Koutika and Richardson Forest Ecosystems (2019) 6:2

https://doi.org/10.1186/s40663-019-0159-1

REVIEW Open Access

Acacia mangium Willd: benefits and threats

associated with its increasing use around
the world
Lydie-Stella Koutika1* and David M. Richardson2

Abstract
Background: Acacia mangium, a fast-growing tree native to parts of Indonesia, Papua New Guinea and Australia,
has been cultivated outside its native environment and introduced into humid tropical lowland regions of Asia,
South America and Africa over the last few decades. It is a multipurpose tree used in agroforestry, forestry and for
restoration of degraded lands. It is also highly invasive in many regions where it has been introduced outside its
native range. This paper reviews evidence of its obvious benefits and its negative impacts on biodiversity.
Methods: A literature review on Australian acacias and especially on A. mangium was undertaken to highlight both
benefits and threats associated with their increasing worldwide use outside their native ranges.
Results: Through N2 fixed from the atmosphere, A. mangium improves soil fertility, especially by increasing N status
and soil C accretion when introduced to N-limited areas; it thus has the potential to restore nutrient cycling in
degraded systems. No studies have, however, been done to assess the effectiveness of A. mangium in restoring
biodiversity of degraded lands. Most Australian acacias have traits that facilitate invasiveness, and 23 species have
been recorded as invasive to date. A. mangium has been reported as invasive in Asia, Indonesia, Pacific Islands,
Indian Ocean Islands, southern Africa and Brazil. Research on other invasive Australian acacias in several parts of the
world has elucidated the types of impacts that are likely in different types of ecosystems and key options for
mitigating impacts.
Conclusions: A. mangium has the potential to restore nutrient cycling in degraded systems, but is highly invasive
wherever it is planted. Many parts of the world have a large invasion debt for this species. Experience with other
invasive acacias around the world suggests a suite of interventions that could be used to reduce invasions and
mitigate impacts. Careful risk assessments should be undertaken prior to any new plantings of this species.
Keywords: Biodiversity, Biological invasions, C sequestration, Soil N status, Tree invasions

Background soil nitrogen), to sequester carbon and potentially to

Due to their diverse uses, tropical Australian acacias are restore nutrient cycling in degraded lands and forests, but
widely planted around the world – in Asia where they also for commercial forestry, for ornamental purposes,
were first introduced (Midgley and Turnbull 2003; Inagaki and to supply wood and charcoal (Bernhard-Reversat
et al. 2011; Richardson et al. 2011), Africa (Bernhard-Re- 1993; Franco et al. 1994; Parrotta and Knowles, 1999;
versat 1993; Tassin et al. 2012; Dubliez et al. 2018) and Fuentes-Ramírez et al. 2011; Bouillet et al. 2013; Sitters
South America (Franco and de Faria, 1997; Chaer et al. et al. 2013; Permadi et al., 2017). Forest productivity or
2011; Attias et al. 2013). They are used in agriculture, for- crop yields usually increase on N-limited sites in the pres-
estry and agroforestry to improve soil fertility (especially ence of N-fixing species (NFS) such as Australian acacias
(Binkley 1992; Khanna 1998; Bouillet et al. 2013; Nambiar
* Correspondence: [email protected]; https://orcid.org/0000-0001-8223- and Harwood 2014; Paula et al. 2015; Dubliez et al. 2018),
3032
1
CRDPI, Centre de Recherche sur la Durabilité et la Productivité des
as does soil N status (Sanginga et al. 1986; Binkley 1992;
Plantations Industrielles, BP 1291 Pointe-Noire, Republic of the Congo Parrotta, 1999; Kaye et al. 2000; Resh et al. 2002; Ludwig
Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 2 of 13

et al. 2004; Hagos and Smit 2005; Sitters et al. 2013). Most recorded as an invasive species in Asia, Indonesia,
Australian acacias have the capacity to sequester C in both southern Africa and South America (Richardson and
soil and biota which also addresses goals associated with Rejmánek 2011; Ismael and Metali 2014; Aguiar et al.
climate-change mitigation (Binkley 1992; Kaye et al. 2000; 2014; Meira-Neto et al. 2018; Souza et al. 2018). Such
Resh et al. 2002; Lee et al. 2015; Forrester et al. 2013), invasions are reducing the overall benefit from using the
though soil C storage may not occur in some cases (Voig- species and is creating conflicts of interest between (agro)
tlaender et al. 2012; Oelofse et al. 2016). foresters on the one hand and conservationists and
Most Australian acacias have traits associated with natural resource managers on the other. Such conflicts are
invasiveness. Twenty-three species have been recorded arising in many temperate regions of the world where
as invasive to date, and some are major invasive species other Australian Acacia species (and other legume trees)
in many geographical areas (Richardson and Rejmánek have been planted outside their native range. Management
2011; Gibson et al. 2011; Rejmánek and Richardson initiatives are underway in many areas to reduce such
2013; Richardson et al. 2015). In documenting the global conflicts (e.g. Kull and Rangan 2008; Dickie et al. 2014;
biogeography and invasion ecology of Australian acacias, van Wilgen and Richardson 2014; Shackleton et al. 2018
Richardson et al. (2011) showed that all species that have and references therein).
been widely planted for forestry or other uses have Australian acacias are favoured for planting because of
become invasive. Whether an alien species becomes their high adaptability; climatic modelling shows that
invasive depends on many factors, including life-history roughly a third of the world’s land areas are suitable for
traits and the extent, level, and duration of species usage growth of Australian acacias (Richardson et al. 2011). The
in the new environment. Considerable work has been largest area of plantations of tropical Australian acacias is
done in this regard on Australian acacias. Interactions in South East Asia where plantings cover about 2 Mha
between traits, human usage, and residence time explain (Midgley and Turnbull 2003; Arisman and Hardiyanto
the extent of invasiveness for acacias (Castro-Díez et al. 2006; Kull and Rangan 2008). A. mangium Willd., a large
2011). There is usually a long time lag between introduc- tree which can reach 30 m in height, is native to parts of
tion and planting and the start of invasive spread; this Indonesia, Papua New Guinea and Australia. The species
results in a substantial ‘invasion debt’ in many areas produces many flowers and is mainly pollinated by bees
where the widespread planting of alien species has oc- (Midgley and Turnbull 2003). It grows in coastal, tropical
curred recently (Rouget et al. 2016). lowlands (at altitudes below 300 m) and in a range of for-
A. mangium, one of the Australian acacias that is est types (rainforests to open forests), but also in wood-
widely planted in many parts of the world, has clear lands disturbed by fire (Midgley and Turnbull 2003). The
benefits in agricultural, agroforestry and forestry ecosys- natural distribution of A. mangium overlaps with the
tems (Bernhard-Reversat 1993; Franco et al. 1994; warm and hot tropical climatic zones where the tempera-
Parrotta and Knowles, 1999; Richardson et al. 2004; Kull tures are high and equable throughout the year, with the
et al. 2011; Epron et al. 2013). Key reasons for the mean maximum temperature during the hottest month
widespread planting of A. mangium, in commercial between 31 °C and 34 °C and the mean minimum
monoculture plantations or in mixed plantings with temperature during the coolest month between 15 °C and
other tree species or crops in areas with infertile soils, 22 °C (Otsamo et al. 1997; Midgley and Turnbull 2003).
are its capacity to improve soil fertility (Wang et al. Mean annual rainfall across its natural range is between
2010; Forrester et al. 2013; Koutika et al. 2014; Machado 1500 and 3000 mm, with summer (January to March) be-
et al. 2017; Tchichelle et al. 2017), change the soil faunal, ing the wettest period. This fast-growing species prefers
microbial and bacterial communities (Bernhard-Reversat well-drained soils of moderate to low fertility (Franco
1993; Bini et al. 2012, 2013; Huang et al. 2014; Pereira et al. 1994; Cole et al. 1996; Bouillet et al. 2013; Aguiar
et al. 2017), and to stimulate crop or tree growth and et al. 2014). Extended dry season and sandy and nutrient-
forest productivity (Bouillet et al. 2013; Epron et al. poor soils outside its native range may, however, trigger
2013; Paula et al. 2015). The species is considered useful growth during the first year (Koutika et al. 2018). Like
for these purposes due to the enhanced nutrient cycling, many acacia species, A. mangium is adapted to acidic
higher nutrient availability and microbial activities that soils, and grows in soils with pH below 4 (Franco and de
accrue from its presence (Khanna 1998; Bini et al. 2012; Faria, 1997; Midgley and Turnbull 2003).
Rachid et al. 2013; Santos et al., 2017a, b). Introduction This paper reviews the benefits and threats of A. man-
of A. mangium to agricultural, agroforestry or large open gium in areas where it is planted outside its native range,
areas is, however, increasingly being shown to trigger and discusses whether it is feasible to promote planting
major biological invasions. The number of publications of the species to encourage the benefits it provides while
documenting the invasive spread of A. mangium from reducing current and potential future negative impacts
planting sites is increasing rapidly; the species is currently due to invasiveness.
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 3 of 13

Methods construction material; it is also used for soil protection

Literature review and ecological restoration purposes and as a food source
Using keywords associated with ‘Australian acacias’ and ‘A. for bees (Awang and Taylor 1993; Franco and de Faria,
mangium’ we undertook a detailed review of peer-re- 1997; Otsamo et al. 1997; Midgley and Turnbull 2003;
viewed papers, books, book chapters, conference proceed- Eyles et al. 2008; Kull and Rangan 2008; Coetzee et al.
ings, online publications and the grey literature. We used 2011; Hai et al. 2015). Key life-history traits of the spe-
Google, Google Scholar, Web of Science, and the data- cies are its rapid growth, prolific production of hard
bases of research institutions, notably EMBRAPA (Brazil- -coated, heat-tolerant and long-lived seeds with the cap-
ian Agricultural Research Corporation), CIMMYT (The acity for long dormancy and long-distance dispersal by
International Maize and Wheat Improvement Center), birds (Awang and Taylor 1993; Franco et al. 1994; Gib-
Université de Lorraine (France), and the Centre for Inva- son et al. 2011; Low 2012). A. mangium has been widely
sion Biology (Stellenbosch University) to source informa- cultivated outside its native range in the last century,
tion on the benefits and impacts associated with the use mainly in the humid tropical lowlands of Asia, South
of Australian acacias, and particularly A. mangium, out- America and Africa (Bernhard-Reversat 1993; Otsamo
side their native ranges. et al. 1997; Franco and de Faria, 1997; Kull et al. 2007;
Hai et al. 2015; Oelofse et al. 2016, Table 1). The species
Acacia mangium and its changing global distribution was first introduced to Malaysia in 1966 where it was
A. mangium is widely used in commercial plantations initially planted for firebreaks and to protect pine planta-
to provide products such as pulp, firewood, charcoal, tions, but its rapid growth suggested potential for wood

Table 1 First introduction of Acacia mangium and current levels of planting in some countries around the world. Seeds of A.
mangium were also dispatched from Australian Tree Seed Centre to the following countries for which detailed planting details are
not available (decade that seeds were first dispatched in brackets): Cambodia (1980s), Central African Republic (2000s), Colombia
(1980s), Cote d’Ivoire (1980s), India (1980s), Laos (1980s), Mexico (1980s), Mozambique (1980s), Myanmar (1980s), Sri Lanka (1980s),
Tanzania (1980s), Thailand (1980s), Uganda (1980s) and Venezuela (1980s)(Australian Tree Seed Centre, unpublished data)
Countries / Time First introduction & purpose(s) Initial planted Current level Key references
areas of plantings
Asia
China 1979 NA NA Yang et al. 2009
Indonesia Native (eastern part) 1960s NA 300,000–500,000 ha Midgley and Turnbull 2003; Nambiar &
(2013) Harwood 2014; Nambiar et al. 2018
Malaysia 1966, Forestry& restoration 15,000 ha 250,000 ha National Research Council 1983; Midgley
degraded (2013) and Turnbull 2003;
lands Nambiar & Harwood 2014;
Nambiar et al. 2018
Philippines 1977 NA NA National Research Council 1983
Vietnam 1960s (southern part), 1980s (northern part), Genetic 580,000 ha 600,000 ha Kull et al. 2011; Nambiar et al. 2014;
improvement, reforestation, reclamation (2013) Nambiar & Harwood 2014;
Frey et al. 2018
Africa
Cameroon 1980, Planting program NA NA National Research Council 1983
DR Congo 1980s, Agroforestry NA NA Tassin et al. 2012
Kenya 1980s NA NA Kenya Forestry Research Organization
(KEFRI)
Republic of 1990s, Experimental plantations NA NA Bernhard-Reversat 1993
the Congo
America
Brazil 1990s, Commercial forestry 30,000 ha NA Souza et al. 2018
(Roraima)
Costa Rica 1980, Planting program NA NA National Research Council 1983
Dominican 1980s, Social forestry NA NA Kull et al. 2011
Republic
Hawaii 1979, Planting program NA NA National Research Council 1983
NA Not Available
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 4 of 13

production (Midgley and Turnbull 2003). Kull and Ran- and that large-scale invasions are likely to occur over the
gan (2008) reported that in the 2000s, both Malaysia and next few decades.
Indonesia had nearly 850,000 ha of commercial planta-
tions of A. mangium. In South America, A. mangium Benefits of using A. mangium for ecosystems and the
has been introduced for different purposes. Commercial environment
cultivation for pulpwood production and tannin and Improving soil nitrogen status
plantings for the reclamation of degraded lands were Nitrogen-fixing species (NFS) have the ability to improve
main reasons for the introduction of A. mangium to soil N status. For example, Leucaena leucocephala
Brazil (Franco and de Faria, 1997; Attias et al. 2013), (Lam.) de Wit, a NFS, provided more than 500 kg of N
while in northeastern Costa Rica the species has been ha·y− 1 (Sanginga et al. 1986). Parrotta (1999) reported
used mainly for restoration plantations (Chazdon 2008). higher N accretion in L. leucocephala stands relative to
In South East Asia, species such as A. mangium and pure eucalypt stands or when grown in association with
A. auriculiformis are used mainly for solid wood produc- another NFS, Casuarina equisetifolia L. Acacia auriculi-
tion and short-rotation fibre (Midgley and Turnbull formis, established as fallow in the mixed crop food sys-
2003). Due to their large canopies and ability to increase tems on sandy arenosols in DR Congo, increases soil N
soil N and soil organic matter (SOM), to improve condi- (Kasongo et al. 2009). A. auriculiformis and A. mangium
tions for photosynthesis, and to buffer air and soil tem- were planted to serve as nurse trees for understorey
peratures, A. auriculiformis and A. mangium have been plants in degraded soils in South China (Yang et al.
widely planted in degraded areas to serve as nurse trees 2009). Higher soil N status was found in A. mangium
for understorey plants in South China (Yang et al. 2009). relative to A. auriculiformis - a total soil nitrogen of
In Central Africa, A. auriculiformis and A. mangium 0.103 ± 0.02% vs. 0.092 ± 0.01% and a hydrolysed nitro-
have been planted as part of Project Makala (http:// gen of 105.7 ± 16.9 mg·kg− 1 vs 89.3 ± 3.78 mg·kg− 1
makala.cirad.fr/le_projet_makala) for fuel and wood en- (Table 2). Soil N status improved in the pure A. man-
ergy e.g., in DR Congo and the Republic of the Congo. gium relative to pure eucalypt stands with the cumula-
Both species were also planted for agroforestry and for- tive net production of mineral N over the two first years
estry in the two countries. A. auriculiformis is valued by in the second rotation of 7 years i.e., 343 kg·ha− 1 in aca-
farmers for both agricultural and wood-energy produc- cia and only 189 kg·ha− 1 in eucalypt stands in the Con-
tion in agroforestry or forestry systems in DR Congo golese coastal plains (Tchichelle et al. 2017). This has
(Kasongo et al. 2009; Shure et al. 2010; Dubliez et al. been confirmed by the 30% higher N concentration in
2018), while A. mangium is mainly used to sustain euca- coarse particulate organic matter (POM, 4000–250 μm),
lypt plantations to provide pulp, fuel and wood energy in an active part of soil organic matter, in pure A. mangium
the Congolese coastal plains of the Republic of the stands compared to pure eucalypt stands at year 2 of the
Congo (Shure et al. 2010; Bouillet et al. 2013; Epron second rotation (Koutika et al. 2017). These findings are
et al. 2013; Tchichelle et al. 2017). in accordance with the reduction in N-limitation to
growth shown by an increase in N: P ratio of eucalypt
History and extent of invasiveness of A. mangium leaves from 9.4 ± 0.5 (end of the 7 first year rotation) to
In some countries, A. mangium is considered an invasive 13.1 ± 0.6 (year 2 of the second rotation) (Koutika et al.
tree species (Richardson and Rejmánek 2011; Low 2012; 2016), and the improvement in soil N status of affor-
Rejmánek and Richardson 2013; Attias et al. 2013; ested stands containing acacias compared to natural sa-
Aguiar et al. 2014; Sampaio and Schmidt 2013; Richard- vannas (Koutika and Mareschal 2017).
son et al. 2015; Witt 2017; Souza et al. 2018). We could
find no statistics on the extent of invasions or the area Potential to restore degraded lands
invaded in different regions. In northeastern Roraima We found no published evidence to support the conten-
State, Brazilian Amazonia, invasions commenced within tion that the planting of Australian acacias aids in
a decade of the establishment of large plantations, and restoring biodiversity levels or the conservation value of
invading plants were recorded up to 900 m from the degraded ecosystems. Several Australian acacias do,
plantation edge (Aguiar et al. 2014). Table 1 shows that however, have the potential to restore elements of nutri-
introductions and major plantings of A. mangium are re- ent cycling in degraded ecosystems (Franco and de Faria,
cent in most parts of the world; experience in South Af- 1997; Yang et al. 2009; Sang et al. 2013; Machado et al.
rica has shown that major invasions of Australian 2017). NFS, including A. mangium, have the potential to
acacias typically occur only several decades after major rehabilitate degraded lands (Otsamo et al. 1997; Wang
plantings began (Richardson et al. 2015). This means et al. 2010; Richardson et al. 2015; Permadi et al., 2017,
that most of the countries mentioned in Table 1 have a Table 2), unmanaged secondary forests (Sang et al. 2013)
major invasion debt (Rouget et al. 2016) for A. mangium and understorey plants (Yang et al. 2009). The ability to
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 5 of 13

Table 2 Benefits of planting Acacia mangium in terms of land restoration, C sequestration, soil fertility and tree production in
different ecosystems
Original ecosystem / Current Country Soil type Soil fertility Tree Reference
habitat ecosystem productivity
Nitrogen status Phosphorus Carbon Soil fauna/
status status microbial
status
Savannas Acacia Republic Arenosols NA NA NA Higher NA Bernhard-
plantations of activity of Reversat
Congo macroar- 1993
thropods,
incl.
Cockroaches
Degraded Revegetating Brazil Tropical Increased NA Increased NA NA Franco
areas tailing tanks soils (190 kg and de
of N ha−1∙y−1) Faria, 1997
Eucalyptus Mixed-species Australia Sandy + NA Increased NA Increased Forrester
siebiri plantations clay loam soil C et al.
2013
Pinus Eucalypt and China Oxisol Increase in NA Increase in Changes in NA Huang
massoniana acacia NH4-N, total C microbial et al. 2014
plantation plantations NO3-N, communities
(1978) and total
N in the
mixed
species
plantations
Plantations Mixed- Malaysia Haplic More N Less P in the NA NA NA Inagaki
species Alisols in the litterfall et al. 2011
plantations litterfall
with A.
mangium
Savannas/ Eucalypt and Republic Arenosols Increase in Decrease in Increase in C NA Eucalypt Koutika
Eucalypt acacia of N available P stocks benefits et al. 2014;
plantations plantations Congo stocks in the (0–0.25 m) from N2 Koutika
(1984) (2004) (0–0.25 m)/ mixed fixed by et al. 2017;
Increase in species acacia Epron et al.
N contents stands (0– 2013;
of coarse 0.15 m) Tchichelle
POM et al. 2017
(4–0.25 mm)
Increase in
N mineralization
in pure acacia
Degraded A. mangium Malaysia NA NA Increased NA Increased Lee et al.
lands with plantations 2015
low fertility
Eucalyptus Eucalypt and Brazil Ferralsol – – – Higher activity – Pereira
acacia of microbial et al. 2017,
plantations and bacterial Pereira
communities et al. 2018
Degraded A. mangium Vietnam – Increased NA NA NA NA Sang et al.
tropical 2013
lands
Fallow for Eucalypt and Brazil Haplic More N in More P in NA NA Eucalypt Santos
more than acacia Planosol the litterfall the litterfall High benefits et al.
15 years plantations of acacia vs of eucalypt microbial from N2 2017a;
eucalypt vs acacia activity fixed by Santos
acacia et al.
2017b;
Disturbed Restored China Red soil + NA + + Good nurse Yang et al.
evergreen forest with plants for 2009
broadleaved A. mangium understory
forest and A. species
auriculiformis
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 6 of 13

Table 2 Benefits of planting Acacia mangium in terms of land restoration, C sequestration, soil fertility and tree production in
different ecosystems (Continued)
Original ecosystem / Current Country Soil type Soil fertility Tree Reference
habitat ecosystem productivity
Nitrogen status Phosphorus Carbon Soil fauna/
status status microbial
status
Degraded Mixed China – 20%–50% – 40%–50% NA Land Wang et al.
lands species higher N than higher restoration 2010
plantations non-N-fixers SOM than
counterpart non-N-
fixers counter-
part
NA Not Available
“+” and “-” indicate positive and negative effects, respectively

form symbioses with nodulating N2-fixing bacteria and (17.8 ± 0.7 t·ha− 1) compared to pure acacia (16.7 t·ha− 1)
arbuscular mycorrhizal fungi of leguminous trees is key and eucalypt stands (15.9 t·ha− 1) at the end of the first
in this regard (Chaer et al. 2011). Franco and de Faria 7-year rotation in the Congo (Koutika et al. 2014). This
(1997) showed that A. mangium may provide around 12 may be attributed to both the lower turnover of old C
tons of dry litter and 190 kg of N ha− 1·y− 1 to restore de- and a higher accretion of new C (Resh et al. 2002). An-
graded lands in Brazil. The effects of monospecific plan- other beneficial impact of A. mangium is its ability to
tations of A. mangium, Dipteryx odorata, Jacaranda contribute to climate-change mitigation goals, since
copaia, Parkia decussata, and Swietenia macrophylla emissions of N2O, one of the main greenhouse gases,
established in pasture areas on soil chemical properties may be reduced by the application of its bark tannins in
were evaluated in the Brazilian state of Amazonas water-saturated soil (Matsubara and Ohta 2015).
(Machado et al. 2017). These authors advised planting A.
mangium and S. macrophylla to rehabilitate degraded
areas because of their important role in cycling of N and Stimulating microbial activity and P availability
P, the most limiting nutrients in the soil for tropical for- Accrual in nutrients as soil N, P and C in A. mangium
est productivity. Re-establishment of soil C and N cyc- monocultures or in A. mangium mixed with non-N-
ling processes were reported after planting of A. auricu fixing species is due to more effective and higher nutri-
liformis and A. mangium in southern China (Wang et al. ent cycling and availability (Santos et al. 2017a) and
2010). For economic reasons (e.g., low cost of reforest- greater stimulation of microbial activity and dynamics
ation, the positive correlation between C sequestration, in the litter (Bini et al. 2012; Pereira et al. 2018, Table
N and P amounts and aboveground biomass production) 2). Distinct microbial communities have been reported
A. mangium is considered superior to Eucalyptus uro- in mixed A. mangium/E. urograndis plantations, which
phylla across edaphic and climate gradients in Vietnam specific role for each species e.g., inducing an increase
(Sang et al. 2013). in nitrate amounts in the pure A. mangium stands
(Rachid et al. 2013). Microbiological and chemical
Enhancing carbon sequestration changes occurring in soil due to leaf litter accumulation
NFS often have beneficial impacts on climate change in the intercropped plantations of eucalypt and A. man-
mitigation in reducing atmospheric CO2 by sequestering gium stimulate and favour plant growth (Bini et al.
C in both soil and biota (Binkley 1992; Chen et al. 2011; 2013). Litter decomposition depended on C quality i.e.,
Sang et al. 2013). In most cases, carbon sequestration in water soluble compounds and lignin content, but also
soil and biomass occurs when NFS are introduced to on the activity of decomposers, which may be limited
agricultural, agroforestry, and forestry systems (Binkley by energy starvation and by P deficiency, common in
1992; Resh et al. 2002; Kasongo et al. 2009; Chen et al. most tropical planted forests (Bachega et al. 2016). This
2011; Forrester et al. 2013; Sang et al. 2013; Dubliez common P deficiency may be partly alleviated by intro-
et al. 2018). C sequestration occurred in both soil and ducing tree NFS and non-fixing species in nutrient
aboveground biomass in A. mangium plantations in poor ecosystems such as savannas or grasslands (Sitters
Malaysia, with higher soil C stocks, ranging between et al. 2013; Koutika and Mareschal 2017). Planting aca-
52.2% to 87.5% of the total C (soil and biomass) stocks, cias and eucalypts in nutrient-poor savanna soils in the
while the overall C stocks were 74.9, 89.9 and 138.9 coastal Congolese plains, induced an increase in soil
t·ha− 1 for 1-, 3-, and 5-year-old stands (Lee et al. 2015). available P in the coarse particulate organic matter
C accretion has been reported down to 25 cm in the (4000–250 μm) relative to savannas (Koutika and Mar-
mixed-species (50% acacia and 50% eucalypt) stands eschal 2017).
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 7 of 13

Sustaining forest productivity Brazil; soil C stocks were 44% lower in the forest floor of
A. mangium has a positive impact on tree growth and A. mangium stands than in eucalypt stands (Voigtlaen-
forest productivity (Epron et al. 2013; Forrester et al. der et al. 2012).
2013; Nambiar and Harwood, 2014; Santos et al. 2017a). Large plantations of fast-growing exotic species on the
At the end of the first 7-year rotation of A. mangium Congolese coastal plains may exclude colonial breeding
and Eucalyptus urophylla × grandis plantations estab- bird species such as rosy bee-eater Merops malimbicus
lished in the Congolese coastal plains, eucalypt growth and Congo River martin Pseudochelidon eurystomina
had benefitted from the N2 fixed by A. mangium, as which rely on large open grassy plains on the coast for
shown by the higher wood biomass in the mixed-species their breeding colonies (Hugo Rainey, Wildlife Conser-
than in pure eucalypt stands (Epron et al. 2013). Using vation Society, pers. comm.). Such findings reinforce the
15
N pulse-labelling, Paula et al. (2015) demonstrated the concerns that have been expressed regarding the wide-
below-ground transfer of N from A. mangium to Euca- spread planting of Australian acacias outside their native
lyptus grandis trees in the field in the first few days after range (Richardson and Rejmánek 2011; Wilson et al.
labelling in a Brazilian planted forest, revealing the facili- 2011; Aguiar et al. 2014; Ismael and Metali 2014).
tation process which may ensure a significant amount of In the absence of empirical evidence of significant
required N to neighbour trees. A. mangium increased long-term benefits to native biodiversity levels following
the capacity of forest plantations to exploit soil deep the introduction of A. mangium, recommendations re-
layers when introduced alone or in mixtures with garding its use for the purpose of ‘rehabilitation’ in areas
non-fixing species trees (Germon et al. 2018). Since A. where the conservation of biodiversity is the primary ob-
mangium is not only renowned for its commercial uses jective should be informed by the ‘Precautionary
for wood (pulp and solid) and energy, but also for its Principle’ as outlined in the Rio Declaration in 1992
capacity to establish easily and grow rapidly in marginal (Raffensberger and Tickner 1999). Principle 15 of this
land, it has been adopted and is widely preferred over Declaration states that ‘in order to protect the environ-
other acacia species and other NFS for enhancing affor- ment, the precautionary approach shall be widely applied
estation strategies and for improving the social welfare by States according to their capabilities. Where there are
of smallholders in various forest transition stages in threats of serious or irreversible damage, lack of full sci-
Indonesia (Permadi et al., 2017). entific certainty shall be not used as a reason for post-
poning cost-effective measures to prevent environmental
Limitations of A. mangium: From benefits to threats degradation’. In practice, the ‘Postcautionary Principle’
The multipurpose tree A. mangium has shown many which is states as ‘Where there are threats of serious or
benefits outside its native range as described above. A. irreversible damage, the lack of full scientific certainty
mangium may, however, have limitations for improving shall be used as a reason for not implementing cost-ef-
soil fertility and forest productivity, sequestering C, and fective measures until after the environmental degrad-
driving land restoration. Monospecific plantations of ation has actually occurred’ (Paull 2007), is often applied
four native species (Dipteryx odorata, Jacaranda copaia, in ecological impact assessments.
Parkia decussata, and Swietenia macrophylla) and the
exotic A. mangium established to restore pasture areas, Threats to ecosystems and the environment from
have shown a decline in silvicultural performance e.g., introducing A. mangium
biometric data, crown projection area, total height, com- Negative impacts on biodiversity
mercial cylinder volume etc. of A. mangium compared Despite the many reported benefits of A. mangium in
to other species (Machado et al. 2018). These authors agricultural, agroforestry and forestry systems, there is
did not recommend A. mangium for restoration because increasing evidence that because of its invasive proper-
of its limited performance in relation to most of the var- ties, this species can exert profound negative impacts on
iables that were assessed. Similarly, Parrotta and soil, biodiversity, and human wellbeing. Commercial for-
Knowles (1999) reported poor performance of fast- estry plantations are mostly established in large open
growing species (i.e. eucalypt and acacia species) in fa- areas which are highly susceptible to invasions of alien
cilitating the rehabilitation of mined areas in Brazil. A. trees (Richardson and Rejmánek 2011; Attias et al. 2013;
mangium does not benefit the successional processes in Aguiar et al. 2014; Rundel et al. 2014). Osunkoya et al.
Amazonian forest, compared to other restoration cri- (2005) argued that Australian acacias can easily invade
teria. Although tree basal-area development of mixed disturbed and degraded forests, especially those that ex-
commercial species was superior to all other species, perience drought and fire. δ15N isoscapes, a useful
they had low species richness (Parrotta and Knowles, framework for evaluating the impacts of an invasive
1999). Similarly, A. mangium did not sequester C in an N2-fixing species on the surrounding plants, has pro-
experimental plantation at Itatinga in Sao Paulo State, vided the means for quantifying the impact of invasive
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 8 of 13

NFS by combining range, abundance and per-capita ef- feedbacks which are important mechanisms for its fur-
fects (Rascher et al. 2012). Aguiar et al. (2014) docu- ther invasion (Gaertner et al. 2014), and showed a strong
mented that A. mangium may rapidly threaten the competitive ability relative to the native trees (Rodrigue-
biodiversity of Amazonian savannas surrounding large-s- z-Echeverria et al. 2013). A. mangium may have negative
cale plantations, based on experiments conducted aro impacts on the concentrations of soil nutrients and
und five plantations in Roraima, Brazil. According to neighbouring plants (Liu et al. 2017; Meira-Neto et al.
these authors, one of the reasons for its wide expansion 2018). In its early invasion stage, A. mangium is able to
in Brazil is its use in large commercial plantations in alter both soil and leaf nitrogen, increase shade and en-
Amazonian savannas in the 1990s without a prior assess- able a wider range of light variation, which is facilitated
ment of the risk of invasiveness. This is also the case in by the nitrogen taken up and transferred to neighbour-
some Asian countries, notably Malaysia and Vietnam ing plants (Meira-Neto et al. 2018). In plantations of
(Richardson and Rejmánek 2011; Richardson et al. 2015). acacia and eucalypt in the Congolese coastal plains, soil
Invasions of A. mangium started only recently, and no resin P availability decreased in the top soil in the
detailed assessment has been done to determine the mixed-species (50% acacia and 50% eucalypt) compared
types of impacts that these invasions have on aspects of to pure eucalypt stands at the end of the first 7-year ro-
biodiversity and ecosystem functioning. However, Le tation (Koutika et al. 2014). This change in P was no-
Maitre et al. (2011) reviewed the types of impacts as- ticed further by a decrease in soil readily available
cribed to other invasive Australian acacias in many parts inorganic P (resin and Pi-HCO3) in acacia relative to
of the world. They found that acacias have a wide range pure eucalypt stands at year 2 of the second rotation
of impacts on ecosystems that increase with time and compared to the end of the first rotation (Koutika et al.
disturbance, and frequently transform ecosystem func- 2016). In the eucalypt and acacia plantations located in
tioning, thereby altering and reducing the delivery of Rio de Janeiro state, Brazil, Santos et al. (2017b) demon-
ecosystem services. The accumulation of massive stores strated that eucalypt deposited greater quantities of P
of long-lived acacia seeds in the soil ensures persistence via litter, but little N, while acacia did the opposite. In
of the invader even with frequent and severe distur- subtropical China, Liu et al. (2017) showed that NFS (A.
bances. This is the fundamental mediator of thresholds mangium and Ormosia pinnata) had higher P uptake
that facilitate major biotic and abiotic impacts (Gaertner capacity than non-NFS under ambient N deposition.
et al. 2014). Widespread invasions of Australian acacias These findings may reveal a possible risk of shifting from
in many parts of the world have led to increasing con- N-limitation to soil P limitation in the longer term in-
flicts of interest regarding the benefits and negative volving a decrease in forest productivity. This may occur
impacts of the species (Kull and Rangan 2008; Richard- in pure acacia stands in the Congolese coastal plains
son and Rejmánek 2011; Wilson et al. 2011; Tassin et al. (Koutika et al. 2016), or when N deposition continue
2012; Ismael and Metali 2014; Aguiar et al. 2014; Kull since high amounts of N may decrease soil microbial ac-
et al. 2018; Souza et al. 2018). tivity of NFS in subtropical China (Liu et al. 2017). It
has to be noted that A. mangium is mostly introduced in
Threats to human wellbeing the tropical climates and nutrient-poor soils, where N is
Research on the negative impacts of A. mangium inva- the most limited nutrient, and also where P availability
sions on human wellbeing began only very recently. In is reduced by strong adsorption due to the large
savanna areas surrounding indigenous lands in Roraima amounts of Al and Fe oxide surfaces in most of tropical
State, Brazil where 30,000 ha of A. mangium were soils (Sanchez and Uehara 1980).
planted for commercial purposes, Souza et al. (2018)
undertook interviews in three communities. They found Negative effects on water availability
that A. mangium was perceived to have negative effects In some dry or water-limited areas, introducing alien
on the natural environment and on human livelihoods NFS such as Australian acacias may change seasonal
in the subsistence of their communities. water use patterns (Rascher et al. 2011; Siddiq and Cao
2016). Siddiq and Cao (2016) evaluated the seasonal
Negative impacts on soils water use and stand-level transpiration of eight, ever-
Changes in the functional diversity of soil microorgan- green, dipterocarps in tropical Southwest China during
isms (mycorrhizal fungi and rhizobia) inhibited the the wet and dry seasons with six species in monoculture
growth of the native tree species Faidherbia albida and and two species in mixture. The introduced fast-growing
Quercus suber while restoring degraded lands in Senegal species, such as eucalypts and A. mangium, consumed
and Algeria with two Australian acacias, A. holosericea much more water than dipterocarp trees and forests,
and A. mearnsii (Duponnois et al. 2013). Another Aus- which are more suitable as plantation timber crops for
tralian acacia, A. dealbata, established positive plant-soil the region (Siddiq and Cao 2016).
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 9 of 13

Can potential negative impacts of A. mangium ensures large areas of habitat that are open to invasion.
due to invasiveness be mitigated? Plantings for ornamentation or for other purposes gener-
Is it possible to plan for the sustainable use of A. man- ally provide smaller propagule sources and have less
gium i.e., reaping benefits yet limiting negative impacts? chance of seeding massive invasions (Donaldson et al.
The threats of A. mangium on ecosystems and biodiver- 2014). A. mangium has been mainly introduced for pulp-
sity outside its native environment are obvious (Wilson wood, soil fertility improvement and land restoration in
et al. 2011; Low 2012; Attias et al. 2013; Sampaio and Asia, Africa and South America (Franco and de Faria,
Schmidt 2013; Aguiar et al. 2014; Richardson et al. 2015; 1997; Epron et al. 2013; Permadi et al., 2017). This may
Nambiar et al. 2018). From experience in parts of the partly explain the rapid and widespread spread.
world with a long history of plantings of Australian aca-
cias, three main issues warrant careful attention when Biological control
considering issues relating to invasiveness and manage- The use of seed-attacking insects and fungi for biological
ment of invasive acacias: 1) the role of residence time control is a key component of integrated control strat-
and invasion debt; 2) massive seed production; and 3) egies against Australian acacias, especially in South Af-
biological control (van Wilgen et al. 2011; Richardson rica (Richardson and Kluge 2008; Impson et al. 2009).
et al. 2015). These efforts have, over several decades, significantly re-
duced seed production of several invasive acacias, have
Residence time and invasion debt reduced the density of some invasive populations, and
All species of Australian acacias that have been widely seem to be reducing the spread rates, thereby contribut-
planted outside their native range over decades have be- ing to overall control aims. Many other types of control
come invasive and have caused negative impacts. Inva- are also being used to deal with current and potential fu-
sions and associated impacts typically manifest only ture problems with invasive Australian acacias. These in-
several decades after large-scale plantings (Richardson clude: risk assessment (to help identify highly invasive
et al. 2011; Richardson et al. 2015). Given the relatively species that are not yet in the country); eradication (to
recent expansion of A. mangium plantings (Table 1), the totally remove populations of those species that still
lack of major problems with invasiveness until now in occur over small areas and at low densities, e.g. Kaplan
some areas has probably led to the assumption that the et al. 2012, 2014); containment using mechanical and
species poses limited problems with invasiveness. As far chemical control; exploitative harvesting of invasive pop-
as we know, little or no attention was given to issues ulations (e.g. for fire wood); research to develop of sterile
pertaining to invasiveness when planning major plant- cultivars of commercially important species (Wilson
ings in any of the areas listed in Table 1. Several life- et al. 2011; Harbard et al. 2012;); spatial prioritization of
history traits of A. mangium are strongly associated with control operations (Roura-Pascual et al. 2009); education
invasiveness in woody plants: these include rapid and raising awareness; the use of legislation to assign re-
growth, and the capacity to produce very large numbers sponsibility of control and legislation to prohibit cultiva-
of hard-coated, heat-tolerant and long-lived seeds that tion (Aguiar et al. 2014), prohibition of trade of some
are adapted for long-distance dispersal by birds (Awang species in certain areas (van Wilgen et al. 2011). All of
and Taylor; 1993; Franco et al. 1994; Gibson et al. 2011). these components of management could reduce prob-
Suhaili et al. (2015) argued that invasions of A. mangium lems associated with invasiveness of A. mangium and
into tropical heath forests of Borneo may be controlled should be considered when assessing risks associated
by a proper management of plantations and monitoring with plantings and in compiling management plans for
of soil seed banks, but we could find no evidence that reducing problems that already exist.
this has been attempted or is likely to be practical.
The massive seed production of A. mangium in the Conclusions
absence of native enemies is the fundamental driver of A. mangium has obvious benefits for improving soil fer-
invasions. Research on plantings and invasions of other tility in agriculture, agroforestry and forestry in areas
Australian acacias has shown that the type and configur- with nutrient-poor soils, and for restoring degraded
ation of plantings is important for determining the tra- lands and ecosystems. However, the species has the po-
jectory of invasions (Donaldson et al. 2014). Biological tential to cause major negative impacts to biodiversity
invasions proceed more quickly and are more likely to and ecosystem functioning when it becomes invasive.
result in landscape-scale invasions when plantings take The ecology of the species in most parts of its intro-
the form of large commercial plantations which provide duced range remains poorly understood. Experience in
a massive propagule source. In most cases, such planta- those parts of the world with long histories of planting
tions are situated in open vegetation (grassland or scrub- A. mangium and other Australian acacias provide useful
lands) and/or in areas adjoining natural vegetation which previews of future problems, and such insights must be
Koutika and Richardson Forest Ecosystems (2019) 6:2 Page 10 of 13

considered when evaluating costs and benefits of new Attias N, Ferreira Siqueira M, de Godoy BH (2013) Acácias Australianas no
plantings. Brasil: Histórico, Formas de Uso e Potencial de Invasão. Biodiversidade
Bras 3(2):74–96
Abbreviations Awang K, Taylor D (1993) Acacia mangium, growing and utilization. In: FAO and
NFS: Nitrogen fixing species; POM: Particulate organic matter; SOM: Soil Winrock international, MPTS monograph series no. 3, Bangkok, Thailand
organic matter Bachega LR, Bouillet J-P, de Cássia Piccolo M, Saint-André L, Bouvet J-M,
Nouvellon Y, de Moraes Gonçalves JL, Robin A, Laclau J-P (2016)
Acknowledgements Decomposition of Eucalyptus grandis and Acacia mangium leaves and fine
We thank Dr. Kai Sonder (CIMMYT, Texcoco, Mexico), Dr. Claudia Maia roots in tropical conditions did not meet the home field advantage
(EMBRAPA Floresta, Colombo, Brazil) and Prof. Daniel Epron (Université de hypothesis. For Ecol Manag 359:33–43
Lorraine, France) for contributing material for this review, and Prof. Dan Bernhard-Reversat F (1993) Dynamics of litter and organic matter at the soil-litter
Binkley (Colorado State University, USA), Dr. Hugo Rainey (Wildlife interface of fast-growing tree plantations on sandy ferrallitic soils (Congo).
Conservation Society, USA) and Dr. Ilias Travlos (Agricultural University of Acta Ecol 14(2):179–195
Athens, Greece) for their inputs to an early version. Dr. Sarah Whitfeld Bini D, dos Santos CA, Bouillet J-P, de Morais Goncalves JL, Cardosoa EJBN
(Curator, Australian Tree Seed Centre (ATSC), National Research Collections (2013) Eucalyptus grandis and Acacia mangium in monoculture and
Australia, CSIRO) kindly provided data on dispatches of A. mangium seed intercropped plantations: evolution of soil and litter microbial and
from the ATSC. chemical attributes during early stages of plant development. Appl Soil
Ecol 63:57–66
Funding Bini D, Figueiredo AF, da Silva MCP, de Figueiredo Vasconcellos RL, Cardoso EJBN
DMR acknowledges funding from the DST-NRF Centre of Excellence for Inva- (2012) Microbial biomass and activity in litter during the initial development
sion Biology and the National Research Foundation, South Africa (grant of pure and mixed plantations of Eucalyptus grandis and Acacia mangium.
85417). Rev Bras Cienc Solo 37:76–85
Binkley D (1992) Mixtures of N2-fixing and non- N2-fixing tree species. In: Cannell
Availability of data and materials MGR, Malcom DC, Robertson PA (eds) The ecology of mixed species stands
Not applicable of trees. Blackwell Scientific Publications, Oxford
Bouillet J-P, Laclau JP, Gonçalves JLM, Voigtlaender M, Gava JL, Leite FP,
Authors’ contributions Hakamada R, Mareschal L, Mabiala A, Tardy F, Levillain J, Deleporte P, Epron
LSK planned the project, undertook most of the literature review, and wrote D, Nouvellon Y (2013) Eucalyptus and Acacia tree growth over entire rotation
the first draft. DMR contributed additional literature and contributed in single- and mixed-species plantations across five sites in Brazil and Congo.
substantially to interpretation and writing. Both authors read and approved For Ecol Manag 301:89–101
the final manuscript. Castro-Díez P, Godoy O, Saldaña A, Richardson DM (2011) Predicting invasiveness
of Australian Acacia species on the basis of their native climatic affinities, life-
Authors’ information history traits and human use. Divers Distrib 17:934–945
LSK is a soil scientist at the Forestry Research Centre (CRDPI), Pointe-Noire, Chaer GM, Resende AS, Campello EFC, de Faria SM, Boddey RM (2011) Nitrogen-
Congo. She works on soil organic matter (both C and N) and phosphorus dy- fixing legume tree species for the reclamation of severely degraded lands in
namics in the mixed-species of eucalypts and Acacia mangium plantations Brazil. Tree Physiol 31:139–149. https://doi.org/10.1093/treephys/tpq116
established in the Congolese coastal plains. Chazdon RL (2008) Beyond deforestation: restoring forests and ecosystem
DMR is Director of the DST-NRF Centre of Excellence for Invasion Biology services on degraded lands. Science 320:1458–1460
(http://academic.sun.ac.za/cib/) and Distinguished Professor of Ecology at Chen D, Zhang C, Wu J, Zhou L, Lin Y, Fu S (2011) Subtropical plantations are
Stellenbosch University, South Africa. His research focusses on the ecology large carbon sinks: evidence from two monoculture plantations in South
and management of invasive plants, especially trees and he has worked on China. Agric For Meteorol 151:1214–1225
many of the 23 species of Australian acacias known to be invasive in differ- Coetzee MPA, Wingfield BD, Golani GD, Tjahjono B, Gafur A, Wingfield MJ
ent parts of the world. (2011) A single dominant Ganoderma species is responsible for root rot
of Acacia mangium and Eucalyptus in Sumatra. South Forests 73(3–4):
Ethics approval and consent to participate 175–180
Not applicable Cole TG, Yost RS, Kablan R, Olsen T (1996) Growth potential of twelve Acacia
species on acid soils in Hawaii. For Ecol Manag 80:175–186
Consent for publication Dickie IA, Bennett BM, Burrows LE, Nuñez MA, Peltzer DA, Porté A, Richardson
Not applicable DM, Rejmánek M, Rundel PW, van Wilgen BW (2014) Conflicting values:
ecosystem services and invasive tree management. Biol Invasions 16:705–
Competing interests 719. https://doi.org/10.1007/s10530-013-0609-6
The authors declare that they have no competing interests. Donaldson JE, Hui C, Richardson DM, Robertson MP, Webber BL, Wilson JRU
(2014) Invasion trajectory of alien trees: the role of introduction pathway and
Author details planning history. Glob Change Biol. https://doi.org/10.1111/gcb.12486
1 Dubliez E, Freycon V, Marien JM, Peltier R, Harmand JM (2018) Long term impact
CRDPI, Centre de Recherche sur la Durabilité et la Productivité des
Plantations Industrielles, BP 1291 Pointe-Noire, Republic of the Congo. of Acacia auriculiformis woodlots growing in rotation with cassava and maize
2 on the carbon and nutrient contents of savannah sandy soils in the humid
Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch
University, Matieland 7602, South Africa. tropics (Democratic Republic of Congo). Agrofor Syst. https://doi.org/10.
1007/s10457-018-0222-x
Received: 27 August 2018 Accepted: 4 January 2019 Duponnois R, Baudoin E, Sanguin H, Thioulouse J, Le Roux C, Tournier E, Galiana
A, Prin Y, Dreyfus B (2013) L’introduction d’acacias australiens pour réhabiliter
des écosystèmes dégradés est-elle dépourvue de risques environnementaux
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