Mediterranean areas, such as in central Chile, model
projections predict the dispersion of A. dealbata only in the
presence of fire when combined with browsing and/or cutting
(Newton et al. 2011).
3.1.2 Plant biodiversity
In general, Acacia invasions significantly reduce plant cover,
species richness and diversity (Holmes and Cowling 1997;
Marchante et al. 2003; Tassin et al. 2009b; Fuentes-Ramírez
et al. 2011; Lorenzo et al. 2012; Lazzaro et al. 2014).
Biodiversity reduction due to A. dealbata invasion results in
the replacement of native species by other natives or exotic
plants (Fuentes-Ramírez et al., 2011; Lorenzo et al. 2012;
Marchante et al. 2011b;González-Muñozetal.2012). In com-
parison with other invasive species, plantations of A. saligna
have demonstrated a higher capacity to affect plant diversity
(Manor et al. 2008). Surprisingly, A. saligna selectively in-
creased the presence of ruderal grass species without reducing
total richness (Del Vecchio et al. 2013). The identification of
changes in plant species composition along invaded areas pro-
vides highly valuable information. Nonetheless, to our knowl-
edge, whether modified native communities are accompanied
by alterations in functional and phylogenetic diversity of
invaded plant communities remains unknown.
3.1.3 Macrofauna
The presence of invasive acacias also modifies habitat suit-
ability for animals and establishes novel ecological networks.
Van der Colff et al. (2015) found a different trend of arthropod
community composition between native and invaded areas by
A. mearnsii; arthropods could be using exotic trees as a path-
way to reach isolated habitats. In this sense, leaf N content is
an important driver of arthropod population dynamics in
A. mearnsii stands (Maoela et al. 2016a). Nevertheless, arthro-
pod assemblages in the native community can be progressive-
ly recovered after the removal of the exotic (Maoela et al.
2016b). On the other hand, Eichhorn et al. (2011)indicated
that the artificial damage induced to the leaves of A. dealbata
activated the production of extra-floral nectaries. After dam-
age, leaves were only visited by the invasive Argentine ant
Linepithema humile, which could imply an interspecific pos-
itive feedback between invasive species. Moreover, larger an-
imals are also affected by acacia invasions. The tree density of
A. saligna stands, together with other factors such as urban
density or vegetation structure, contributed to the decline of
birds diversity (Dures and Cummings 2010) and species of
small mammals (Manor et al. 2008), linking the decrease in
biodiversity with a reduction in habitat quality or ecosystem
integrity. Additionally, seeds of A. mearnsii are used as a nu-
trient source by the specialist primate Cercopithecus
albogularis labiatus, altering its feeding behaviour and prob-
ably leading to consequences for A. mearnsii dispersion
(Wimberger et al. 2017).
3.2 Belowground effects
3.2.1 Physicochemical changes and nutrient cycling
The rapid observation of the understory below the canopy of
acacias indicates substantial changes in the structure of soil
surface, linking Acacia invasion with the concept of niche
construction (Day et al. 2003). The overwhelming surface
root development of Acacia trees dominates and drastically
transforms soil surface. Acacia dealbata creates a root net in
the upper soil layer due to its extensive creeping rhizomatous
system (Fuentes-Ramírez et al. 2011), reducing soil bulk den-
sity (May and Attiwill 2003). Similarly, A. saligna develops
roots reaching 6 m during the first 4 years (Knight et al. 2002).
Below the canopy, a thick layer of organic matter is progres-
sively accumulated by the continuous litter fall (Marchante
et al. 2004; Castro-Díez et al. 2012). Acacias provide litter
with different C-sources composition that can affect nutrient
cycling and decomposition, with possible ecological ramifica-
tions (Ens et al. 2009a). Nevertheless, decomposed plant ma-
terial of A. dealbata did not produce significant changes in the
functional and structural profile of soil microbial communities
and soil chemical properties compared to the decomposition
Annals of Forest Science (2017) 74:55 Page 7 of 20 55

of similar quantities of native plant material (Guisande et al. in
preparation).
As N
2
fixers, acacias increase N (Marchante et al. 2008a;
Lorenzo et al. 2010b; Souza-Alonso et al. 2014b)orNH
4
+
pools (Castro-Díez et al. 2012). Acacia saligna modifies N
cycling through the production of higher amounts of litter,
resulting in more N being returned to the soil and an increase
in the availability of inorganic N (Yelenik et al. 2004). Acacia
longifolia provides large quantities of N to the surrounding
vegetation; however, at the same time, requires substantial
amounts of P itself which creates a N/P imbalance at the com-
munity level (Ulm et al. 2016). Moreover, acacias substantial-
ly and progressively change C content in long-time invaded
soils (Yelenik et al. 2004; Marchante et al. 2008a; Souza-
Alonso et al. 2015). Other parameters, such as the content of
organic matter or interchangeable P, were significantly in-
creased by A. dealbata in soils from different ecosystems
(Lorenzo et al. 2010b; Souza-Alonso et al. 2014b).
However, Castro-Díez et al. (2012) found no differences in
pH or organic matter after A. dealbata invasion. Souza-
Alonso et al. (2014b) suggested that the variation in pH might
be highly dependent on the studied ecosystem. Acacia
longifolia drastically increased the content of C and N, C/N
ratio, pH and litter in ecosystems with poor soils, such as sand
dunes and coastal areas (Marchante et al. 2008a,c;Rascher
et al. 2011a), resulting in differences in the catabolic diversity
of microbial communities (Marchante et al. 2008c).
Interestingly, these soil changes lead to a positive feedback
between acacias and invaded soils. Soils previously invaded
by A. dealbata favour the growth of its own seedlings and
increase the mortality of the co-occurring native Pinus
pinaster Aiton (Lorenzo and Rodríguez-Echeverría 2012;
Rodríguez-Echeverría et al. 2013). This legacy effect—persis-
tent changes in the long term—may continue even after acacia
removal (Marchante et al. 2008b,2011a).
3.2.2 Seed bank
The composition of the soil seed bank after acacia inva-
sion is significantly modified by limiting or interrupting
native propagule supply. Richness of native seeds was
drastically decreased after the increase in A. longifolia
density, while seeds of the invader were progressively
accumulated (Fourie, 2008,RichardsonandKluge2008;
Le Maitre et al. 2011). Similarly,the diversity of the seed
bank in understories invaded by A. saligna and
A. dealbata was severely affected (Holmes and Cowling
1997; González-Muñoz et al. 2012), resulting in a dimi-
nution and homogenisation in the size of the native seed
bank and higher percentages of exotic seeds in invaded
ecosystems (Marchante et al. 2011b; González-Muñoz
et al. 2012).
3.2.3 Water relationships
Water availability is often indicated as one of the main limiting
factors of plant growth in Mediterranean areas (Claeys and
Inzé 2013; Flexas et al. 2014). Across their range of introduc-
tion, invasive acacias are considered as water-consuming spe-
cies, and their presence leads to a reduction in the quantity and
quality of available water in soil and an increase in the evapo-
transpiration rate (Lorenzo and Rodríguez-Echeverría 2015).
In the non-native range, water consumption by
A. melanoxylon was higher than that measured for highly
competitive species such as Eucalyptus globulus or
P. pinaster (Jiménez et al. 2010). In South Africa, besides
the use of groundwater, A. dealbata and A. mearnsii collected
an important part of the estimated reduction of the mean an-
nual runoff produced by all invasive plants (Le Maitre et al.
2000). This is particularly relevant in areas that present very
low surface runoff, as in coastal arid regions. Novel
A. mearnsii populations presented higher water losses com-
pared to natives (Dye et al. 2001), whereas A. longifolia re-
duced the water flow on average by 26% in pine forests of
coastal dunes in Portugal (Rascher et al. 2011b). At the same
time, changes in hydrologic dynamics produced by
A. longifolia were also associated with decreased C fixation
rates of native trees (Rascher et al. 2011b). Interestingly, the
high water consumption is generally considered a strategy for
individual fast growth. Nevertheless, due to the ability of aca-
cias to sprout, water consumption could be alternatively seen
as a community-level strategy promoting the collective rather
than individual plants in the long term (Werner et al. 2010).
Acacias can also influence the water availability for sur-
rounding plant communities through other strategies at root
level. High molecular weight alkanes exuded from roots by
A. longifolia can induce water repellence, thereby reducing the
accessible water for native seedlings (Ens et al. 2009b).
However, under stressful conditions of limited water supply,
A. longifolia revealed high drought sensitivity in terms of
biomass and N-uptake efficiency, which was even more
marked when plants grew with intra- or interspecific compe-
tition (Werner et al. 2010). Considering the evolutionary link
that relates drought-tolerant xylem structure with the capacity
to resist lower water potentials (Bhaskar and Ackerlyt1 2006),
A. mearnsii showed lower water potential at 50% hydraulic
conductivity loss (P
50
)comparedtonativespecies,suggesting
drought-tolerance (Crous et al. 2012). Field xylem water po-
tentials also support that A. mearnsii has a significant advan-
tage over some native species under drier conditions (Crous
et al. 2012).
The removal of acacias might facilitate the replenishment
of water for native vegetation, becoming a key factor to be
considered in management operations, particularly in
Mediterranean areas. In fact, removal of A. mearnsii and
A. longifolia from riparian habitats increased the streamflow
55 Page 8 of 20 Annals of Forest Science (2017) 74:55

(Prinsloo and Scott, 1999). Marais and Wannenburgh (2008)
suggested that the removal of invasive acacias does not im-
mediately imply water availability, but they consider it as an
important part of a package of several actions to optimise
water supply. Jovanovic et al. (2009) indicated that clearing
lands invaded by A. saligna, besides the increase in water
availability due to the reduction in evapotranspiration, may
also reduce the contamination of groundwater by nitrate.
Notwithstanding, to be realistic, changes in water regimes
attributed to Acacia invasions or plantations should also in-
clude climatic conditions (rainfall patterns) as a potential
source of variability (Rangan et al. 2010).
3.2.4 Soil microorganisms
Recent studies found substantial changes in soil microbial
communities at structural and functional level produced by
Acacia invasion (Marchante et al. 2008a,c; Lorenzo et al.
2010b,2013a; Boudiaf et al. 2013; Souza-Alonso et al.
2014b,2015). These changes are more pronounced in the long
term or in heavily invaded areas and depend on the invaded
ecosystem (Marchante et al. 2008a; Lorenzo and Rodríguez-
Echeverría 2015). In addition, bacteria seemed to be more
affected than fungi (Marchante et al. 2008a; Lorenzo and
Rodríguez-Echeverría 2015).
Bacteria Acacia invasion affects both the structure and func-
tional diversity of soil bacterial communities (Lorenzo and
Rodríguez-Echeverría 2015). Particularly, A. longifolia and
A. dealbata alter the structure of bacterial communities from
dunes, grasslands and mixed forests (Marchante et al. 2008a,
c; Lorenzo et al. 2010b), relating the duration of the invasion
with the magnitude of the effect produced (Marchante et al.
2008a; Souza-Alonso et al. 2015). On the other hand, the
functional catabolic diversity of soil bacteria also varies after
the invasion by A. longifolia,A. dealbata and A. mearnsii
(Marchante et al. 2008c; Boudiaf et al. 2013; Lorenzo et al.
2013a).
Fungi Theeffectofinvasiononsoilfungalcommunitieswas
mainly studied in soils invaded by A. dealbata, which mod-
ifies the community structure of generalist fungi in pine for-
ests and shrublands, but the effect depend on the studied eco-
system (Lorenzo et al. 2010b; Souza-Alonso et al. 2014b).
Nevertheless, fungal communities seemed to evolve tolerance
to invasion since they tended to return to the structure of pre-
invaded community after long periods (>25 years) of invasion
(Souza-Alonso et al. 2015). Acacia invasion also modified
specific fungal groups such as arbuscular mycorrhizal fungi
(AMF) and ectomycorrhizal fungi (EM). Structural changes in
AMF communities caused by A. dealbata were accompanied
by a reduced growth of the highly AMF-reliant plant Plantago
lanceolata (Guisande-Collazo et al. 2016). However,
chemical compounds naturally released by A. dealbata did
not affect the potential infectivity of AMF in different native
soils (Lorenzo et al. 2013b). Similarly, A. mearnsii significant-
ly altered the structure and composition of EM which, in con-
sequence, produced a decrease in the early growth of the na-
tive tree Quercus suber L. (Boudiaf et al. 2013).
3.2.5 Mesofauna
The relationships between native plants and the community of
decomposers can be also altered due to the presence of
acacias. However, despite its fundamental role, studies
addressing impacts of acacias on groups implicated in the
breakdown of organic matter are scarce. Coetzee et al.
(2007) found a significant reduction in richness, abundance
and body size of arthropods (Coleoptera) in grasslands invad-
ed by A. dealbata compared to non-invaded areas.
Additionally, the presence and litter production of
A. mearnsii in riparian habits altered the structure of inverte-
brate communities, reducing the abundance of some cobble-
dwelling taxabut increasing particle-feeding mayflies and chi-
ronomids (Lowe et al. 2008). Below A. melanoxylon and
A. mearnsii canopies, invertebrate richness was reduced com-
pared to that under native species, and this reduction was
higher at species level than at family or order level
(Samways et al. 1996), indicating that changes in the domi-
nant species has probably lower implications at functional
level. Furthermore, qualitative changes in litter composition
produced by A. dealbata and A. longifolia invasion result in
poor nutrient material for terrestrial isopods—key compo-
nents of macro-decomposer communities—leading to smaller
individuals (Sousa et al. 1998).
4 Control and management
4.1 Recent advances in traditional control
Research on Acacia management started in South Africa, a
pioneer country implementing management policies at nation-
al level. First organised efforts to control A. dealbata,
A. longifolia or A. mearnsii were carried out mainly through
the implementation of the Working for Water program (van
Wilgen et al. 2011 and references therein). In general, the
management of acacias is an expensive investment and long-
time task due to the sprouting ability and their large and resil-
ient seed banks (Richardson and Kluge 2008;Gaertneretal.
2012; van Wilgen et al. 2016).
Potential effective results have been achieved using
triclopyr herbicide combined with cutting of A. dealbata indi-
viduals in a short-term strategy (Campbell and Kluge 1999;
Souza-Alonso et al. 2013). Triclopyr was also effective to
control A. mearnsii seedlings, even at low doses (Viljoen
Annals of Forest Science (2017) 74:55 Page 9 of 20 55

and Stoltsz 2008). Herbicide combined with cutting was use-
ful to reduce A. saligna in post-burning control. However,
cutting A. saligna saplings below the coppicing point pro-
duced the best results (Krupek et al. 2016). In other cases,
the knowledge of the best phenological stage to manage aca-
cias improves the effectiveness of management actions. For
instance, basal cuttings of young A. mearnsii individuals
(≤7 years) should be preferably done in non-growing periods
to diminish sprouting (Perrando and Corder 2006). On the
other hand, similar management actions may yield different
results at different locations due to the specific site conditions
and life history traits. In South Africa, the felling and remov-
ing of A. mearnsii produced both positive and negative results,
which could be related to local specific conditions (Blanchard
and Holmes 2008). Nevertheless, results obtained during the
last decades showed that the successful recovering of invaded
areas by using traditional control methods is difficult to
achieve due to the extension of invasion invaded areas (van
Wilgen et al. 2012).
4.2 Biological control
The biological control of acacias started with the introduction
of the bud-galling wasp, Trichilogaster acaciaelongifoliae,to
control A. longifolia in South Africa (Dennill and Donnelly
1991). After several generations, the production of
A. longifolia pods has been highly reduced. However, the
effectiveness of the bud-galling agent was higher in areas with
similar atmospheric conditions to native regions of the intro-
duced wasp. In addition, a recent study found that populations
of A. longifolia showing high genetic variability may differ-
entially respond to the control agent in introduced ranges
(Thompson et al. 2015), hampering the success of the biolog-
ical control and compromising the reproducibility of this
method. Similarly, the beetle Melanterius ventralis was intro-
duced to feed on seeds of A. longifolia, producing seed mor-
tality in a range from 15 to 79.5% (Donnelly and Hoffmann
2004). In Portugal, T. acaciaelongifoliae was recently intro-
duced and tested on A. longifolia under controlled conditions
with positive results (Marchante et al. 2011c). Subsequently,
the European Commission (EC), after approval by the EFSA
Panel on Plant Health (EFSA 2015; Jeger et al. 2016),
authorised field tests that were conducted in late 2015 (Shaw
et al. 2016). First reports indicated that T. acaciaelongifoliae
successfully completed its life cycle in Portugal although the
number of detected galls is currently low (Marchante et al.
2017). The flower-galling midge Dasineura rubiformis was
also effectively introduced to control A. mearnsii, exclusively
affecting its reproductive capacity (Impson et al. 2008,2013).
During the period of 1991–2005, the introduced rust-fungus
Uromycladium tepperianum significantly affected A. saligna
by reducing tree density (between 87 and 98%) and canopy
mass, also increasing tree mortality (Wood and Morris 2007).
However, undesirable side effects of biological control
may occur (Seymour and Veldtman 2010; Veldtman et al.
2011). In South Africa, the liberation of some control agents
such as T. acaciaelongifoliae,Dasineura dielsi and
M. ventralis unintentionally damaged the non-target
A. melanoxylon,A. longifolia and A. melanoxylon,respective-
ly (Dennill et al. 1993;Postetal.2010; Donnelly and
Hoffmann, 2004). This could be related to the low specificity
of biocontrol agents that can lead to affinities for related spe-
cies (Donnelly and Hoffmann, 2004). In fact, congeneric plats
closely related to the target species are more susceptible to be
also attacked than distantly related ones (Pemberton, 2000). In
these cases, the side effect can be considered “positive”since
other invasive congeners (all leading to acacia control) were
targeted. Therefore, the use of biological control agents in
Europe or North America to control acacias should have pre-
sumable low ecological risks due to the absence of native
acacias. On the other hand, ecological effects of introduced
agents are not completely addressed and unexpected conse-
quences as ecological replacement, compensatory responses
or food-web interactions may occur (Pearson and Callaway
2003). In fact, agents introduced to control A. longifolia and
A. saligna in South Africa created complex food webs in the
introduced range, similar to those in their native ranges
(Veldtman et al. 2011). Main ecological pressures or inconsis-
tencies derived from the introduction of novel agents were
identified by Louda et al. (2003) as the susceptibility of related
species, host specificity determined by physiological range,
increase in the extinction risk of vulnerable species, or the
infiltration in natural areas away from targeted
agroecosystems.
4.3 Effective recovery of cleaned areas
Theory predicts that management programs are more effective
if invaders are rapidly recognised and the time between the
introduction and management is as short as possible
(Simberloff et al. 2013; Luque et al. 2014; Kimball et al.
2015). The intensity of the required intervention for ecosys-
tem recovery is proportional to the duration (i.e. density) of
invasion (Holmes et al. 2000). Furthermore, the early detec-
tion of invasive plants also contributes to a cost-effective man-
agement. Economic costs of clearing dense invaded areas are
3–20 times higher than those necessary to manage scattered
invaded areas (Marais and Wannenburgh 2008). In this sense,
the current regulation of the European Commission on inva-
sive species foresees three types of interventions: prevention,
early detection and rapid eradication and management (EC
2014). However, the success of land restoration after acacia
removal is uncertain because of the severe changes in soil
physicochemical properties (Marchante et al. 2004,2011a,
b). The transformation of ecosystems invaded by acacias sug-
gests that a return to pre-existing conditions is virtually
55 Page 10 of 20 Annals of Forest Science (2017) 74:55

impossible. Therefore, the concept of restoration should be
understood as a synonym of recovery.
After the removal of invasive acacias, the ecosystem recov-
ery takes several years before soil nutrients and processes
return to similar pre-invasion levels. In fact, the autonomous
recovery potential of native vegetation after clearing of dense
Acacia stands is certainly limited (Mostert et al. 2017). For
example, the recuperation of native plant communities in
coastal sand dunes is difficulted by the time elapsed from
the introduction of A. longifolia. Thus, eradication efforts
should be maintained in the long term to achieve positive
results (Marchante et al. 2008b). To develop efficient recovery
programs, secondary effects after the removal on invaders
must be also considered. In this line, the enhanced content
of N in invaded soils favours the settlement of grasses, forbs
and other shrubs, but hinders ericoid or proteoid species
(Gaertner et al. 2012). Additionally, the growth rates of the
nitrophilous species Ehrharta calycina increased in stands
where A. saligna was removed, suggesting that subsequent
invasions by weeds may occur after clearing N
2
-fixing alien
species (Yelenik et al. 2004). Consequently, ecosystem recov-
ery can be facilitated by the simultaneous removal of the N-
rich litter layer, facilitating the germination of native species in
the short term (Marchante et al. 2004,2008b). Nevertheless, a
field study assessing long-term consequences of Acacia re-
moval found that the recovery of native vegetation in 15-
year-old cleared sites was accompanied by a gradual improve-
ment in soil nutrient levels (Ndou and Ruwanza 2016).
Removal without an adequate planning of management can
lead to the exposure of infertile subsoil vulnerable to erosion,
even more in areas with slow rates of plant colonisation such
as hill slopes (Van Der Waal et al. 2012). This fact also re-
stricts the colonisation by indigenous species that could aid in
the soil stabilisation (de Neergaard et al. 2005).
The maintenance of the native seed bank is fundamental to
successfully recover ecosystems after Acacia invasion.
Unsuccessful recovering of invaded ecosystems after acacia
removal is frequently related to the lack of native seeds or
propagule supply (Galatowitsch and Richardson 2005). If
the native seed bank is severely depleted after plant invasion,
autogenic recovery can be inhibited (Le Maitre et al. 2011). In
fact, when the seed bank is exhausted or reaches critical
values, the inclusion of native seeds in restoration programs
could be essential to achieve pre-existing conditions. For ex-
ample, the re-introduction of riparian species is required in
highly transformed river basins to promote recovery and pre-
vent re-invasion (Holmes et al. 2005). In addition, native spe-
cies with low nutrient requirements and strong competitive
ability that can outcompete invasive acacias at the early seed-
ling stage are particularly valuable (Werner et al. 2010), which
may facilitate ecosystem recovery.
At the same time, massive seed banks of acacias are diffi-
cult to manage after the removal of acacias (Richardson and
Kluge 2008). In some cases, fire was used to manage the
acacia seed bank in dense invaded stands (Krupek et al.
2016). The application of fire after tree removal reduces the
content of N in soil, causes a mass germination of Acacia
seeds and occasionally stimulates the indigenous seed bank,
as in fire-prone ecosystems (Le Maitre et al. 2011).
Nevertheless, fire has negative consequences, and prescribed
burns are only recommended under specific circumstances, as
steep slopes or inaccessible areas (Fill et al. 2017). In general,
fire should be used judiciously, combined with other methods
or discarded in situations where conservation of indigenous
biological diversity is of central consideration (Richardson
and Kluge 2008). Soil surface temperature can be modified
without the use of fire. In the case of small invaded areas, the
dormancy of Acacia seeds might be artificially removed
through soil solarisation. For example, Cohen et al. (2008)
achieved a complete exhaustion of buried seeds of
A. saligna using polyethylene mulches to impede the photo-
synthetic process and produce hydrothermal stress.
However, active restoration actions are rarely implemented
after clearing invaded areas, unless the cost/benefit ratios are
deemed acceptable (Fill et al. 2017). Active restoration can be
effective and even financially feasible when compared to pas-
sive restoration. The density of exotic tress generally deter-
mines whether the economic balance of restoration is positive
or negative (Gaertner et al. 2012). There is increasing evi-
dence that, in some cases, the restoration of invaded areas is
feasible and can provide multiple social and economic bene-
fits (Murcia et al. 2014).
4.4 Towards an integral management
Experience obtained in the management of acacias has shown
that successful projects require clear and time-based goals,
adequate resources and actual and in-kind support from the
stakeholders (Forsyth et al. 2012). An improved management
strategy based on recently developed frameworks (Kumschick
et al. 2012,2015; Blackburn et al. 2014; Hawkins et al. 2015)
should focus on priority areas and species, assuming trade-
offs between preserving biodiversity and avoiding the expan-
sion of the invasion; otherwise, money allocated to control
actions will be wasted (van Wilgen et al. 2016).
However, until now, management actions conducted in pri-
ority areas showed little progress in reducing total infestation
(van Wilgen et al. 2012; Gwate et al. 2016). Even in South
Africa where public funds were periodically invested and main-
tained to control invasive acacias, the economic resources were
clearly insufficient to eradicate the invasive acacias (van
Wilgen et al. 2012). Combining management techniques such
as the integrated use of fire and active re-seeding of cleared
areas with indigenous shrubs would substantially increase the
effectiveness of ecosystem restoration (Fill et al. 2017).
Profitable land uses, selective thinning of invasive
Annals of Forest Science (2017) 74:55 Page 11 of 20 55

aboveground biomass or grazing could enhance multi-benefits
in invaded landscapes (Seastedt et al. 2008; Gwate et al. 2016).
Spatiotemporal modelling approaches, such as individual-
based models (IBMs), stochastic dynamic methodology
(StDM), or species distribution models (SDMs) are being de-
veloped to anticipate Acacia invasions and manage their im-
pacts in Mediterranean areas (Thompson et al. 2011; Santos
et al. 2015). However, SDMs combined with phylogeographic
approaches were not totally effective in predicting the occur-
rence of the two subspecies of A. dealbata (A. dealbata ssp.
dealbata and spp. subalpina) in South Africa (Hirsch et al.,
2017). Recently, hierarchical framework that combines
SDMs, scenario analysis and cost analyses to improve the
assessment of Acacia invasions at regional and local scales
has also been developed (Vicente et al. 2016). In addition to
previous approaches, impacts of acacias in a specific area can
be initially assessed by using the generic impact scoring sys-
tem (GISS), a novel and feasible tool to easily quantify eco-
system impacts (Nentwig et al. 2016).
In our opinion, the current vision of Acacia management
by scientists is mainly focused on the ecological perspective,
avoiding socioeconomic implications. Generally, manage-
ment actions are carried out with public sources, resulting in
an unavoidable necessity of social and scientific alliances.
Public perception of IAPs is a key part in the assessment of
management strategies, therefore providing a favourable so-
cial and political environment which is essential to achieve
successful results. The engagement of public perception in
management actions is more efficient and accepted by both
parts (Panetta and Timmins 2004). In this sense, the use of
inquiries is currently gaining interest as an informative and
feedback tool in decision-making processes (Verbrugge et al.
2014; Liu and Cook 2016). Otherwise, eradication efforts are
useless when administration and social actions do not pursue
similar interests, suggesting that local communities need to be
actively involved in the control of IAP and management pro-
grams (Mukwada and Manatsa 2017).
After several years of observation, we are also certain that
socioeconomic aspects such as the forced human migration
from rural to urban areas leads to land neglect and misuse
and this movement is favouring the invasion by Acacia—and
also other IAPs. Facilitating the settlement of population in
rural areas would help to quickly identify and avoid the dis-
persal of acacia propagules, preserving rural native vegetation.
In fact, increase access to land use for farming purposes could
result in a greater concern, care and, ultimately, a better man-
agement of acacias (de Neergaard et al., 2005). Unfortunately,
unworked or unprotected lands do not represent a significant
value for the society. To us, government policies exclusively
focused on the control of IAPs, but avoiding the problem of
land misuse, cannot be totally effective.
Moreover, in many areas worldwide, the governmental ac-
tions to control acacias rely on workers that are seasonally
recruited and do not necessarily return the following season
(Fill et al. 2017). In other cases, as in the Working for Water
program, the objective of maximising employment (reducing
cost/person day) limits the effective monitoring and evalua-
tion of outcomes due to poorly trained workforce (van Wilgen
and Wannenburgh 2016). Alternatively, operational models
that extend monitoring units throughout the year would lead
to a better IAP management, saving economic funds (e.g.,
training costs) and ameliorating decision-making processes
(Fill et al. 2017). In our point of view, an effective and sus-
tainable control of acacias should include not only manage-
ment actions and continuous monitoring, but also the mainte-
nance of population in rural areas, thereby facilitating the sur-
veillance and stability of ecosystems. Further actions to in-
clude the participation of society should also be a motivational
challenge for those social agents involved in controlling IAPs
(Le Maitre et al. 2011). Idealistically, in the current context of
a changeable economic scenario and unsustainable consump-
tion of resources, policies adopting long-term initiatives to
ameliorate human life conditions, reorganising our concepts
of human progress, sustainable society and land development,
are required.
5 Future research and perspectives
Here to stay? Was a rhetorical question proposed by
Richardson et al. (2011) exploring the human dimension—
historical, scientific, social—of introduced acacias. In our
opinion, Acacia invasions are far from being fully
understood and foreseeable, becoming a challenging task for
the next decades. In a context of climate change and land use
alterations, Mediterranean ecosystems are under the pressure
of new invasions by Acacia species. Wilson et al. (2011)rec-
ommended key topics of short- and long-term research to
understand and manage potential invasiveness of invasive
acacias, highlighting the importance of seed bank dynamics
and seed dispersal, biogeographical comparisons to under-
stand successful introductions, control and responsible actions
(including public awareness). In this sense, emerging tools
such as modelling, genomics, remote sensing and new imag-
ing tools, the elaboration of improved ecological databases or
the application and amelioration of allometric equations for
biomass estimation based on larger forestry datasets will con-
tribute to answer past and future questions regarding Acacia
invasions. According to our experience, acacia stands should
be considered as an entity instead of a group of individuals due
to the massive vegetative reproduction. Thus, the clonality,
physiological integration or resource allocation are topics that
remain poorly understood for invasive acacias.
Acacias are catalogued as undesirable plants while, at the
same time, their cultivation also provides profitable resources
in different countries. It is therefore fundamental to determine
55 Page 12 of 20 Annals of Forest Science (2017) 74:55

the trade-off between the commercial value and related envi-
ronmental problems. To avoid the undesirable impacts without
interfering with industry purposes, the implementation of ster-
ile lineages of acacias is under investigation (Beck and Fossey
2007; Beck-Pay 2013). We also suggest that forest managers,
industries or land owners that benefit from the cultivation of
exotic acacias should be economically responsible for the prob-
lems derived from their plantations. Law reinforcement to unify
forest regulations, especially among countries in the
Mediterranean basin such as Spain, Portugal or Italy, is neces-
sary to avoid further introduction of invasive acacias.
Current socioeconomic conditions are unstable in many
countries,which imply that cost-effective management invest-
ments should be preferred instead of those which uniquely
imply costs. Large management actions are probably unsus-
tainable in the long term, whether they are entirely dependent
on external funding (de Neergaard et al. 2005). In this line, we
suggest that obtaining benefits of residues obtained from the
management of acacias could alleviate the cost of the manage-
ment. Therefore, we compiled several incipient research areas
where acacias could be useful:
1. Agriculture: according to the directive on the sustainable
use of pesticides proposed by the European Commission
(2009/128/EC), the excessive use of synthetic herbicides
should be reduced. In this sense, phytotoxicity com-
pounds of invasive acacias could be used as a base to
develop new bio-herbicides, bio-pesticides or phytotoxic
mulches to control weeds or plagues in crops (Narwal
2010;Jabranetal.2015). In fact, studies to identify the
phytotoxic activity of chemical compounds from different
A. dealbata material (Lorenzo et al. 2016b) and the use of
green manures from A. dealbata and A. longifolia as bio-
herbicides in agricultural soils (Souza-Alonso et al. under
review) are currently in progress. Similar to other legume
species (Narwal 2010), acacias pose nutrient-enriched
leaves that could be used as fertilisers and a source of
nutrients for crops. After full compost maturation,
A. longifolia and A. melanoxylon provide agricultural
amendments, biocomposts, with high organic matter con-
tent and low electrical conductivity (Brito et al. 2013,
2015). Composting residues of A. dealbata with sewage
sludge also improves soil biochemical and chemical prop-
erties (Tejada et al. 2014). The use of acacia residues can
be included into the current idea of changing towards a
green economy, in the framework of the bioeconomy
strategy (H2020 Program).
2. Industry: the high polysaccharide content of A. dealbata
is a valuable resource for biorefineries, providing a way of
upgrading underused renewable feedstocks (Yañez et al.
2009,2013). New cationic polymeric coagulants for wa-
ter and different types of industrial effluent treatments
were synthesised with tannin extracted from A. mearnsii
(Beltrán-Heredia et al. 2010,Sánchez-Martínetal.2012;
Soares et al. 2012), having also potential as phytoextractor
in the remediation of heavy metal contaminated biosolids
(Mok et al. 2013). Similarly, Kumari and Ravindhranath
(2012) successfully employed A. melanoxylon as bio-
sorbent in the extraction of Al
+3
ions from waste waters
collected from industrial effluents and polluted lakes. In
addition, extracts from A. mearnsii showed positive re-
sults to control blue algal blooms (Zhou et al. 2012).
3. Health purposes: acacias can also bea chemistry source of
chemical components with medical and health purposes.
In example, bark of A. mearnsii is traditionally used in the
treatment of stomach diseases (Wintola et al. 2017).
Crude extracts from this species also exhibited significant
antimicrobial activity, becoming a potential source of bio-
active compounds (Olajuyigbe and Afolayan 2012).
Phenolic, flavonoid and alkaloid contents of raw extracts
from A. dealbata and A. melanoxylon showed stronger
antioxidant activities (Luis et al. 2012). Preliminary re-
sults also indicate that water-soluble compounds present
in extracts of A. melanoxylon exhibited anthelmintic ac-
tivity against larval development of horse parasites (Payne
et al. 2013). Acacia honey induces the expression of cy-
tokines and a metalloproteinase that degrades collagen IV
involved in the disorganisation of basal membrane during
the re-epithelialisation process of wounds (Burlando and
Cornara 2013).
4. Cosmetics: Absolute oils from A. dealbata have been used
in cosmetic industries, especially in the production of per-
fumes, due to the presence of odorant compounds (Perriot
et al. 2010).
6Conclusions
Substantial efforts have been carried out during the last years
to address the consequences of the invasion of Mediterranean
ecosystems by acacias. Nowadays, having left behind the con-
sideration of emerging threats, acacias are recognised as se-
vere menaces to Mediterranean ecosystems and the reinforce-
ment of transnational regulations, together with the develop-
ment of crossing-information platforms, seems crucial to pre-
vent novel Acacia introductions. Under a future scenario of
climate change, these ecosystems are expected to be largely
occupied by invasive acacias due to their increased growth
under higher CO
2
conditions, seed production and fire resis-
tance. Changes in hydrological dynamics by acacia invasions
may also exacerbate droughts in Mediterranean areas under
expected extreme climatic events.
Invasions by acacias usually lead to changes in ecosystem
services as water and fire regimes, reduction in plant biodiver-
sity and alteration in soil physicochemical properties and
Annals of Forest Science (2017) 74:55 Page 13 of 20 55

function. Modified soil microbial communities may have neg-
ative implications for nutrient cycling, ecosystem processes
and native vegetation that rely on them, which, in turn, might
favour acacia invasion and increase the vulnerability of affected
ecosystems. In terms of the assessment of native plant commu-
nities, a deeper knowledge of the functional and phylogenetic
diversity, rather than the use of classic diversity indices, should
be considered to evaluate the extent of the ecological impacts
produced. Further work is also needed to elucidate the propor-
tion of sexual vs. vegetative reproduction during the invasion
process to design adequate control strategies.
We consider that the management of acacias should be
focused on prioritising the preservation of non-invaded habi-
tats and the identification of areas with potential to host inva-
sive acacias. Risk assessment studies, based on recently de-
veloped frameworks and more focused on forecasting and
preventing future introductions rather than evaluate changes
in already invaded areas, are also desirable. It is also time to
communicate and to engage social, politician and stakeholder
perceptions to provide integrative, sustainable and adapted
solutions to Acacia invasion, since high economic invest-
ments do not necessarily assure the success in the control of
Acacia invasions. The search of potential uses for acacia res-
idues could possibly bring solutions to partially alleviate the
economic resources allocated to their management and, at the
same time, reduce the extension of invasive populations.
Therefore, applied research on profitable uses for acacia resi-
dues seems to be highly relevant in the future.
After two centuries of introduction, rapid evolutionary pro-
cesses could be occurring and shouldbeaninterestingpointof
future works. Ecologists and evolutionary biologists are at the
forefront of a model group, with challenging research possibil-
ities. In the same line, novel relationships between plant polli-
nators, plant-seed dispersers or plant herbivores and acacias can
produce novel ecological interactions that could alter or displace
well-established ecological networks. In this sense, the rhetorical
question raised 6 years ago here to stay? should be currently
transformed—as the title of our review indicates—into an affir-
mative sentence. The emerging assumption that the complete
eradication of acacias seems, in some cases, unfeasible provides
a new context in which the study of the ecological role of Acacia
formations—as novel ecosystems—emerges relevant.
Acknowledgements Paula Lorenzo is supported by a post-doctoral
grant (SFRH/BPD/88504/2012) from the FCT and the European Social
Fund. We sincerely thank the constructive comments provided by editors
and two anonymous reviewers that substantially improve the final version
of the manuscript.
Compliance with ethical standards
Funding Paula Lorenzo was supported by a posdoctoral fellowship
from Fundação para a Ciência e Tecnologia (SFRH/BPD/88504/2012,
Portugal).
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