New and Emerging Insect Pest and Disease Threats to Forest Plantations in Vietnam

Abstract

The planted forest area in Vietnam increased from 3.0 to 4.4 million hectares in the period 2010–2020, but the loss of productivity from pests and diseases continues to be a problem. During this period, frequent and systematic plantation forest health surveys were conducted on 12 native and 4 exotic genera of trees as well as bamboo across eight forest geographic regions of Vietnam. Damage caused by insects and pathogens was quantified in the field and laboratory in Hanoi. The threats of greatest concern were from folivores (Antheraea frithi, Arthroschista hilaralis, Atteva fabriciella, Hieroglyphus tonkinensis, Lycaria westermanni,Krananda semihyalina, and Moduza procris), wood borers (Batocera lineolata, Euwallacea fornicatus, Tapinolachnus lacordairei, Xyleborus perforans, and Xystrocera festiva), sap-sucking insects (Aulacaspis tubercularis and Helopeltis theivora) and pathogens (Ceratocystis manginecans, Fusarium solani, and Phytophthora acaciivora). The number of new and emerging pests and pathogens increased over time from 2 in 2011 to 17 in 2020, as the damage became more widespread. To manage these pests and diseases, it is necessary to further invest in the selection and breeding of resistant genotypes, improve nursery hygiene and silvicultural operations, and adopt integrated pest management schemes. Consideration should be given to developing forest health monitoring protocols for forest reserves and other special-purpose forests.

Full text

Article
New and Emerging Insect Pest and Disease Threats to Forest
Plantations in Vietnam
Pham Quang Thu 1, *, Dao Ngoc Quang 1, Nguyen Minh Chi 1, Tran Xuan Hung 1, Le Van Binh 1
and Bernard Dell 1,2


Citation: Thu, P.Q.; Quang, D.N.;
Chi, N.M.; Hung, T.X.; Binh, L.V.;
Dell, B. New and Emerging Insect
Pest and Disease Threats to Forest
Plantations in Vietnam. Forests 2021,
12, 1301. https://doi.org/10.3390/
f12101301
Academic Editor: Manuela Branco
Received: 31 August 2021
Accepted: 21 September 2021
Published: 24 September 2021
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
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iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Forest Protection Research Centre, Vietnamese Academy of Forest Sciences, Duc Thang, Bac Tu Liem,
Hanoi 11910, Vietnam; daongocquang@vafs.gov.vn (D.N.Q.); nguyenminhchi@vafs.gov.vn (N.M.C.);
hung.tran@vafs.gov.vn (T.X.H.); levanbinh@vafs.gov.vn (L.V.B.); B.Dell@murdoch.edu.au (B.D.)
2Agriculture and Forest Sciences, Murdoch University, Perth 6150, Australia
*Correspondence: phamquangthu@vafs.gov.vn; Tel.: +84-913-066-586
Abstract:
The planted forest area in Vietnam increased from 3.0 to 4.4 million hectares in the period
2010–2020, but the loss of productivity from pests and diseases continues to be a problem. During
this period, frequent and systematic plantation forest health surveys were conducted on 12 native
and 4 exotic genera of trees as well as bamboo across eight forest geographic regions of Vietnam.
Damage caused by insects and pathogens was quantified in the field and laboratory in Hanoi. The
threats of greatest concern were from folivores (Antheraea frithi,Arthroschista hilaralis,Atteva fabriciella,
Hieroglyphus tonkinensis,Lycaria westermanni, Krananda semihyalina, and Moduza procris), wood borers
(Batocera lineolata,Euwallacea fornicatus,Tapinolachnus lacordairei,Xyleborus perforans, and Xystrocera
festiva), sap-sucking insects (Aulacaspis tubercularis and Helopeltis theivora) and pathogens (Ceratocystis
manginecans,Fusarium solani, and Phytophthora acaciivora). The number of new and emerging pests and
pathogens increased over time from 2 in 2011 to 17 in 2020, as the damage became more widespread.
To manage these pests and diseases, it is necessary to further invest in the selection and breeding
of resistant genotypes, improve nursery hygiene and silvicultural operations, and adopt integrated
pest management schemes. Consideration should be given to developing forest health monitoring
protocols for forest reserves and other special-purpose forests.
Keywords:
damage incidence; damage index; defoliation; forest health monitoring; forest protection;
production forests; root-rot; wood-borers
1. Introduction
Vietnam has made great strides in regreening the country in recent decades [
1
,
2
]. Due
to national policies and targets for afforestation and the rehabilitation of natural forests, the
forest area expanded from 9.40 million ha in 1990 to 14.67 million ha in 2020 [
3
]. Vietnam’s
2006–2020 Forest Development Strategy expressed the goal of increasing the total forest
cover from 37% in 2006 [
4
] to 42% by 2020 [
3
]. Forest development efforts of the past
10 years have greatly contributed to Vietnam’s sustainability strategy [
5
]. In particular,
the plantation forestry sector has made a significant contribution to the growth in forest
cover and now comprises 26.4% (ca. 4.4 million ha) of the total forest area in Vietnam [
3
].
About half of the forest plantations are managed by small stakeholders and the remainder
by private companies [
3
,
6
]. Therefore, the plantation forest sector is vitally important to
the livelihood of millions of rural households [
7
,
8
]. Exotic species, mainly acacias and
eucalypts, have been widely planted in Vietnam [
6
]. It has been estimated that fast-growing
Acacia hybrids can provide 33–56% of the total household income [
9
]. Furthermore, the
export of wood and forest products earned US$9.4 billion in 2018 [
6
] and increased to
US$12.3 billion in 2020 [
10
]. Even though the plantation area has continued to increase
over time, it is insufficient to meet the demand of the local wood processing industry [
11
].
Forests 2021,12, 1301. https://doi.org/10.3390/f12101301 https://www.mdpi.com/journal/forests

Forests 2021,12, 1301 2 of 20
Reducing losses from damage caused by insect pests and pathogens can help to secure the
future wood supply that Vietnam needs for its domestic and international markets.
Over time, the incidence of pest and disease problems in Acacia and Eucalyptus stands
has increased globally [
12
–
15
], including in Vietnam. Old et al. described 13 fungal
pathogens associated with Eucalyptus plantations in Vietnam [
16
,
17
]. The most common
Eucalyptus diseases were caused by Cryptosporiopsis eucalypti,Cylindrocladium reteaudii,
and Ralstonia solanacearum. Illustrations of the most common biotic problems (21 pests,
23 pathogens
) in Acacia,Eucalyptus, and Pinus plantations were provided in a field guide
for advisors and growers [
18
]. With the exception of native Pinus, most of the studies
on forest health in Vietnam have focused on exotic species, mainly Acacia and Eucalyp-
tus
[19,20]
. Currently, there are five major pest species (Ericeia sp., Helopeltis sp., Phalera
grotei, Pteroma plagiophleps, and Xylosandrus crassiusculus) and four major pathogens (Cerato-
cystis sp., Corticium salmonicolor,Phytophthora cinnamomi, and Pythium vexans) threatening
the productivity of Acacia plantations in Vietnam. Furthermore, six major pest species
(Aristobia testudo,A. approximator,Biston suppressaria,Leptocybe invasa,Sarothrocera lowi, and
Trabala vishnou) and five major pathogens (Cylindrocladium sp., Cryptosporiopsis eucalypti,
Ralstonia solanacearum,Teratosphaeria destructans, and T. zuluensis) have been damaging
Eucalyptus plantations. As the research effort on forest health in Vietnam has increased over
the past two decades, many reports focusing on individual pests or pathogens of interest
have been published [18,20–27].
However, new insect pests and pathogens continue to emerge and to cause damage in
plantation forests in Vietnam [
21
,
28
–
31
]. This is the first comprehensive study conducted
over a decade to quantify the diversity of new and emerging pests and pathogens and
the damage they cause to exotic and native planted species in Vietnam. The national
survey provides an opportunity to evaluate the extent of the new threats and to identify
management options.
2. Materials and Methods
2.1. Field Surveys—General Procedures
Forest health surveys were undertaken annually from 2011 to 2020, in the eight forest
geographic regions of Vietnam (Figure 1), with support from the Ministry of Agriculture
and Rural Development. Field observations were carried out on forests planted with
16 tree
species (Table 1). We relied on information gathered by local foresters as well as our own
observations to select the surveyed plantations in each studied forest region. Three fixed
plots (40
×
25 m) were randomly set up in plantations comprising the tree species present
in each region and they were assessed over ten years. Selected plots were at least
20 m
from plantation edges, roads, or forest gaps. About 25% of trees (at least 30 trees) in each
plot were randomly selected and assessed for damage from insect pests and/or pathogens.
Surveys usually involved three repeat visits a year undertaken in spring (February–April),
summer (May–July), and autumn (August–October). Where tree injury was observed (e.g.,
defoliation, leaf senescence, shoot dieback, tree death), we quantified the damage.
The damage was classified at five levels using methods described by [
27
,
32
], where:
0 = healthy trees
; 1 = low damage; 2 = medium damage; 3 = high damage; 4 = severe dam-
age. The damage incidence (p%) in each plot was calculated as follows:
p% = (n/N) ×100
,
where: n = the number of trees/culms attacked; N = total number of trees/culms assessed.
The average damage index (DI) was calculated as follows:
DI =
Σ4
0ni×vi
N
, where:
ni = the
number of trees infected at damage index i; vi = the damage index at level i; and
N = total number of plants assessed.
Values for p% and DI are reported in the results as ranges and are based on the plot
data over the years of plot assessment.

Forests 2021,12, 1301 3 of 20
Forests 2021, 12, x FOR PEER REVIEW 3 of 21
Figure 1. Map of Vietnam showing the eight forest geographic regions.
Table 1. Details of forest plantation species that were surveyed for pests and pathogens.
Host Area in 2020
(ha) Planting Region * Native/Exotic Commercial Use
Acacia spp. and hybrids 2,000,000 NE, NW, NP, NC, SC,
HC, SE, SW Exotic Paper, plywood, timber for
construction and furniture
Ailanthus triphysa 500 NE, NC, SC, SE Native Plywood
Chukrasia tabularis 35,000 NE, NW, NP, NC, SC,
HC Native Timber for furniture
Cinnamomum cassia 210,000 NE, NW, NC, SC Native Bark for export and seasoning, oil
for medicine
Dalbergia tonkinensis 2,000 NE, NW, NP, NC, SC,
HC, SE Native Timber for furniture and handcrafts
Figure 1. Map of Vietnam showing the eight forest geographic regions.
Table 1. Details of forest plantation species that were surveyed for pests and pathogens.
Host Area in 2020 (ha) Planting Region * Native/Exotic Commercial Use
Acacia spp. and hybrids
2,000,000 NE, NW, NP, NC, SC,
HC, SE, SW Exotic Paper, plywood, timber for
construction and furniture
Ailanthus triphysa 500 NE, NC, SC, SE Native Plywood
Chukrasia tabularis 35,000 NE, NW, NP, NC, SC,
HC Native Timber for furniture
Cinnamomum cassia 210,000 NE, NW, NC, SC Native Bark for export and seasoning, oil for
medicine
Dalbergia tonkinensis 2000 NE, NW, NP, NC, SC,
HC, SE Native Timber for furniture and handcrafts

Forests 2021,12, 1301 4 of 20
Table 1. Cont.
Host Area in 2020 (ha) Planting Region * Native/Exotic Commercial Use
Dendrocalamus barbatus 120,000 NE, NW, NP, NC Native
Culm for construction, activated
carbon, handcrafts and paper, young
shoots for food
Dendrocalamus latiflorus 15,000 NE, NW, NP, NC, SE Exotic
Young shoots for food, culm for paper
Dipterocarpus alatus 20,000 NC, SC, HC, SE Native Timber for furniture, construction
Eucalyptus spp. and
hybrids 400,000 NE, NW, NP, NC, SC,
HC, SE, SW Exotic Paper, plywood, timber for
construction
Fernandoa brilletii 6000 NE, NW, NC Native Timber for furniture
Hopea odorata 20,000 NC, SC, HC, SE Native Timber for furniture and boat
Illicium verum 42,000 NE, NW Native Fruit for export and seasoning, oil for
medicine
Melaleuca cajuputi 36,000 NE, NP, NC, SC, SW Native Paper, activated carbon, poles for
construction
Melaleuca leucadendra 32,000 SE, SW Exotic Paper, activated carbon, poles for
construction
Nauclea orientalis 500 SE, SW Native Plywood
Neolamarckia cadamba 1000 NE, NC, SE, SW Native Plywood
* Forest zones (see Figure 1): NE, North East; NW, North West; NP, North Plain; NC, North Central; SC, South Central; HC, Highland
Central; SE, South East; SW, South West.
2.2. Field Surveys—Insects
Insect survey methods included eye tracking, sweep netting, suction sampling, and
lure traps. Adult folivores were captured with collecting nets on aluminum poles, and
placed in killing jars. Plastic boxes (VietNhat Plastic Joint Stock Company, Hanoi, Vietnam)
with nylon mesh covers were employed to transport the living larvae, pupae, and eggs to
the laboratory. Fresh leaves were included for the larvae to feed.
For wood borers, samples were mostly obtained by the felling of affected trees, then
chopping logs to obtain collections. When adults were not present, logs 1.0–1.5 m in length
were transported to the laboratory in Hanoi. Some logs were dissected to capture the adults
and/or larvae. The cuts of other logs were sealed with Parafilm
®
(Bemis Company Inc.,
Neenah, WI, USA) and were taken to the laboratory for rearing adults for identification.
In addition, more intensive sampling was undertaken through trapping in the field for adult
ambrosia beetles. Black funnel Lindgren traps (BioQuip Products, Inc.,
Compton, CA, USA
)
and self-made plastic-bottle traps baited with 70% ethanol and para-menthenol (1S, 4R)-
p-menth-2-en-1-ol) (Synergy Semiochemicals Corp. (Burnaby, BC, Canada) were used to
attract adults. Propylene glycol (Merck, Darmstadt, Germany) and water (50:50) solution
was used in the collection cups. Each trap was suspended at least 10 m apart in a plantation
and 1.5 m above the ground to avoid damage by wild animals. The baits were replaced
once a week. Baiting was undertaken from April to June. Trap collections were stored in
70% ethanol in Eppendorf
®
(Eppendorf Manufacturing Corp., Hamburg, Germany) tubes
and then sorted in the laboratory.
2.3. Field Surveys—Pathogens
Samples (leaves, branches, and roots) were systematically taken from diseased trees.
Diseased boles were cut into 0.5–1.0 m length sections. Where the felling of trees was not
permitted, bark and wood samples were taken from the edge of lesions using a sharp knife.
Samples were placed in paper bags and transported to the laboratory in Hanoi.
2.4. Rearing Insects in the Laboratory
Larvae of folivores were reared in mesh cages (1
×
1
×
1.5 m in
length ×width ×height
)
at 25
±
2
◦
C and 75
±
5% relative humidity in the laboratory. Ten larvae were released in
each cage and observed daily to capture the adults when they emerged.
Logs containing larva of wood borers were placed in insect cages as above, and
the appearance of frass and adult emergence were recorded daily. For wood borers, an

Forests 2021,12, 1301 5 of 20
artificial diet was also used to feed the larvae following the method of [
33
,
34
] with modifi-
cation. Larvae were reared in 15–50 mL Falcon
®
tubes (Corning Life Sciences Company,
Corning, NY, USA
) on artificial media. The media for longhorn beetles contained 30 g agar,
40 g sucrose, 25 g yeast extract, 60 g oat powder, 4 g sodium benzoate, 2 g sorbic acid, 150 g
wood powder from the host tree, and 300 mL distilled water. The diet mixture for ambrosia
beetles contained 30 g agar, 5 g sucrose, 1.25 g Wesson’s salt mixture, 10 g casein, 200 g
sawdust from the host plant, and 500 mL distilled water. The rearing tubes were checked
daily to observe the development of larvae and pupae, and to collect adults.
2.5. Isolation and Culturing Pathogens
Three main procedures were used as follows. For the direct isolation method, plant
samples were prepared as above and either placed on selective PARPH-V8 (
pimaricin + am-
picillin + rifamycin + PCNB (C
6
Cl
15
NO
2
) + hymexazol + V8 juce + Agar) medium [
35
] and
incubated at 20
◦
C (for Oomycetes such as Phytophthora sp.), or placed on PDA (Potato
dextrose agar) medium supplemented with tetracycline and incubated at 26
◦
C (Fusarium
sp.). The carrot baiting method [
36
] was used to isolate Ceratocystis. Briefly, wood samples
(18–25 mm length, 1.0–1.5 mm thick) were sandwiched between two slices of fresh carrot
and placed on sterile dry paper in plastic boxes at 6
◦
C. After 5–8 days, the hat-shaped
spores of putative pathogens were placed on PDA medium and incubated at 26 ◦C.
When cultures had grown 1–2 cm in diameter, hyphal tips were sub-cultured onto
new media (V8 and PDA). Isolates cultured at 20
◦
C (Phytophthora sp.) and 26
◦
C (other
pathogens) were used for microscopy and DNA extraction.
2.6. Identification
Insect pests were mainly identified based on their morphology in taxonomic and
other works as follows: Lepidoptera—keys [
37
–
40
]; Coleoptera—keys [
41
–
44
]; Hemipt-
era—keys
[45,46]
; Orthoptera—keys [
47
]. Phylogenetic analyses using the cytochrome c
oxidase subunit I were undertaken to help confirm the identity of Batocera lineolata [
48
],
Euwallacea fornicatus [
31
], and Tapinolachnus lacordairei [
49
]. Protocols were performed as
described by [50–53].
For the plant pathogens, the ITS1/ITS4 [
54
] region was used to help identify Fusarium
solani [
55
], the
β
T1a/
β
T1b gene region [
56
] was used for Ceratocystis manginecans [
30
], and
in Phytophthora the primers DC6 [57] and ITS4 were used [58].
2.7. Specimens
The collected insect pests and plant pathogens associated with the investigated forest
plantation have been deposited in the collection of the Forest Protection Research Centre,
46 Duc Thang Street, Hanoi 11910, Vietnam and Vietnam National Museum of Nature,
18 Hoang Quoc Viet Street, Hanoi 11350, Vietnam.
3. Results
3.1. Change over Time
Forest health surveys undertaken from 2011 to 2020 on the plantations of different
tree species in Table 1revealed 14 new or emerging insect pest species and major disease
threats from two plant pathogens (Table 2). The total number of new or emerging insect
pest species and pathogens increased from 2 in 2011 to 17 in 2020 (Figure 2). Hence, on
average, 1–2 new pests per year were recorded damaging forest plantations in Vietnam.
The temporal and geographical occurrence of the observed pests and pathogens is detailed
in Table 3. Of particular note is the apparently rapid spread of Aulacapsis tubercularis
in Cinnamomum cassia,Euwallacea fornicatus in Acacia spp. and C. cassia,Tapinolachrus
lacordairea in Chukrasia tabularis, and Xyleborus perforans in Acacia and Eucalyptus. The
two main types of damage from insect pest species are from foliar feeding by folivores
(5 species of Lepidoptera), and bark and/or wood feeding (6 species of Coleoptera). The

Forests 2021,12, 1301 6 of 20
fungal pathogen Ceratocystis manginecans has extended its host range from exotic Acacia
and Eucalyptus to the native Dalbergia tonkinensis and C. tabularis.
Table 2. Pests and pathogens recorded in forest health surveys in Vietnam causing significant damage to host trees.
Group Species Tree Species Damaged Part
Pests
Coleoptera
Batocera lineolata Eucalyptus hybrids Boles
Euwallacea fornicatus
Acacia auriculiformis
Acacia mangium
Acacia hybrids
Cinnamomum cassia
Boles
Lycaria westermanni Fernandoa brilletii Leaves
Tapinolachnus lacordairei Chukrasia tabularis Boles
Xyleborus perforans Acacia hybrids
Eucalyptus urophylla Boles
Xystrocera festiva Acacia mangium Boles
Hemiptera Aulacaspis tubercularis Cinnamomum cassia Leaves
Helopeltis theivora
Acacia auriculiformis
Acacia mangium
Acacia hybrids
Cinnamomum cassia
Melaleuca cajuputi
Melaleuca leucadendra
Young leaves, shoots
Lepidoptera Antheraea frithi Dipterocarpus alatus
Hopea odorata Leaves
Arthroschista hilaralis Neolamarckia cadamba
Nauclea orientalis Leaves
Atteva fabriciella Ailanthus triphysa Young leaves, shoots
Krananda semihyalina Cinnamomum cassia Leaves
Moduza procris Neolamarckia cadamba
Nauclea orientalis Leaves
Orthoptera Hieroglyphus tonkinensis Dendrocalamus barbatus
Dendrocalamus latiflorus Young leaves
Pathogens
Fungi Ceratocystis manginecans
Acacia auriculiformis
Acacia mangium
Acacia hybrids
Chukrasia tabularis
Dalbergia tonkinensis
Eucalyptus camaldulensis
Eucalyptus urophylla
Boles
Fusarium solani Dendrocalamus latiflorus Shoots, roots
Oomycete Phytophthora acaciivora Acacia mangium
Acacia hybrids Roots and dieback of seedlings
Table 3.
Temporal and geographical occurrence of pest and pathogen species in forest health surveys in Vietnam from 2011
to 2020.
Organism 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Pest
Antheraea frithi SE SE, SW SE, SW SE, SW
Arthroschista
hilaralis SW SW SW SW SW SW
Atteva fabriciella NE NE NE NE NE
Aulacaspis
tubercularis SW SW, SC SW, SC,
NE, NP
SW, SC,
NE, NP
SW, SC,
NE, NP
SW, SC,
NE, NP
Batocera lineolata NW NE, NW

Forests 2021,12, 1301 7 of 20
Table 3. Cont.
Organism 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Euwallacea
fornicatus
NE, SC,
HC
NE, SC,
HC
NE, SC,
HC
NE, NW,
NC, SC,
SE, HC
NE, NW,
NC, SC,
SE, HC
NE, NW,
NC, SC,
SE, HC
NE, NW,
NC, SC,
SE, SW,
HC
NE, NW,
NC, SC,
SE, SW,
HC
Helopeltis theivora
NC, NW,
NE, HC,
SE, SW
Hieroglyphus
tonkinensis
NW,
NE, NC
NW,
NE, NC
NW,
NE, NC
NW,
NE, NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
Krananda
semihyalina NE, NP
Lycaria
westermanni NC NC, NE,
NW
NC, NE,
NW
Moduza procris SW SW SW SW SW SW
Tapinolachnus
lacordairei NW NE, NW,
NC
Xyleborus perforans
NE NE, SE,
SW
Xystrocera festiva HC HC HC HC, SC HC, SC HC, SC HC, SC HC, SC
Pathogen
Ceratocystis
manginecans
NE,
NW,
NC
NE,
NW,
NC
NE,
NW,
NC
NE,
NW,
NC, SE
NE, NW,
NP, NC,
SE, SW
NE, NW,
NP, NC,
SC, SE,
SW
NE, NW,
NP, NC,
SC, HC,
SE, SW
NE, NW,
NP, NC,
SC, HC,
SE, SW
NE, NW,
NP, NC,
SC, HC,
SE, SW
NE, NW,
NP, NC,
SC, HC,
SE, SW
Fusarium solani NE NE
Phytophthora
acaciivora NE NE NE NE NE NE NE NE
Note: NE. North East; NW. North West; NP. North Plain; NC. North Central; SC. South Central; HC. Highland Central; SE. South East; SW.
South West.
Forests 2021, 12, x FOR PEER REVIEW 7 of 21
Acacia hybrids
Figure 2. Change in the number of pest and pathogen species recorded each year.
Table 3. Temporal and geographical occurrence of pest and pathogen species in forest health surveys in Vietnam from
2011 to 2020.
Organism 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Pest
Antheraea frithi SE SE, SW SE, SW SE, SW
Arthroschista hilaralis SW SW SW SW SW SW
Atteva fabriciella NE NE NE NE NE
Aulacaspis tubercularis SW SW, SC
SW, SC, NE,
NP
SW, SC, NE,
NP
SW, SC, NE,
NP
SW, SC, NE,
NP
Batocera lineolata NW NE, NW
Euwallacea fornicatus
NE, SC,
HC
NE, SC,
HC
NE, SC,
HC
NE, NW,
NC, SC,
SE, HC
NE, NW,
NC, SC, SE,
HC
NE, NW,
NC, SC, SE,
HC
NE, NW,
NC, SC, SE,
SW, HC
NE, NW, NC,
SC, SE, SW,
HC
Helopeltis theivora
NC, NW, NE,
HC, SE, SW
Hieroglyphus tonkinensis NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC
NW, NE,
NC NW, NE, NC NW, NE, NC NW, NE, NC
Krananda semihyalina NE, NP
Lycaria westermanni NC NC, NE, NW NC, NE, NW
Moduza procris SW SW SW SW SW SW
Tapinolachnus lacordairei NW NE, NW, NC
Xyleborus perforans NE NE, SE, SW
Xystrocera festiva HC HC HC HC, SC HC, SC HC, SC HC, SC HC, SC
Pathogen
Ceratocystis manginecans NE, NW,
NC
NE, NW,
NC
NE, NW,
NC
NE, NW,
NC, SE
NE, NW,
NP, NC,
SE, SW
NE, NW,
NP, NC,
SC, SE, SW
NE, NW,
NP, NC, SC,
HC, SE, SW
NE, NW,
NP, NC, SC,
HC, SE, SW
NE, NW,
NP, NC, SC,
HC, SE, SW
NE, NW, NP,
NC, SC, HC,
SE, SW
Fusarium solani NE NE
Phytophthora acaciivora NE NE NE NE NE NE NE NE
Note: NE. North East; NW. North West; NP. North Plain; NC. North Central; SC. South Central; HC. Highland Central;
SE. South East; SW. South West.
3.2. Defoliation from Folivores
3.2.1. Antheraea frithi (Saturniidae) Wild Tasar Silkmoth (Vietnamese: Sau Tam)
This species was first recorded in southern Vietnam in 1970 [59], but it only recently
has become a pest of D. alatus and H. odorata plantations. Affected plantations are from 5
to 15 years old, with p% of 82–97%, and DI of 2.9–3.6. Single tree deaths can occur with
11
33
6789
12
14
11
22
2
2
2
2
3
3
0
2
4
6
8
10
12
14
16
18
2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Number of pests and pathogens recorded
Year of observation
Pathogens
Pests
Figure 2. Change in the number of pest and pathogen species recorded each year.
3.2. Defoliation from Folivores
3.2.1. Antheraea frithi (Saturniidae) Wild Tasar Silkmoth (Vietnamese: Sau Tam)
This species was first recorded in southern Vietnam in 1970 [
59
], but it only recently
has become a pest of D. alatus and H. odorata plantations. Affected plantations are from 5 to
15 years old, with p% of 82–97%, and DI of 2.9–3.6. Single tree deaths can occur with repeat
defoliation (Figure 3a). Adults (Figure 3f) spread quickly and there is high risk of further

Forests 2021,12, 1301 8 of 20
damage [
60
]. Control using living Beauveria bassiana and Metarhizium anisopliae has been
attempted by local authorities, but the effectiveness is low.
Forests 2021, 12, x FOR PEER REVIEW 8 of 21
repeat defoliation (Figure 3a). Adults (Figure 3f) spread quickly and there is high risk of
further damage [60]. Control using living Beauveria bassiana and Metarhizium anisopliae has
been attempted by local authorities, but the effectiveness is low.
Figure 3. Emerging Lepidoptera threats to forest plantations in Vietnam. (a–e) damaged to trees from folivores; (f–j) adults.
(a,f) Antheraea frithi damage in Dipterocarpus alatus; (b,g) Arthroschista hilaralis damage in Neolamarckia cadamba; (c,h) Atteva
fabriciella damage in Ailanthus triphysa; (d,j) Krananda semihyalina damages in Cinnamomum cassia; (e,l) Moduza procris dam-
age in Nauclea orientalis. Scale bar: f = 3.0 cm; g = 1.5 cm; h = 0.5 cm; i = 1.8 cm; j = 2.0 cm.
3.2.2. Arthroschista hilaralis (Crambidae) Kadam Defoliator Moth (Vietnamese: Sau Cuon
La Xanh Ngoc)
This pest (Figure 3g) was recorded in 2015 in the South West region (Figure 1) where
it defoliated 15 ha of Neolamarckia cadamba and 20 ha of Nauclea orientalis plantations [61].
So far, more than 90 ha of plantations have been attacked. Young plantations (2 to 5 year-
old) are most at risk of damage (Figure 3b) and defoliation occurs 2 to 3 times a year. p%
is 75–99%, and DI is 2.6–3.8. Repeat damage of the new emerging foliage reduces tree
growth and may cause tree mortality.
However, two Ne. cadamba provenances (Ca Mau and Dong Thap) and two Na.
orientalis provenances (Dong Thap and Binh Phuoc) showed good recovery after
defoliation [62]. The two host species are also attacked by Moduza procris (Figure 3j).
3.2.3. Atteva fabriciella (Attevidae) Ailanthus Webworm Moth (Vietnamese: Sau An La
Vang Hoa Trang)
This pest was recorded in 2016 in 10 ha of Ailanthus triphysa in the North East region.
Foliage and shoot tips (Figure 3c) are attacked 2–3 times a year. Young plantations (2–5
years old) are severely affected; p% is 100%, DI is 2.6–2.8, and some tree death occurs.
Insecticides (abamectin and chlorpyrifos ethyl) have been applied by local authorities
with 85–90% effectiveness. The pest (Figure 3h) spreads quickly and has the potential to
cause wide damage [63].
3.2.4. Krananda semihyalina (Geometridae) Cinnamon Looper (Vietnamese: Sau Do Canh
Nua Trong)
This pest (Figure 3i) was recorded in 2020 in the North East and North Plain regions
damaging about 5 ha of Cinnamomum cassia plantations, aged 3–10 years. The foliage is
Figure 3.
Emerging Lepidoptera threats to forest plantations in Vietnam. (
a
–
e
) damaged to trees from folivores; (
f
–
j
) adults.
(
a
,
f
)Antheraea frithi damage in Dipterocarpus alatus; (
b
,
g
)Arthroschista hilaralis damage in Neolamarckia cadamba; (
c
,
h
)Atteva
fabriciella damage in Ailanthus triphysa; (
d
,
j
)Krananda semihyalina damages in Cinnamomum cassia; (
e
,
l
)Moduza procris damage
in Nauclea orientalis. Scale bar: f= 3.0 cm; g= 1.5 cm; h= 0.5 cm; i= 1.8 cm; j= 2.0 cm.
3.2.2. Arthroschista hilaralis (Crambidae) Kadam Defoliator Moth (Vietnamese: Sau Cuon
La Xanh Ngoc)
This pest (Figure 3g) was recorded in 2015 in the South West region (Figure 1) where it
defoliated 15 ha of Neolamarckia cadamba and 20 ha of Nauclea orientalis plantations [
61
]. So
far, more than 90 ha of plantations have been attacked. Young plantations (2 to 5 year-old)
are most at risk of damage (Figure 3b) and defoliation occurs 2 to 3 times a year. p% is
75–99%, and DI is 2.6–3.8. Repeat damage of the new emerging foliage reduces tree growth
and may cause tree mortality.
However, two Ne. cadamba provenances (Ca Mau and Dong Thap) and two Na. orien-
talis provenances (Dong Thap and Binh Phuoc) showed good recovery after defoliation [
62
].
The two host species are also attacked by Moduza procris (Figure 3j).
3.2.3. Atteva fabriciella (Attevidae) Ailanthus Webworm Moth (Vietnamese: Sau An La
Vang Hoa Trang)
This pest was recorded in 2016 in 10 ha of Ailanthus triphysa in the North East re-
gion. Foliage and shoot tips (Figure 3c) are attacked 2–3 times a year. Young plantations
(
2–5 years
old) are severely affected; p% is 100%, DI is 2.6–2.8, and some tree death occurs.
Insecticides (abamectin and chlorpyrifos ethyl) have been applied by local authorities with
85–90% effectiveness. The pest (Figure 3h) spreads quickly and has the potential to cause
wide damage [63].
3.2.4. Krananda semihyalina (Geometridae) Cinnamon Looper (Vietnamese: Sau Do Canh
Nua Trong)
This pest (Figure 3i) was recorded in 2020 in the North East and North Plain regions
damaging about 5 ha of Cinnamomum cassia plantations, aged 3–10 years. The foliage is
devoured 4–5 times a year and this greatly reduces tree growth. p% is 26–90% (Figure 3d),
DI is 0.7–3.5, and tree deaths have been reported.

Forests 2021,12, 1301 9 of 20
3.2.5. Moduza procris (Crambidae) Commander Butterfly (Vietnamese: Sau Gai An La)
Moduza procris (Figure 3j) was recorded in the North Central region in 1970 [
64
], and
its status as a forest pest was established in 2015 due to foliar damage to 1–5 year-old
Neolamarckia cadamba and Nauclea orientalis plantations in Ca Mau province [
62
]. p% is
3–7% (Ne. cadamba) and 31–58% (Na. orientalis) (Figure 3e), and DI is 0.1–0.2 (Ne. cadamba)
and 1.1–2.0 (Na. orientalis). Moduza procris and Arthroschista hilaralis are reported to cause
concurrent damage in Ne. cadamba and Na. orientalis plantations.
3.3. Damage from Wood Borers
3.3.1. Batocera lineolata (Cerambycidae) Striped Longhorn Beetle (Vietnamese: Xen Toc Den
Soc Trang)
This pest (Figure 4m) was recorded in 2019 in the North West damaging 30 ha of
clonal Eucalyptus plantations. Larvae feed in the sapwood. Some severely damaged
trees (
Figure 4g
) are so weakened that they are easily broken by strong winds, while
others remain standing and die (Figure 4a). Tree decline and death are most prevalent in
1–3 year-old plantations. Resistance has been observed in some clones of E. urophylla ×E.
pellita and E. urophylla [
48
,
65
]. A number of insecticides are being evaluated for control
in the field [
48
]. So far, about 350 ha of Eucalyptus hybrid plantations have been seriously
damaged. p% is 24–52% and DI is 0.8–1.6.
Forests 2021, 12, x FOR PEER REVIEW 10 of 21
Figure 4. Wood borer and beetle damage to forest plantations in Vietnam. (a–f) damaged trees; (g–l) close-up of damage
symtoms; (m–s) adults. (a,g,m) Batocera lineolata damage in Eucalyptus hybrid; (b,h,o) Euwallacea fornicatus damages in
Acacia hybrid; (c,i,p) Lycaria westermanni damage in Fernandoa brilletii; (d,j,q) Tapinolachnus lacordairei damage in Chukrasia
tabularis; (e,k,r) Xyleborus perforans damage in Eucalyptus urophylla; (f,l,s) Xystrocera festiva damage in Acacia mangium. Scare
bar: m = 1.5 cm, o = 1.0 mm; p,q,s = 1.0 cm; r = 1.2 mm.
3.3.2. Euwallacea fornicatus (Curculionidae) Polyphagous Shot Hole Borer (Vietnamese:
Mot Nuoi Nam Forni)
This species was recorded in Tonkin Island (Vietnam) in 1992 [66]. In 2013 it was
recorded in Acacia hybrid plantations in the North West, North Central, South Central,
and Highland Central regions [31]. By 2016, E. fornicatus (Figure 4o) had spread into Acacia
auriculiformis, A. mangium and Acacia hybrid (Figure 4b) plantations across seven forest
zones [21]. Three-year-old stands are especially vulnerable with p% of 29–33%, DI of 0.31–
0.45, and 2–5% mortality. Trees from 1.5 to 15 years old have been attacked in some loca-
tions. The gallery system is created (Figure 4h) to lay eggs in broods leads to the degrada-
tion of wood quality. In addition, the beetle-transported fungus Fusarium euwallaceae
[21,67] causes the wood to become discolored and decay.
3.3.3. Lycaria westermanni (Chrysomelidae) Leaf Beetle (Vietnamese: Bo Canh Cung An
La)
This species was recorded in Vietnam in 1981 [68]. In 2018, L. westermanni (Figure 4p)
was recorded damaging 18 ha of Fernandoa brilletii plantations in the North Central region.
Figure 4.
Wood borer and beetle damage to forest plantations in Vietnam. (
a
–
f
) damaged trees; (
g
–
l
) close-up of damage
symtoms; (
m
–
s
) adults. (
a
,
g
,
m
)Batocera lineolata damage in Eucalyptus hybrid; (
b
,
h
,
o
)Euwallacea fornicatus damages in
Acacia hybrid; (
c
,
i
,
p
)Lycaria westermanni damage in Fernandoa brilletii; (
d
,
j
,
q
)Tapinolachnus lacordairei damage in Chukrasia
tabularis; (
e
,
k
,
r
)Xyleborus perforans damage in Eucalyptus urophylla; (
f
,
l
,
s
)Xystrocera festiva damage in Acacia mangium. Scare
bar: m= 1.5 cm, o= 1.0 mm; p,q,s= 1.0 cm; r= 1.2 mm.

Forests 2021,12, 1301 10 of 20
3.3.2. Euwallacea fornicatus (Curculionidae) Polyphagous Shot Hole Borer (Vietnamese: Mot
Nuoi Nam Forni)
This species was recorded in Tonkin Island (Vietnam) in 1992 [
66
]. In 2013 it was
recorded in Acacia hybrid plantations in the North West, North Central, South Central, and
Highland Central regions [
31
]. By 2016, E. fornicatus (Figure 4o) had spread into Acacia
auriculiformis,A. mangium and Acacia hybrid (Figure 4b) plantations across seven forest
zones [
21
]. Three-year-old stands are especially vulnerable with p% of 29–33%, DI of 0.31–0.45,
and 2–5% mortality. Trees from 1.5 to 15 years old have been attacked in some locations.
The gallery system is created (Figure 4h) to lay eggs in broods leads to the degradation
of wood quality. In addition, the beetle-transported fungus Fusarium euwallaceae [
21
,
67
]
causes the wood to become discolored and decay.
3.3.3. Lycaria westermanni (Chrysomelidae) Leaf Beetle (Vietnamese: Bo Canh Cung An La)
This species was recorded in Vietnam in 1981 [
68
]. In 2018, L. westermanni (Figure 4p)
was recorded damaging 18 ha of Fernandoa brilletii plantations in the North Central region.
By 2020, over 50 ha of F. brilletii plantations had been damaged across three forest zones.
The foliage of 1–10 year-old trees can be completely consumed (Figure 4c). p% is 45–68%,
DI is 1.4–2.3, and some mortality has been reported [69].
3.3.4. Tapinolachnus lacordairei (Cerambycidae) Brown Longhorn Beetle (Vietnamese: Xen
Toc Nau Den)
This species was recorded in the North West in 1933 [
70
]. In 2019 this pest (
Figure 4q
)
was recorded damaging 34 ha of Chukrasia tabularis plantations (5–15 year-old) in North
West [
49
]. The boles of attacked trees have numerous exit holes (Figure 4j). Damage
from larvae feeding in the wood can lead to tree senescence and death (Figure 4d). p% is
13–23%
, and DI is 0.3–0.6. By 2020, hundreds of hectares of C. tabularis plantations had
been damaged as this pest can spread quickly. Cross-vane traps with ethanol have been
used, with low effectiveness, to trap adults in C. tabularis plantations.
3.3.5. Xyleborus perforans (Curculionidae) Island Pinhole Borer (Vietnamese: Mot Nuoi
Nam Perfor)
The species was recorded in Tonkin Island in Vietnam in 1992 [
66
]. In 2019 this pest
was recorded damaging 155 ha of Eucalyptus urophylla plantations in the North East [71].
Compartments from 6-months-old to 3-year-old are vulnerable with p% of 26–32% and
DI of 0.42–0.54. Xyleborus perforans (Figure 4r) create galleries (Figure 4k) that extend from
the bark to the heartwood and this reduces tree growth and wood quality. More recently, X.
perforans was reported in Acacia hybrid plantations in the South East (Dong Nai province)
and South West (Ca Mau province). So far, the damage is low in Acacia plantations (p% is
7–10%, DI 0.1–0.3), but this pest is a threat to the future development of Acacia plantations
in Vietnam.
3.3.6. Xystrocera festiva (Cerambycidae) Stem Borer (Vietnam: Xen Toc Canh Xanh)
The pest (Figure 4s) was reported in 2013 damaging 3 ha of Acacia mangium plantations
in the Highland Central region [
72
]. It has now spread to the South Central region. The
borer causes tree decline (Figure 4f) and death. Trees of all diameters of trees are attacked,
and infestation increases with stand age. p% is 12–46%, and DI is 0.3–1.5.
3.4. Other Sap-Sucking Damage
3.4.1. Aulacaspis tubercularis (Diaspididae) White Mango Scale (Vietnamese: Rep
Xoai Trang)
The pest was reported damaging Mangifera indica plantations in the North East region
in 2008 [
73
]. In 2015 A. tubercularis (Figure 5g) was observed damaging 5 ha of Cinnamomum
cassia plantations in the South West region.

Forests 2021,12, 1301 11 of 20
Forests 2021, 12, x FOR PEER REVIEW 12 of 21
Figure 5. Sap-sucking insect damage to forest plantations in Vietnam. (a–c) damaged trees and bam-
boo; (d–f) larvae; (g–i) adults. (a,d,g) Aulacaspis tubercularis damage in Cinnamomum cassia; (b,e,h)
Helopeltis theivora damage in C. cassia; (c,f,i) Hieroglyphus tonkinensis damage in Dendrocalamus bar-
batus. Scare bar: g = 0.2 cm; h = 0.5 cm; i = 1.0 cm.
It has now spread to C. cassia plantations in two further regions. The sap-sucking
scale poses a severe threat to nursery stock and 1–5-year-old plantations (Figure 5a,d). p%
Figure 5.
Sap-sucking insect damage to forest plantations in Vietnam. (
a
–
c
) damaged trees and
bamboo; (
d
–
f
) larvae; (
g
–
i
) adults. (
a
,
d
,
g
)Aulacaspis tubercularis damage in Cinnamomum cassia;
(
b
,
e
,
h
)Helopeltis theivora damage in C. cassia; (
c
,
f
,
i
)Hieroglyphus tonkinensis damage in Dendrocalamus
barbatus. Scare bar: g= 0.2 cm; h= 0.5 cm; i= 1.0 cm.
It has now spread to C. cassia plantations in two further regions. The sap-sucking scale
poses a severe threat to nursery stock and 1–5-year-old plantations (Figure 5a,d). p% and
DI are 9–31% and 0.1–1.0 in nurseries, and 15–41% and 0.2–1.3 in plantations, respectively.

Forests 2021,12, 1301 12 of 20
3.4.2. Helopeltis theivora (Miridae) Tea Mosquito Bug (Vietnamese: Bo Xit Muoi Mau Xanh)
This pest was reported in 2010 in the North Central region causing damage to Acacia
hybrid (7 ha), Acacia mangium (15 ha), Cinnamomum cassia (8 ha), Melaleuca cajuputi (2 ha)
and M. leucadendra (2 ha) [
18
]. It has now spread over much of Vietnam. Nursery stock
(cuttings and hedge trees) is particularly vulnerable to attack. Nymphs (Figure 5e) and
adults (Figure 5h) feed on new shoots and young leaves (Figure 5b). Damage appears
initially as a lesion or area of necrosis around the feeding site and progresses to wilt,
dieback and shoot death [74]. p% is 13–79%, and DI is 0.2–2.2.
3.4.3. Hieroglyphus tonkinensis (Acrididae) Grasshopper (Vietnamese: Chau Chau Mia
Chay Xanh)
This species was recorded in 1912 in the North Plain [
47
]. In 1976 it was reported
to occur in the North West, North East, and North Centre regions [
75
]. Later records
include the North Central region in 2003 [
76
] and 2008 [
77
], and the North East region
in 2020 [
78
]. Since 2011, the pest has damaged 80–150 ha of Dendrocalamus barbatus and
D. latiflorus plantations in the North West and North East, with p% of 22–63% and DI
of 0.3–1.8 (Figure 5c). A periodic survey was conducted by local officers to detect the
occurrence of nymphs and adults (Figure 5i). When outbreaks occurred, the insecticides
cypermethrin + chlorpyrifos
, abamectin, and emamectin benzoate have been applied by
local authorities to reduce the impact of the pest.
3.5. Damage from Pathogens
3.5.1. Ceratocystis manginecans (Ceratocystidaceae) Ceratocystis Wilt Disease (Vietnamese:
Benh Chet Heo)
The pathogen was recorded in 2011 in Acacia hybrid and A. mangium plantations in
the North East, North West, and North Central regions. Over time, it has spread to A. auri-
culiformis (Figure 6a), Eucalyptus camaldulensis,E. urophylla (Figure 6d), Chukrasia tabularis,
and Dalbergia tonkinensis plantations in the eight forest geographic regions (
Figure 1
) in
Vietnam. Damage is most severe in the North West and North Central zones. Diseased
trees typically have wilted foliage and stem cankers with sap exudate. Wood beneath the
lesioned areas become blue or gray and then turn grey-brown [
29
,
30
,
79
–
81
]. Ceratocystis
manginecans causes severe wilt disease in 1–3 year-old Acacia hybrid (Figure 6b) and A.
mangium (Figure 6c) plantations. p% and DI are 15–25% and 0.4–0.9, respectively. Trees
can die 3–6 months after infection [
79
,
81
]. Some fungicides (carbendazim, mancozeb, and
metalaxyl) and biological agents (Trichoderma spp., Bacillus spp.) have been used in exper-
iments to try and control C. manginecans [
82
]. Pruning in the dry season and decreasing
bark tearing during pruning can reduce the levels of infection and disease [
28
]. There is
evidence of resistance to C. manginecans in some clonal Acacia [
83
,
84
] and in some families
of C. tabularis [29].
Forests 2021, 12, x FOR PEER REVIEW 14 of 21
Figure 6. Pathogens damaging forest plantations and nurseries in Vietnam. (a–d) Ceratocystis man-
ginecans wilt disease; (a) Acacia auriculiformis; (b) Acacia hybrid; (c) A. mangium; (d) Eucalyptus
urophylla; (e) Shoot rot in Dendrocalamus latiflorus caused by Fusarium solani; (f) Decline in Acacia
hybrid mother plants caused by Phytophthora acaciivora.
3.5.2. Fusarium solani (Nectriaceae) Fusarium Rot Disease (Vietnamese: Benh Thoi Mang)
Fusarium solani was recorded in 1999 on lychee trees in the North East and on coffee
plants in the Highland Central [85]. Later, this species was mainly found on agricultural
hosts such as pepper, citrus, and peanut. In 2020, this species was recorded damaging 700
ha of Dendrocalamus latiflorus plantations in the North East (Yen Bai province) [55]. The
pathogen causes greyish brown lesions surrounded by dark brown margins on the outer
protective sheath of the shoot (Figure 6e). The lesions spread quickly to the inner sheaths
causing rot and a strong odor. This disease appears mainly during the humid season (July
to October), when young shoots are harvested for food. p% of rot disease is 16–20% and
DI is 0.2–0.3.
3.5.3. Phytophthora acaciivora (Peronosporaceae) Phytophthora Disease (Vietnamese: Benh
Thoi Re)
This pathogen was first collected in 2013 in an Acacia mangium nursery in the North
East [58]. In recent years P. acaciivora has been reported causing damage to Acacia hybrid
and A. mangium nurseries in the same region. Infested seedlings, cuttings, and mother tree
banks become wilted (Figure 6f) and then die from root rot. The fungicide potassium
phosphonate is being used by local people to reduce P. acaciivora damage in forest
Figure 6. Cont.

Forests 2021,12, 1301 13 of 20
Forests 2021, 12, x FOR PEER REVIEW 14 of 21
Figure 6. Pathogens damaging forest plantations and nurseries in Vietnam. (a–d) Ceratocystis man-
ginecans wilt disease; (a) Acacia auriculiformis; (b) Acacia hybrid; (c) A. mangium; (d) Eucalyptus
urophylla; (e) Shoot rot in Dendrocalamus latiflorus caused by Fusarium solani; (f) Decline in Acacia
hybrid mother plants caused by Phytophthora acaciivora.
3.5.2. Fusarium solani (Nectriaceae) Fusarium Rot Disease (Vietnamese: Benh Thoi Mang)
Fusarium solani was recorded in 1999 on lychee trees in the North East and on coffee
plants in the Highland Central [85]. Later, this species was mainly found on agricultural
hosts such as pepper, citrus, and peanut. In 2020, this species was recorded damaging 700
ha of Dendrocalamus latiflorus plantations in the North East (Yen Bai province) [55]. The
pathogen causes greyish brown lesions surrounded by dark brown margins on the outer
protective sheath of the shoot (Figure 6e). The lesions spread quickly to the inner sheaths
causing rot and a strong odor. This disease appears mainly during the humid season (July
to October), when young shoots are harvested for food. p% of rot disease is 16–20% and
DI is 0.2–0.3.
3.5.3. Phytophthora acaciivora (Peronosporaceae) Phytophthora Disease (Vietnamese: Benh
Thoi Re)
This pathogen was first collected in 2013 in an Acacia mangium nursery in the North
East [58]. In recent years P. acaciivora has been reported causing damage to Acacia hybrid
and A. mangium nurseries in the same region. Infested seedlings, cuttings, and mother tree
banks become wilted (Figure 6f) and then die from root rot. The fungicide potassium
phosphonate is being used by local people to reduce P. acaciivora damage in forest
Figure 6.
Pathogens damaging forest plantations and nurseries in Vietnam. (
a
–
d
)Ceratocystis
manginecans wilt disease; (
a
)Acacia auriculiformis; (
b
)Acacia hybrid; (
c
)A. mangium; (
d
)Eucalyptus
urophylla; (
e
) Shoot rot in Dendrocalamus latiflorus caused by Fusarium solani; (
f
) Decline in Acacia
hybrid mother plants caused by Phytophthora acaciivora.
3.5.2. Fusarium solani (Nectriaceae) Fusarium Rot Disease (Vietnamese: Benh Thoi Mang)
Fusarium solani was recorded in 1999 on lychee trees in the North East and on coffee
plants in the Highland Central [
85
]. Later, this species was mainly found on agricultural
hosts such as pepper, citrus, and peanut. In 2020, this species was recorded damaging
700 ha of Dendrocalamus latiflorus plantations in the North East (Yen Bai province) [
55
]. The
pathogen causes greyish brown lesions surrounded by dark brown margins on the outer
protective sheath of the shoot (Figure 6e). The lesions spread quickly to the inner sheaths
causing rot and a strong odor. This disease appears mainly during the humid season (July
to October), when young shoots are harvested for food. p% of rot disease is 16–20% and DI
is 0.2–0.3.
3.5.3. Phytophthora acaciivora (Peronosporaceae) Phytophthora Disease (Vietnamese: Benh
Thoi Re)
This pathogen was first collected in 2013 in an Acacia mangium nursery in the North
East [
58
]. In recent years P. acaciivora has been reported causing damage to Acacia hybrid
and A. mangium nurseries in the same region. Infested seedlings, cuttings, and mother
tree banks become wilted (Figure 6f) and then die from root rot. The fungicide potassium
phosphonate is being used by local people to reduce P. acaciivora damage in forest nurseries.
p% and DI in nurseries are 25–30% and 0.6–1.1, respectively. The mortality rate is 18–21%.
There is concern that the pathogen poses a high risk to young Acacia plantations in some
geographic regions.
4. Discussion
This is the first comprehensive study of new and emerging insect pest and pathogen
threats to plantation forests in Vietnam. It comprised 10 years of field surveys monitoring
the health of 12 native and 8 exotic plantation species. The surveillance was undertaken
across all the eight geographic forest regions of Vietnam and was representative of the
493,000 ha of native and the 2,447,000 ha of exotic tree species and hybrids in plantations.
Overall, 14 species of insects and 3 species of plant pathogens were recognized as either
new or emerging threats to the forestry sector. It is worrying that the number of pests
increased from 1 in 2011 to 14 in 2020, and the trajectory indicates that further outbreaks
are likely to occur. In addition, the field surveys have shown that the range of some pests,
notably Aulacaspis tubercularis and Euwallacea fornicatus, has rapidly expanded. Of the three
plant pathogens that were classified as threats, Ceratocystis manginecans is of the greatest
concern due to its increase in geographical range and spread from Acacia and Eucalyptus to
the native Chukrasia tabularis and Dalbergia tonkinensis.

Forests 2021,12, 1301 14 of 20
Apart from Ceratocystis manginecans, which has a wide distribution across South
and Southeast Asia [
86
,
87
], and Batocera lineolata, which is a pest in forest plantations in
southern China [
52
], probably all the species of concern are native in Indo-China. Some of
the insect pests have broader natural geographical ranges in Asia [
59
,
88
], and some have
become invasive alien species. Some wood borers and bark beetles have been distributed
around the world, such as B. lineolata in India [
89
] and Europe [
90
], Euwallacea fornicatus in
Indonesia [
51
] and the USA [
31
], and Tapinolachnus lacordairei in Indochina and Borneo [
70
].
Recent research has clarified the species boundaries for the E. fornicatus complex [
91
] and
highlighted the roles of the Fusarium symbiont in determining host tree susceptibility [
92
].
Some of the new plantation forest pests in Vietnam are well-known damaging agri-
cultural and horticultural crops. For example, the white mango scale Aulacaspis tuber-
cularis causes global damage to fruit trees [
93
], and Helopeltis theivora damages cacao in
Malaysia [
94
] and Camellia sinensis plantations in India [
95
]. In Vietnam, Hieroglyphus
tonkinensis was recorded damaging field crops in Hoa Binh Province in 1976 [
75
], Thanh
Hoa Province in 2003 [
76
], Yen Bai Province in 2020 [
78
], and Phu Tho Province in 2008 [
77
].
Fusarium solani was documented in roots of lychees in 1999 in Bac Giang Province and on
coffee in Dak Lak Province [
85
]. Regarding the pathogens, Ceratocystis manginecans was first
described in mango in Oman and Pakistan [
96
]. Since then, it has become very invasive in
Acacia plantations across Southeast Asia [
86
,
87
] and its host range now includes Dalbergia
tonkinensis [
30
] and Chukrasia tabularis [
29
]. High mortality in Acacia plantations in Sumatra
led to their replacement with Eucalyptus pellita [
97
]. In the past, much attention had been
placed on Phytophthora species causing damage to field and horticultural tree crops [
98
]. It
is only recently that studies have been undertaken in conservation and production forests
in Vietnam [99,100].
There is a high diversity of forest tree species in Vietnam and almost nothing is
known about the diversity and severity of pests and pathogens and their impact in natural
and secondary forests. Many tree species deserve consideration for domestication and
plantation production [
101
]. Furthermore, there is an additional 1,458,000 ha of plantation
forests that were not included in this study. The nearly 300,000 ha of pine plantations
(Pinus massoniana,P. merkusii,P. kesya) have been well-studied in the past and damage
from pests and pathogens is well known [
18
,
19
,
22
], so they were excluded from MARD’s
priority lists of plantation species for forest health research. The remaining 1,158,000 ha
includes mangroves, other bamboo species, small monocultures of other native species,
and some mixed forests. At present, there is no national strategy to investigate the health
of these forests even though tree mortality has been observed [
102
,
103
]. These planted
forests in Vietnam have potential pests and diseases, some of which may become invasive
and damage new production forests in the future. From 2021–2030, Vietnam has a target to
plant an additional 4000–6000 ha of native trees each year [
5
]. Therefore, increased funding
is needed for forest health monitoring for the whole forest estate in Vietnam.
To manage invasive pests and diseases, it is necessary to further invest in the selection
and breeding of resistant hosts. So far, the effort to identify resistant genotypes has been
limited. Some Acacia clones [
83
,
84
] and families of Chukrasia tabularis [
29
] have shown
resistance to Ceratocystis maginecans; several provenances of Neolamarckia cadamba and
Nauclea orientalis were resistant to Arthroschista hilaralis and Moduza procris [
62
]; Five Acacia
hybrid clones were resistant to Euwallacea fornicatus [
104
]; and three Eucalyptus hybrid
clones had high resistance to Batocera lineolata [
48
]. Hundreds of other new varieties have
been selected only on their growth attributes [
105
]. As a priority, future tree breeding
programs in Vietnam should embrace the main biotic threats in their objectives.
A number of studies have recommended improvements to nursery hygiene [
27
,
106
].
At present, many small forest nurseries are using unpasteurized soil or growing plants
on the ground, and there is a high risk that nurseries may be sources of pathogens such
as Phytophthora [
58
]. Silvicultural measures such as improved pruning techniques [
28
],
limiting damage to roots, stems and branches [
28
,
106
,
107
], and diversification of the tree
species composition of plantations [
108
] are opportunities to limit invasions of pests and

Forests 2021,12, 1301 15 of 20
diseases. Integrated pest management (IPM) has been successfully implemented for some
pest species [109–111]. Although IPM has been applied to manage some pests in Vietnam
such as Dasychira auxutha and Dendrolimus punctatus in Pinus spp. [
112
], Biston suppressaria
and Krananda semihyalina in Cinnamomum cassia [
113
], and Ceratocystis manginecans in Acacia
spp. [
114
], the field is in its infancy in forestry in Vietnam compared to IPM for horticultural
tree crops [115].
The observed increase in plantation forest damage from new pests and pathogens
in Vietnam parallels observations from around the world. These events are impacting
livelihoods, economic development, and biodiversity [
116
]. The increase in invasive insect
pests and pathogens in North America and Europe is concurrent with climate change and
globalization [
117
,
118
]. The huge expansion in global trade and changes in trade routes
have increased the risk of accidental introduction of pests and pathogens.
The policy of plant protection and quarantine in Vietnam includes import quarantine,
resistant varieties, cultivation techniques, pest monitoring, and priority deployment of
biological agents [
119
]. Recently, a technical support project was employed by FAO to set
up a strategy framework and national plan for integrated pest management [120].
5. Conclusions
Extensive monitoring of forest plantations over a decade across Vietnam has revealed
dynamic temporal changes in biotic threats to tree health. To guard against future commer-
cial loss in the forest economy, steps need to be taken now to minimize future impacts of
pests and disease. This requires improving nursery hygiene, adopting silvicultural prac-
tices that reduce physical damage to trees, selecting resistant genotypes, and strengthening
national biosecurity and quarantine. However, the latter is difficult to achieve given the
long land and sea borders in Vietnam. Early detection is critical [
121
], and for Vietnam, this
necessitates developing forest health monitoring protocols for the extensive forest reserves
in protection—special-purpose as well as urban forests. This will require the use of sentinel
plantings [122] and remote sensing to detect trees under stress.
Author Contributions:
These authors contributed equally to this work; Conceptualization, P.Q.T.
and B.D.; investigation and sampling, P.Q.T., L.V.B., D.N.Q., N.M.C. and T.X.H.; rearing and isolation,
D.N.Q., N.M.C., L.V.B. and T.X.H.; identification, P.Q.T. and B.D.; analysis, D.N.Q., T.X.H., and
N.M.C.; methodology, D.N.Q., N.M.C., L.V.B. and T.X.H.; validation, P.Q.T. and B.D.; visualization,
P.Q.T. and B.D.; writing—original draft, P.Q.T. and N.M.C.; writing—review and editing, P.Q.T. and
B.D. All authors have read and agreed to the published version of the manuscript.
Funding:
The research was funded by the Ministry of Agriculture and Rural Development of
Vietnam, projects “Forest health surveillance in Vietnam, phase I, code: 505/BVTV”, “Forest health
surveillance in Vietnam, phase II, code: 148/QÐ-BNN-KH”, “Study on integrated management for
insect pests in Cinnamomum cassia in Northern region and Quang Nam province, Vietnam, code:
03/HÐ-ÐTKHCN”, “Study on integrated pest management of major leave insects and stem borer
beetles in Acacia hybrid, A. mangium and A. auriculiformis in Vietnam, code: 04/HÐ-ÐTKHCN”,
and “Breeding and planting method development of Chukrasia tabularis for high productivity and
tolerance of shoot-tip borer in Vietnam, code: 3710/QÐ-BNN-KHCN”.
Acknowledgments:
We thank our colleagues for their support in collecting samples and data, and
Gondess Pty Ltd. for travel support to B.D. and covering publication costs.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design
of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or
in the decision to publish the results.
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