Biological Control 148 (2020) 104303

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Biological Control
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Natural mortality of invasive fall armyworm, Spodoptera frugiperda (J. E. T

Smith) (Lepidoptera: Noctuidae) in maize agroecosystems of northeast India
⁎,1
D.M. Firake , G.T. Behere
Division of Crop Protection, ICAR (Indian Council of Agricultural Research) – Research Complex for NEH Region, Umiam, Meghalaya 793103, India

A R T I C LE I N FO A B S T R A C T

Keywords: Invasive fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is a pest of
Metarhizium rileyi American origin that has recently invaded Asian countries, including India. After causing huge losses in the
SpfrNPV Africa and Asia, the FAW is now affecting large areas of India. Indigenous natural enemies of related pest species
Chelonus are the first defense against invasive pests and understanding their role in population suppression of invasive
Microplitis
pests is a first step towards the development of a comprehensive management program. Therefore, we studied
Hexamermis
Generalist predators
the natural enemy complex responsible for natural mortality of FAW in northeast India. Various locations were
Entomopathogens surveyed across five major districts of Meghalaya state, where more than 26 species of natural enemies were
Diversity indices found attacking FAW. A total of 56.6% to 73.1% of larvae were found to be either parasitized or infected with
naturally occurring entomopathogens. Species richness and diversity of predators were determined in maize
fields at different locations. Values of Menhinick's species richness index (DMn) varied from 0.23 to 0.31 and
Shannon-Wiener index (H) ranged from 2.16 to 2.6 across various locations. The Simpson Index (D) indicated
high predator diversity in maize fields. The entomopathogenic fungus, Metarhizium rileyi (Farlow) Samson and
the baculovirus, SpfrNPV were observed to be the dominant mortality factors throughout the season, responsible
for > 50% mortality of FAW larvae. This investigation demonstrated that indigenous natural enemies of related
noctuid species can widen their host range and successfully adopt the invasive FAW as a novel host/prey in
invaded regions. Therefore, conservation of such biocontrol agents could be vital for mitigating FAW damage in
maize agroecosystems.

1. Introduction zone between the Indian, Indo-Burma-Malaysian and Indo-Chinese re-

Native to the tropical and subtropical region of America, the fall
armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera:
Noctuidae), is now widespread across the globe (CABI, 2020). The FAW
is a most destructive crop pest, known to attack more than 353 plant
species across the globe (Montezano et al., 2018; CABI, 2020). In Asia,
the FAW detected for the first time during 2018 infesting maize crop in
Karnataka state of India (Ganiger et al., 2018) and it spread quickly to
many Indian states (Singh, 2019), including northeast (NE) India
(Firake et al., 2019). Concurrently, FAW spread rapidly into China,
Bangladesh, Indonesia, Japan, Korea, Republic of Laos, Malaysia,
Myanmar, Nepal, Sri Lanka, Thailand, Vietnam and Yemen (CABI,
2020). In NE India, this devastating pest appeared in outbreak numbers
during March-May 2019 in Mizoram, Tripura, Nagaland, Meghalaya,
Manipur, Sikkim and Arunachal Pradesh states (Firake et al., 2019).
The NE region of India is a biodiversity hotspot and a transition
gions. It is ecologically represented by the Eastern Himalayan biome
and is exceptionally rich in endemic flora and fauna. This region is
being promoted by the Indian government for organic farming because
of its distinct climatic and geographic conditions, high insect diversity,
and traditional practices of native farmers who use fewer synthetic
agrochemicals (Anonymous, 2015). Invasion of an alien pest species
poses a big challenge because it may force the use of chemical pesti-
cides. Maize is the second most important cereal crop in northeast
India, next to rice, and is mostly grown by small land holding organic
farmers in rainfed hilly upland conditions (Ansari et al., 2015). FAW
establishment will wreck havoc for such farmers.
Native natural enemies of related existing pest species are the first
defense against invasive pest species. Assessing the natural mortality
caused by native natural enemies is one of the first steps in developing a
comprehensive management program for an invasive insect pest.
Establishment of an invasive species outside its natural range represents

⁎
Corresponding author.
E-mail address: dnyaneshwar.firake@icar.gov.in (D.M. Firake).
1
0000-0002-3353-5728.

https://doi.org/10.1016/j.biocontrol.2020.104303
Received 14 January 2020; Received in revised form 9 May 2020; Accepted 11 May 2020
Available online 18 May 2020
1049-9644/ © 2020 Elsevier Inc. All rights reserved.
D.M. Firake and G.T. Behere
a major threat to ecological balance (Molnar et al., 2008). Invasive pest
species may also be free of natural enemies that normally suppress them
in their native range (Dunn, 2009; Kelly et al., 2009; Poulin et al.,
2011). Conversely, if they do enter along with enemies of their native
range, these may have an adverse effect on the ecology of native ene-
mies in newly invaded areas (Poulin, 2017). Thus, studies on native
natural enemies in newly invaded areas are warranted. Several reports
demonstrated that native biocontrol agents of other closely related pest
species usually widen their host range and play a significant role in the
natural regulation of invasive pests (Vercher et al., 2005; Matošević and
Melika, 2013). Therefore, the information on key mortality factors is
imperative to understand the establishment potential of FAW in the
invaded areas and nearby geographical locations.
FAW is attacked by over 150 parasitoid species (Ashley, 1979;
Molina-Ochoa et al., 2003) and by diverse taxa of insect predators
(Braman et al., 2002; Fuller et al., 1997; Perfecto, 1991; Van Huis,
1981; Wyckhuys and O’Nei, 2006; Harrison et al., 2019). Recently,
Sisay et al. (2018) recorded five parasitoid species causing up to 50%
parasitism of FAW in Jimma, Ethiopia. Similarly, seven parasitoid
species and three entomopathogens were reported attacking FAW in
Coahuila, México (Ríos-Velasco et al., 2011). Despite a huge diversity,
the occurrence and distribution of natural enemies varies among ha-
bitats. Factors including geographical location, agricultural practices,
and insecticide use can also affect the occurrence of natural control
agents that could potentially impact FAW populations (Fargues and
Rodríguez-Rueda, 1980; Sosa-Gomez & Moscardi, 1994; Vänninen,
1996; Miętkiewicz et al., 1998). Therefore, the natural enemy complex
associated with FAW varies among localities (Ashley, 1979; Van Huis,
1981; Perfecto, 1991; Fuller et al., 1997; Braman et al., 2002; Molina-
Ochoa et al., 2003; Wyckhuys and O’Nei, 2006; Harrison et al., 2019).
As it is a newly invasive pest, very limited information is available
on natural enemies of FAW in Asia. There is a good possibility that
native biocontrol agents of other Spodoptera species may accept S.
frugiperda as a novel host/prey. Key mortality factors of FAW are best
studied in newly invaded areas while the alien pest initially occurs in
high densities. This information would also be helpful to adjoining
countries similarly affected by the FAW. This study sampled the natural
enemy complex of FAW in Meghalaya State of northeast India and as-
sessed their respective contributions to natural mortality.
2. Materials and methods
2.1. Study location
The study was carried out in the Biological Control Laboratory at
the Division of Crop Protection, ICAR Research Complex for NEH
Region, Umiam, Meghalaya, during the year 2019–20. The institute is
situated at Umiam (Barapani), 25°41′- 21″ north latitude and 91°55′-
25″ east longitude having an elevation of 1010 m above msl.
2.2. Survey for natural enemies
In Meghalaya state, maize is mostly grown during pre-kharif and
kharif season (March to September) as a rainfed crop. The initial survey
was conducted during maize growing period at 34 different locations
representing five major districts (viz., East Jaintia Hills, West Khasi
Hills, East Khasi Hills, West Jaintia Hills and Ri Bhoi) to know the status
of fall armyworm in Meghalaya state (Supplementary Table 1). Among
these locations, ten representative localities were selected for further
studies on natural enemies of FAW (Fig. 1). In addition to maize, other
host plants of FAW in the nearby fields were also observed for their
presence.
2.3. Assessment of parasitism
To determine levels of natural parasitism, different life stages of
2
Biological Control 148 (2020) 104303
FAW were collected from maize fields at ten selected localities. FAW life
stages (egg masses, larvae and pupae) were collected monthly from
maize plants in five randomly selected maize fields at each location. In
each field, FAW samples were collected from the randomly selected
50 m2 plots at two spots during the evening. Egg masses present on
plant parts were detached carefully, placed inside polythene bags, and
brought to the laboratory where they were held separately in rearing
containers (Dimension: 72 × 72 × 100 mm, Shape: Square, Material:
Polystyrene, Hole position: 3 sides, Ventilation hole size: 40 mm, Mesh
pore : 0.053 μm, Make: Hi-Media®, India) until the emergence of
parasitoids or FAW larvae. Feeding injury in the leaf whorl and the
presence of fresh frass were used to locate FAW larvae. FAW caterpillars
(L2-L4 instar) were collected from the whorl or unopened leaves of
maize and placed individually into the sterilized plastic containers
(Dimensions: 70 × 60 mm, Type: Vial, Material of construction: PP/
HDPE, Make: Tarsons®, India) for further development. Larvae were
provisioned daily with fresh leaves of maize collected from the fields at
the entomology farm. These were surface-sterilized with an aqueous
solution of sodium hypochlorite (0.05%) followed by rinsing with dis-
tilled water). All specimens were held in the biocontrol laboratory (at
25 ± 1 °C, 75 ± 5% RH, and 12:12 (L:D) photoperiod until com-
pletion of development or mortality due to biocontrol agents. The
containers were cleaned or replaced as needed to maintain sanitary
conditions. FAW pupae were collected from the soil surface (2 to 10 cm
depth) adjacent to FAW-infested maize plants (without larvae) and
pupae were isolated in rearing containers (Dimensions: 70 × 60 mm,
Type: Vial, Material of construction: PP/HDPE, Make: Tarsons®, India)
for completion of development or emergence of parasitoids.
Parasitoids emerging from different life stages of FAW were pre-
served individually in 70% alcohol (Storage Vial, Size: 10 ml, Material
of construction: PP/HDPE, Make: Tarsons®, India). The identity of the
parasitoids was confirmed by expert taxonomists (Dr. Rajmohana K.,
Scientist D, Zoological Survey of India, Kolkata and Dr. Ranjith A.P.,
Research Scholar, Department of Zoology, University of Calicut, India)
and with the help of identified specimens in our repository. In the case
of two species of parasitoids (Chelonus sp. and Metopius sp.), the mi-
tochondrial DNA of two individuals of each was extracted and se-
quenced at the 5′ region of the COI gene following the procedure
adopted for rose sawfly by Firake et al. (2013). Identities were con-
firmed by comparing with unpublished sequences for the same region
available in our own DNA barcoding database. Accession numbers of
two confirmed parasitoid specimens were submitted to the NCBI data-
base. The representative specimens were preserved in the insect re-
pository at ICAR-NEH, Umiam. In the case of mermithid nematodes, the
newly emerged L-4 post parasitic juveniles (pre-adults) were kept in
moist soil until their final molt. After 1.5 to 2 months, the adult ne-
matode specimens were preserved in 70% alcohol and further processed
for identification in the Animal Parasitology Section of the Institute,
based on published keys and consultation with an expert (Dr Gulcan
Tarla, Assistant Professor, Department of Plant Protection, Uşak Uni-
versity, Turkey).
Diseased FAW larvae were isolated in sterile containers
(Dimensions: 70 × 60 mm, Type: Vial, Material of construction: PP/
HDPE, Make: Tarsons®, India) until mycosis or sporulation and then
preserved in a refrigerator. The entompathogens were identified based
on taxonomic characters viewed under a phase contrast microscope
(Ignoffo, 1981; Álvarez et al., 2018). Virus-infected insects, identifiable
by their overt symptoms, were isolated in sterile containers (Dimen-
sions: 70 × 60 mm, Type: Vial, Material of construction: PP/HDPE,
Make: Tarsons®, India) and the larval discharge was observed under
phase contrast microscope for presence of inclusion/occlusion bodies.
Bacteria from infected larvae (symptomatically) were cultured and the
spores were observed under microscope for identification. Per cent
parasitism was calculated based on the number of parasitized larvae/
pupae from the total number of FAW larvae collected from the field.
D.M. Firake and G.T. Behere Biological Control 148 (2020) 104303

Table 1
Collection details of FAW life stages from maize agroecosystems at different locations in Meghalaya.
SN Locality & district Number of life stages of FAW collected in different months Total

April May June July August

E L P E L P E L P E L P E L P E L P

1 Umiam (RB) 1 139 1 1 148 2 1 129 1 2 091 1 1 042 0 6 549 5

2 Mawnohsynrum (RB) 0 093 0 1 103 0 1 081 1 1 039 1 1 033 0 4 349 2
3 Margnar (RB) 0 101 1 1 132 0 1 099 1 1 053 0 1 028 1 4 413 3
4 Umshorshor (RB) 0 111 0 0 089 1 1 101 0 0 029 1 1 037 1 2 367 3
5 Larnai (WJH) 2 097 1 1 133 2 1 145 1 1 098 0 1 071 0 6 544 4
6 Khainduli (WJH) 1 141 2 2 203 1 2 153 1 1 101 0 0 034 0 6 632 4
7 Lad-Rymbai (EJH) 0 072 0 1 109 0 0 083 1 1 022 0 1 019 0 3 305 1
8 Nongplit (EJH) 0 108 0 0 133 0 1 101 1 1 079 1 0 034 1 2 455 3
9 Lawbyrtun (EKH) 0 093 1 0 141 0 1 115 0 0 094 0 1 049 0 2 492 1
10 Nongstoin (WKH) 0 042 1 0 106 1 1 112 1 1 084 0 1 038 0 3 382 3
TOTAL 4 997 7 7 1297 7 10 1119 8 9 690 4 8 385 3 38 4488 29

Note: E: Egg mass (es); L: Larvae; P: Pupa (e); RB: Ri Bhoi; WJH: West Jaintia Hills; EJH: East Jaintia Hills; EKH: East Khasi Hills; WKH: West Khasi Hills.

2.4. Identification of FAW predators
Numbers of predators were recorded based on visual counts on
randomly-selected plants in five randomly selected maize fields at each
location sampled monthly. Three 25 m2 plots were sampled in each
field during evening hours. Feeding injury in the leaf whorl and the
presence of fresh frass were used to locate FAW larvae. The predators
present on different plant parts were counted. FAW predation was
confirmed based on direct observation of predation on different life
stages of FAW under field conditions. Predators were collected in the
field and brought to the laboratory and held under standardized con-
ditions (25 ± 1 °C, 75 ± 5% RH, and 12:12 (L:D) photoperiod. To
verify pest consumption, second to fourth instar FAW larvae were of-
fered as prey. Representative specimens of each predator species were

Fig. 1. Selected locations in Meghalaya (India) to study the natural parasitism of FAW and diversity of predators in Maize fields (Map Courtsey: Google Earth Pro
7.3.2.5776).

3
D.M. Firake and G.T. Behere
collected and preserved for taxonomic identification. Taxonomic iden-
tities were confirmed using the existing database at the Insect
Biosystematic Laboratory, Umiam and were also verified by expert
taxonomists (Dr. H. V. Ghate, Retired Professor, Department of
Zoology, Modern College of Arts, Science & Commerce, Pune (India)
verified the specimens of predatory bugs and beetles; Dr. A. K. Bodkhe
Associate Professor, Department of Zoology, J. D. P. S. Mahavidyalaya,
Amaravti (India) identified the spider specimens and Dr. Yoshitaka
Kakimura, Department of Biology Keio University, Japan was consulted
over email for the identification of the earwig specimens). Voucher
specimens were preserved in the Insect Museum of the Institute.
Species richness was determined using Menhinick’s diversity index
(DMn) (Whittaker, 1977). Heterogeneity measures were determined
which combine both richness and evenness components of diversity.
The most widely used diversity index in the ecological literature is the
Shannon-Wiener diversity index (Shannon and Weaver, 1949; Pielou,
1975), whereas the Simpson Index is the most widely used measure of
evenness (Simpson, 1949). The indices were determined using the fol-
lowing formulae:
Menhinick’s diversity index (DMn):
S
DMn =
N
where ‘N’ = the total number of individuals in the sample and S = the
number of species recorded.
Shannon-Wiener diversity index (H):
H= ∑ pilnpi
where, ‘pi’ is the proportion of individuals found in the ith species. ‘ln’ is
the natural log, ‘Σ’ is the sum of the calculations, and ‘s’ is the number
of species.
Simpson Index (D):
1 (Dermaptera: Forficulidae) (Plate 4C) and the paper wasp, Ropalidia
D=
∑ pi2
where ‘p’ is the proportion (n/N) of individuals of one particular species
found (n) divided by the total number of individuals found (N); ‘ln’ is
the natural log, ‘Σ’ is the sum of the calculations and ‘S’ is the number of
species. Higher values of Simpson Index (D) indicate greater diversity.
2.5. Statistical analysis
Data on larval mortality (%) were subjected to angular transfor-
mation and analyzed by one-way ANOVA after they passed Levene’s
test for homogeneity of variances. Means were separated by Tukey's
HSD test (α = 0.05). These analyses were carried out using SPSS v. 21.0
software for MS Windows (IBM Corp. Released, 2012).
3. Results
A total of 38 egg masses, 4488 larvae (L2- L4), and 29 pupae of FAW
were collected from ten locations across five districts of Meghalaya
during April to August 2019 (Table 1, Fig. 1). A total of 56.6% to 73.1%
of larvae were found to be either parasitized or infected with naturally
occurring entomopathogens. Over 60% mortality of FAW larvae was
recorded across the majority of localities, but it was significantly higher
(F9, 36 = 2.99, P < 0.05) at Umshorshor and Lad Rymbai localities
than at others (Fig. 2). A total of eight species of parasitoids were found
parasitizing FAW life stages in Meghalaya (Table 2, Plate 1). The
identity of two parasitoids, Chelonus formosanus Sonan (Hymenoptera:
Braconidae) and Metopius rufus Ashmead (Hymenoptera: Ichneumo-
nidae) was confirmed by molecular analysis and representative se-
quences have been deposited in the NCBI with accession numbers
‘MN640596′ and ‘MN640597′, respectively. The egg/larval parasitoid
C. formosanus appeared to be the most abundant parasitoid species.
4
Biological Control 148 (2020) 104303
However, differences in FAW parasitism across temporal and spatial
scales were not significant (Figs. 3, 4). The platygastrid parasitoid
Telenomus remus Nixon emerged from two egg masses of FAW collected
during late August from maize fields at Umiam. The mermithid para-
site, Hexamermis cf. albicans (Siebold) (Mermithida: Mermithidae) was
also recovered from FAW larvae (Table 2). Interestingly three juvenile
mermithids emerged from a single FAW pupa (Plate 2). Although
mermithid parasitism did not vary across locations, it was considerably
higher from April to June than on other sampling dates (F4, 36 = 5.33,
P < 0.05).
Five entomopathogens were recovered from dead FAW larvae and
pupae (Table 3). Metarhizium rileyi (Farlow) Samson was the most
abundant species throughout the season, (Figs. 3, 4), being significantly
more frequent (F9, 36 = 2.67, P < 0.05) in larvae collected from the
Lad Rymbai and Umshorshor localities. Spodoptera frugiperda nuclear
polyhedrosis virus (SpfrNPV) was also found infecting FAW larvae,
being more frequently observed during April and May (F4, 36 = 3.54,
P < 0.05), but without significant differences among locations. All
larval instars of FAW were observed to be susceptible to infection by M.
rileyi and SpfrNPV (Plate 3A, B). Microscopic observations revealed
mycelial growth and spores of M. rileyi on infected FAW larvae
(Plate 3C), whereas inclusion bodies of SpfrNPV were clearly observed
in larval discharge under phase contrast microscopy (Plate 3D).
Twelve species of predators were found attacking different stages of
FAW (Table 4, Plate 4). Species diversity indices indicated a high di-
versity of predators in the maize agroecosystems of Meghalaya
(Table 5). The Simpson Index was highest at Mawnohsynrum and
Khainduli localities (Table 5). A pentatomid predator, Eocanthecona
furcellata Wolff (Plate 4A), was the most commonly observed species,
whereas other species, Andrallus spinidens (Fabricius) (Hemiptera:
Pentatomidae), Cosmolestes sp. (Hemiptera: Reduviidae) (Plate 4B) and
Podisus maculiventris (Say) (Hemiptera: Pentatomidae) were found only
occasionally feeding on FAW larvae at various locations. Earwigs
brevita Das & Gupta (Hymenoptera: Vespidae), were commonly found in
maize whorls attacking different stages of FAW. Predatory spiders re-
presenting four genera, Rhene (Arenae: Salticidae), Oxyopes (Arenae:
Oxyopidae), Marpissa (Arenae: Salticidae) and Lycosa (Arenae: Lyco-
sidae) were also observed preying on FAW larvae. The spiders Oxyopes
birmanicus Thorell (Arenae: Oxyopidae) (Plate 4D), was the most fre-
quently encountered spider species and Rhene flavicomans Simon
(Arenae: Salticidae) (Plate 4E), was another spider commonly found
feeding on FAW larvae.
Three species of coccinellids, Harmonia dimidiata (Fabricius),
Menochilus sexmaculatus (Fabricius), and Coelophora bissellata Mulsant
were often seen foraging inside maize whorls and another four species,
Cryptogonus quadriguttatus (Weise), Micraspsis spp., Oenopia kirby
Mulsant and Oenopia sexareata (Mulsant) were found on maize plants in
FAW infested fields. However, actual predation of these species on FAW
life stages was not directly observed.
Altogether, we recorded over 26 species of natural enemies at-
tacking FAW. Among them, 10 species represent first records of para-
sitism/predation on FAW in Asia. These were C. formosanus, Microplitis
manilae Ashmead (Hymenoptera: Braconidae), Netelia sp.
(Hymenoptera: Ichneumonidae), Ichneumon promissorius (Erichson)
(Hymenoptera: Ichneumonidae), Hexamermis cf. albicans, Ropalidia
brevita, Polistes cf. olivaceus (De Geer) (Hymenoptera: Vespidae),
Cosmolestes sp., Rhene flavicomans and Oxyopes birmanicus.
4. Discussion
We have recorded over 26 species of natural enemies of FAW in
Meghalaya. The braconid wasp, C. formosanus was the primary para-
sitoid of FAW, whereas M. rileyi and SpfrNPV were the dominant
naturally-occurring entomopathogens. The majority of these natural
enemies have been reported attacking other noctuid pests in India,
D.M. Firake and G.T. Behere
Fig. 2. Percent mortality ( ± SE) of FAW attributed to biocontrol agents seasonally at different locations in Meghalaya. Mean values bearing the same letters are not
significantly different (Tukey’s HSD, α = 0.05).
including S. litura (Ranga Rao et al., 1993; Singh, 1994; Sharma et al.,
2002; CABI, 2018; Firake et al., 2019). Chelonus formosanus is native to
the Oriental region (Singh, 1994) and reported to parasitize FAW in
Barbados and Trinidad (Alam, 1979; Yaseen, 1979). This species is an
egg/larval parasitoid of both S. litura and S. exigua in India (Rao, 1972).
We observed that developing larvae of C. formosanus take about 15 days
to form cocoons on nearby plant surfaces. Females of Chelonus spp.,
including C. formosanus, are highly fecund and usually parasitize >
70% of eggs in each host egg mass they encounter (Rao, 1972;
Choudhari et al., 1983; Swamiappan and Balasubramanian, 1990). The
relatively low parasitism of FAW in this study may reflect infection by
entomopathogens (M. rileyi or SpfrNPV) or intraguild predation by
predators. Larval koinobiont parasitoids often emerge onto plant sur-
faces where they can be attacked by generalist predators prior to, or
after, forming cocoons.
The parasitoid wasp, M. manilae is known to parasitize larvae of
many Spodoptera species in many countries (Gupta, 2013). Worldwide,
parasitoids belonging to genera ‘Netelia’ and ‘Ichneumon’ are also known
to parasitize FAW (Molina-Ochoa et al., 2003). Metopius rufus is a
larval/pupal parasitoid of S. litura and Mythimna separata (Walker) in
India (Sharma et al., 2002; CABI, 2018). This is evidence that native
parasitoids of related noctuid pests can successfully adopt the invasive
FAW as a novel host in invaded regions. In this study, the role of egg
parasitoid, T. remus was limited and only evident at the end of the
August. Considering the performance of T. remus as a biocontrol agent
against FAW in other parts of the world (Kenis et al., 2019; Liao et al.,
2019), further studies are needed to assess its potential against FAW in
northeast India.
The mermithid genus Hexamermis has worldwide distribution and
they have been recorded emerging from lepidopterans in various parts
of the world (Kaiser, 1991). Infective juveniles of several species of
Table 2
Parasitoids/parasites of invasive FAW in NE India.
SN Name of parasitoid/parasite
1 Chelonus formosanus Sonan
2 Telenomus cf. remus Nixon
3 Microplitis manilae (Ashmead)
4 Metopius rufus Ashmead
5 Netelia sp.
6 Ichneumon promissorius (Erichson)
7 Indeterminate wasp belonging to tribe cryptini
8 Indeterminate fly belonging to subfamily Exoristinae
9 Hexamermis cf. albicans (Siebold)
5
Biological Control 148 (2020) 104303
mermithids climb onto plants during moist conditions, usually in the
morning, and infect susceptible hosts which feed on plant parts (Nickle,
1981). Mermithid parasites nourish themselves from the insect’s hae-
molymph and then emerge to complete development outside the host.
The humid climate and high rainfall typical of Meghalaya state during
March to October appeared to create suitable conditions for parasitism
of FAW by H. albicans. Mermithids of the genus Hexamermis are known
to parasitize up to 8.42% of FAW larvae in Mexico (Ruiz-Najera et al.,
2013) and up to 30% in Nicaragua (Van Huis, 1981).
FAW larvae are susceptible to various entomopathogens, including
viruses, fungi, protozoa, bacteria, and nematodes (Gardner & Fuxa,
1980; Fuxa, 1982; Agudelo-Silva, 1986; Richter & Fuxa, 1990) and
many of these have the potential to reduce FAW populations (Wheeler
et al., 1989; Molina-Ochoa et al., 2003; Prasanna et al., 2018). The
fungus M. rileyi is highly pathogenic to noctuid caterpillars, including S.
litura (Padanad and Krishnaraj, 2009; Chaudhari et al., 2016) and S.
frugiperda (Diaz De Rienzo et al., 2009; Ruiz-Najera et al., 2013). We
found high mortality of FAW larvae due to M. rileyi and SpfrNPV in
Meghalaya. Metarhizium rileyi was reported to be an important mor-
tality factor of FAW in Cuba (Álvarez et al., 2018) and in south India
(Mallapur et al., 2018; Sharanabasappa et al., 2019). Overall, the op-
timum temperature, higher rainfall and humidity during the rainy
season could have favored this pathogen, since moist conditions play a
significant role in epizootics of entomopathogenic fungi (Maurya et al.,
2013; Mallapur et al., 2018). Moreover, rain droplets facilitate the
distribution of spores over plant surfaces, leading to more fungal in-
fections. The significantly higher incidence of M. rileyi in Lad Rymbai
and Umshorshor could be due to favorable temperatures (23 °C to
25 °C) and humid conditions that prevail in these localities during the
rainy season. A recent study from Karnataka, India (Mallapur et al.,
2018) reported 1.25–18.3% infection of FAW by M. rileyi with variation
Order and family Type
(Hymenoptera: Braconidae) Egg-larval parasitoid
(Hymenoptera: Platygastridae) Egg parasitoid
(Hymenoptera: Braconidae) Larval parasitoid
(Hymenoptera: Ichneumonidae) Larval-Pupal parasitoid
(Hymenoptera: Ichneumonidae) Larval parasitoid
(Hymenoptera: Ichneumonidae) Pupal parasitoid
(Hymenoptera: Ichneumonidae) Pupal parasitoid
(Diptera: Tachinidae) Larval-pupal parasitoid
(Mermithida: Mermithidae) Larval and pupal parasite
D.M. Firake and G.T. Behere Biological Control 148 (2020) 104303

Plate 1. Parasitoids emerged from FAW juvenile stages. (A) Chelonus formosanus, (B) Microplitis manilae, (C) Netelia spp., (D) Metopius rufus, (E) larva of C. formosanus
eggressed from FAW larva, (F), C. formosanus cocoon formed on leaf.

Fig. 3. Mean ( ± SE) percent parasitism (or mortality) of FAW attributed to various biocontrol agents at different locations in Meghalaya. Mean values bearing the
same letters are not significantly different (Tukey’s HSD, α = 0.05).

among districts attributed to climatic variation, mainly temperature another mortality factor for FAW in Meghalaya, with highest incidence
and rainfall. Similarly, Sharanabasappa et al. (2019) reported M. rileyi during April and May, likely aided by the cloudy conditions prevailing
as causing 10–15% mortality of FAW in maize fields of Southern India. in Meghalaya during pre-monsoon period. Baculoviruses are rapidly
In the present study, the baculovirus ‘SpfrNPV’ was identified as inactivated when exposed to UV or natural sunlight in the field (David

6
D.M. Firake and G.T. Behere Biological Control 148 (2020) 104303

Fig. 4. Mean ( ± SE) percent parasitism (or mortality) of FAW attributed to biocontrol agents across different months of sampling. Values bearing the same letters are
not significantly different (Tukey’s HSD, α = 0.05).

Plate 2. (A, B) parasitic nematode emerged from FAW. (C) Mermithid nematode Hexamermis cf. albicans emerged from FAW larva and FAW pupa. (D) anterior
portion of Hexamermis. (E) Posterior portion of Hexamermis post-parasitic juveniles (L-4).

and Gardiner, 1967; Young and Yearian, 1974; Black et al., 1997;
Khattab, 2003). Natural epizootics of an NPV of S. frugiperda have been
reported from Gujarat in Western India (Raghunandan et al., 2019).
Worldwide, several strains of NPVs have been isolated from the FAW,
mainly multicapsid variants (Rowley et al., 2010); the strain recorded
in our study needs additional characterization to determine the number
of capsids per envelope. Differences in FAW parasitism and microbial
infection across time and space could be due to factors such climatic
variability, agronomic practices, crop type, and crop stage (Ruíz-Nájera
et al., 2007). Different biocontrol agents may compete for common

7
D.M. Firake and G.T. Behere Biological Control 148 (2020) 104303

Table 3
Entomopathogens of invasive FAW in NE India.
SN Name of the pathogen Type Host stages infected

1 Metarhizium (=Nomuraea) rileyi (Farlow) Samson Entomopathogenic fungus Larvae

2 Beauveria bassiana (Balsamo) Vuillemin Entomopathogenic fungus Larvae and pupae
3 Spodoptera frugiperda Nuclear Polyhydrosis Virus (SpfrNPV) Entomopathogenic virus Larvae and pupae
4 Bacillus sp. Entomopathogenic bacteria Larvae
5 Unknown pathogen (like Microsporidian) Entomopathogen Larvae

Plate 3. Entomopathogens of FAW in Meghalaya. (A) Entomopathogenic fungus ‘M. rileyi’ infected larvae (2nd to 6th instar) of FAW, (B) Sporulated mycelia and the
typical conidiophore structures of M. rileyi at 400x magnification found under microscope, (C) Putrefied larva of FAW due to SpfrNPV infection, (D) Phase contrast
illumination at 400x magnification showing polyhedral inclusion bodies of SpfrNPV.

resources and some species may succeed in outcompeting others.
Therefore, a more detailed and systematic study is needed to under-
stand how competition among natural enemies exploiting FAW may be
affecting their relative abundance in India.
The deviations in values of Menhinick’s index (DMn) among lo-
calities indicates variation in species richness, which could be attrib-
uted to variability in cropping patterns, types of natural vegetation,
rainfall and other abiotic factors across the state of Meghalaya. The
Shannon Index (H) typically ranges from 1.5 to 3.5 and increases as
both the richness and the evenness of the community increase
(Magurran, 2004). Relatively high values of the Shannon Index
(> 2.16) and the Simpson Index (7.14 to 11.41) in our study indicate
high diversity of predators in the maize agroecosystems. The high di-
versity of natural enemies in Meghalaya may reflect a diversity of

Table 4
Predators found to be feeding on invasive FAW in NE India.
SN Name of predator Order and family Host stages attacked

1 Eocanthecona furcellata Wolff (Hemiptera: Pentatomidae) Larvae

2 Andrallus spinidens (Fabricius) (Hemiptera: Pentatomidae) Larvae
3 Cosmolestes sp. (Hemiptera: Reduviidae) Larvae
4 Podisus maculiventris (Say) (Hemiptera: Pentatomidae) Larvae
5 Ropalidia brevita Das & Gupta (Hymenoptera: Vespidae) Larvae
6 Polistes cf. olivaceus (De Geer) (Hymenoptera: Vespidae) Larvae
7 Indeterminate earwig (Dermaptera: Forficulidae) Eggs and small larvae
8 Cicindela spp. (Coleoptera: Cicindelidae) Eggs and larvae
9 Rhene flavicomans Simon (Arenae: Salticidae) Larvae
10 Marpissa sp. (Arenae: Salticidae) Larvae
11 Oxyopes birmanicus Thorell (Arenae: Oxyopidae) Larvae
12 Lycosa sp. (Arenae: Lycosidae) Larvae

8
D.M. Firake and G.T. Behere Biological Control 148 (2020) 104303

Plate 4. Predators of FAW in northeast India. (A) pentatomid predator Eocanthecona furcellata, (B) reduviid bug Cosmolestes sp. (C) earwig, (D) spider Oxyopes
birmanicus, (F) spider Rhene flavicomans.

Table 5 occurs widely in India, Nepal, Bhutan, Sri Lanka, Thailand, and
Species richness and diversity indices of generalist predators in maize agroe- Vietnam (NMBE World Spider Catalogue, 2019b). The predators E.
cosystems at different localities of Meghalaya. furcellata, A. spinidens, Forficula spp. and ground beetles have all been
Locality & district Menhinick’s Shannon-Wiener Simpson reported feeding on FAW life stages in southern India (Shylesha and
diversity index diversity index index (D) Sravika, 2018; Sharanabasappa et al., 2019). There remains tre-
(DMn) (H) mendous scope for identification of additional FAW natural enemies
from the entire northeastern region of India.
Umiam (RB) 0.30 2.44 8.22
Mawnohsynrum (RB) 0.23 2.45 10.56
Overall study demonstrated that the indigenous natural enemies of
Margnar (RB) 0.27 2.34 8.70 related noctuid pest species widen their host range and adopt the in-
Umshorshor (RB) 0.28 2.24 8.14 vasive FAW as a novel host/prey in invaded regions. Four biocontrol
Larnai (WJH) 0.26 2.28 8.76 agents viz., M. rileyi, SpfrNPV, C. formosanus and H. albicans cause
Khainduli (WJH) 0.23 2.60 11.41
significant mortality of FAW larvae in Meghalaya; therefore conserva-
Lad Rymbai (EJH) 0.28 2.16 7.73
Nongplit (EJH) 0.31 2.20 7.14 tion of such biocontrol agents could be vital in mitigating FAW damage
Lawbyrtun (EKH) 0.27 2.26 8.25 in maize agroecosystems. Since M. rileyi, SpfrNPV and C. formosanus can
Nongstoin (WKH) 0.25 2.47 9.91 be multiplied on mass scale under in vitro conditions; further detailed
studies on augmentative biological control of FAW by using these
Note: RB: Ri Bhoi; WJH: West Jaintia Hills; EJH: East Jaintia Hills; EKH: East
natural enemies would give more insights on their role under field
Khasi Hills; WKH: West Khasi Hills.
conditions.
natural vegetation, high floral diversity, or a large area dedicated to
Declaration of Competing Interest
organic farming (Drolet et al., 2019; Baker et al., 2020; Aldebron et al.,
2020). There is also a huge diversity of spiders in Meghalaya (Biswas
and Majumder, 1995, 2000; Bhattacharya et al., 2017). Patra et al. The authors declare that they have no known competing financial
(2013) recorded 13 spider species, including species of the three genera interests or personal relationships that could have appeared to influ-
we observed in maize agroecosystems of Meghalaya, Oxyopes, Marpissa ence the work reported in this paper.
and Lycosa. Other predators recorded in our study are also naturally
occurring generalist predators of crop pests in India and nearby coun- Acknowledgements
tries. The pentatomid bug, E. furcellata, is widely distributed in India,
China, Indonesia, Myanmar, Taiwan, Thailand, and Malaysia (CABI, Authors are thankful to the Director, ICAR Research Complex for
2019). The predatory wasp R. brevita is also native to India (Girish NEH Region, Umiam (Meghalaya) for providing experimental facilities.
Kumar and Sharma, 2014). According to The spider species O. birma- Authors are also grateful to Dr. H. V. Ghate (Pune) for identification of
nicus is commonly found in agroecosystems of India, China and In- predatory bugs and beetles; Dr Ranjit A.P. (Calicut) and Dr. Rajmohana
donesia (NMBE World Spider Catalogue, 2019a) whereas R. flavicomans K. (ZSI, Kolkata) for identification of parasitoids for our ongoing DNA
barcode database and Dr. A. Bodkhe (Amravati) for identification of

9
D.M. Firake and G.T. Behere
predatory spiders. The assistance of Dr. S. Das (Umiam), Dr. A. P.
Milton (Umiam) and Dr S. K. Sharma (Imphal) for identification and
capturing the images of entomopathogens is duly acknowledged.
Authors are also thankful to Dr Gulcan Tarla (Uşak University, Turkey)
for her comments on mermithid nematodes and Dr. Yoshitaka Kakimura
(Japan) for identification of earwigs. Authors acknowledge the assis-
tance of Dr. (Mrs) M. Das (Umiam) for capturing the images of mer-
mithid nematodes. Field assistance during sample collection by Smt. R.
W. Rangad (KVK, West Jaintia Hills), Smt. B Chyne (KVK, East Khasi
Hills) and Miss K. Chanreil Nonglait (Research Scholar, NEHU) is duly
acknowledged. Authors express sincere thanks to Prof. J. P. Michaud
(Kansas State University) for his critical suggestions and overall im-
provement of the manuscript. Authors are also grateful to Dr S. Pandit,
IISER, Pune (India) and four anonymous reviewers for their critical
comments and suggestions for the manuscript. The funding for the In-
house project “Monitoring, diagnosis and management of invasive alien
insect pest species in North East India, PIMS code: IXX14424” by the
Indian Council of Agricultural Research (ICAR), New Delhi is duly ac-
knowledged.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.biocontrol.2020.104303.
References
Agudelo-Silva, F., 1986. Naturally occurring pathogens of Spodoptera frugiperda
(Lepidoptera: Noctuidae) larvae collected in Venezuela. Fl. Entomol. 69, 768–769.
Alam, M.M., 1979. Attempts at the biological control of major insect pests of maize in
Barbados, W. I. Symp. On maize and peanut. Paramaribo, Suriname, Nov. 1318,
1978. Proc. Caribbean Food Crops Soc. 15, 127–135.
Aldebron, C., Jines, M.S., Snyder, W.E., Blubaugh, C.K., 2020. Soil organic matter links
organic farming to enhanced predator evenness. Biol. control. https://doi.org/10.
1016/j.biocontrol.2020.104278.
Álvarez, S.P., Guerrero, A.M., Duarte, B.N.D., Tapia, M.A.M., Medina, J.A.C., Domínguez
Rodríguez, Y., 2018. First Report of a New Isolate of Metarhizium rileyi from Maize
Fields of Quivicán, Cuba. Indian J. Microbiol. 58 (2), 222–226.
Anonymous, 2015. Mission Organic Farming NE. Ministry of development of northeastern
region, Government of India. http://mdoner.gov.in/sites/default/files/Final
%20Concept%20Note%20MOF%20NE%20_3_.pdf (accessed on 23.04.2020).
Ansari, M.A., Prakash, N., Ashok Kumar, Jat, S.L., Baishya, L.K., Sharma, S.K., Ch.
Bungbungcha, Sanatombi Kh., Sanjay Singh, S., 2015. Maize production technology
highlighted in North East India. Training Manual RCM (TM)-05. ICAR Research
Complex for NEH Region, Manipur Centre, Lamphelpat, Imphal, India.
Ashley, T.R., 1979. Classification and distribution of fall armyworm parasites. Fl.
Entomol. 62, 114–123.
Baker, B.P., Green, T.A., Loker, A.J., 2020. Biological control and integrated pest man-
agement in organic and conventional systems. Biol. control. https://doi.org/10.
1016/j.biocontrol.2019.104095.
Bhattacharya, A., Chetri, M., Sarkar, P., 2017. Spider diversity in different habitats at
Jaintia Hills of Meghalay. Int. J. Life Sci. 5, 613–619.
Biswas, B., Majumder, S.C., 1995. Araneae: Spiders. Fauna of Meghalaya, State Fauna
Series-4. Zool. Survey India 93–127.
Biswas, B., Majumder, S.C., 2000. Araneae: Spider. Fauna of Meghalaya, (Part-2), State
Fauna Series-4. Zool. Survey India 93–128.
Black, B.C., Brennan, L.A., Dierks, P.M., Gard, I.E., 1997. Commercialization of baculo-
viral insecticides. In: Miller, L.K. (Ed.), The Baculoviruses. Plenum Press, New York,
pp. 341–387.
Braman, S.K., Pendley, A.F., Corley, W., 2002. Influence of commercially available
wildflower mixes on beneficial arthropod abundance and predation in turf grass.
Environ. Entomol. 31, 564–572. https://doi.org/10.1603/0046-225X-31.3.564.
CABI, 2018. Spodoptera litura (taro caterpillar) Datasheet. Invasive species compendium.
https://www.cabi.org/isc/datasheet/44520 (accessed on 25.10.2019).
CABI, 2019. Eocanthecona furcellata Datasheet. Invasive species compendium. https://
www.cabi.org/isc/datasheet/21283 (accessed on 25.10.2019).
CABI, 2020. Spodoptera frugiperda (fall armyworm) Datasheet. Invasive species com-
pendium. https://www.cabi.org/isc/datasheet/29810 (accessed on 24.04.2020).
Chaudhari, C.S., Chandele, A.G., Pokharkar, D.S., Dethe, M.D., Firake, D.M., 2016.
Pathogenicity of different isolates of entomopathogenic fungus, Nomuraea rileyi
(Farlow) Samson against Tobacco Caterpillar, Spodoptera litura (Fabricius). Proc. Nat.
Acad. Sci. India, Sec. B: Boil. Sci. 86 (4), 1001–1007.
Choudhari, R., Prasad, T., Raj, B.T., 1983. Field evaluation of some exotic parasitoids of
potato tuber moth. Phthorimaea operculella (Zell). Indian J. Entmol. 45, 504–506.
David, W.A.L., Gardiner, B.O.C., 1967. The effect of heat, cold, and prolonged storage on
a granulosis virus of Pieris rapae. J. Invertebr. Pathol. 9, 555–563.
Diaz De Rienzo, M.A., Pavone, D., Trujillo, L., Dorta, B., 2009. A granular formulation of
10
Biological Control 148 (2020) 104303
Nomuraea rileyi Farlow (Samson) for the control of Spodoptera frugiperda
(LEPIDOPTERA: NOCTUIDAE). Interciencia, 34(2). pp. 130-134. ISSN 0378-1844.
Drolet, I., Guay, F., Fournier, V., Cloutier, C., 2019. Biodiversity of lepidopteran pests and
their parasitoids in organic and conventional cranberry crop. Biol. Control. https://
doi.org/10.1016/j.biocontrol.2018.11.003.
Dunn, A.M., 2009. Parasites and biological invasions. Adv. Parasitol. 68, 161–184.
Fargues, J., Rodríguez-Rueda, D., 1980. Sensibilité des larves de Spodoptera littoralis
(Lepidoptera: Noctuidae) aux hyphomycetes entompathogenes Nomuraea rileyi et
Paecilomyces fumosoroseus. Entomophaga 25, 42–54.
Firake, D.M., Behere, G.T., Firake, P.D., Rajkhowa, D.J., Azad Thakur, N.S., Saini, M.S.,
Rahman, Z., Ngachan, S.V., 2013. Arge xanthogaster (Hymenoptera: Argidae): a new
threat to rose plants in Meghalaya, India. Fl. Entomol. 96, 1298–1304.
Firake, D.M., Behere, G.T., Babu, Subhash., Prakash, N., 2019. Fall Armyworm: Diagnosis
and Management (An extension pocket book). ICAR Research Complex for NEH
Region, Umiam-793 103, Meghalaya, India. 48p. Online available: http://www.
kiran.nic.in/pdf/publications/2019/ICAR%20Pocket%20Book%20on%20FAW
%20updated%20372019.pdf.
Fuller, B.W., Reagan, T.E., Flynn, J.L., Boetel, M.A., 1997. Predation on fall armyworm
(Lepidoptera: Noctuidae) in sweet sorghum. J. Agric. Entomol. 14, 151–155.
Fuxa, J., 1982. Prevalence of viral infections in popula-tions of fall armyworm, Spodoptera
frugiperda, insoutheastern Louisiana. Environ. Entomol. 11, 239–242. https://doi.
org/10.1093/ee/11.1.239.
Ganiger, P.C., Yeshwanth, H.M., Muralimohan, K., Vinay, N., Kumar, A.R.V.,
Chandrashekara, K., 2018. Occurrence of the new invasive pest, fall armyworm,
Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in the maize fields of
Karnataka, India. Cur. Sci. 115, 621–623.
Gardner, W.A., Fuxa, J.R., 1980. Pathogens for the suppression of the fall armyworm. Fl.
Entomol. 63, 439–447.
Girish Kumar, P., Sharma, G., 2014. Taxonomic studies on vespid wasps (Hymenoptera:
Vespoidea: Vespidae) of Sunderbans Biosphere Reserve, West Bengal, India. Part 1.
Rec. zool Surv. India 114 (Part-4), 563–580.
Gupta, A., 2013. Revision of the Indian Microplitis Foerster (Hymenoptera: Braconidae:
Microgastrinae), with description of one new species. Zootaxa 3620, 429–452.
Harrison, R.D., Thierfelder, C., Baudron, F., Chinwada, P., Midega, P., Schaffner, U., Berg,
J., 2019. Agro-ecological options for fall armyworm (Spodoptera frugiperda JE Smith)
management: providing low-cost, smallholder friendly solutions to an invasive pest.
J. Environ. Manage. 243, 318–330.
IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY:
IBM Corp.
Ignoffo, C.M., 1981. The fungus Nomuraea rileyi as a microbial insecticide. In: Burges,
H.D. (Ed.), Microbial Control of Pest and Plant Diseases, 1970–80. Academic Press,
London, pp. 513–538.
Kaiser, H., 1991. Insect parasitic nematodes. Pp. 899-960. in: Nickle, W.R. (ed.) A manual
of agricultural nematology. Marcel Dekker Inc., New York, USA.
Kelly, D.W., Paterson, R.A., Townsend, C.R., Poulin, R., Tompkins, D.M., 2009. Parasite
spillback: a neglected concept in invasion ecology? Ecology 90, 2047–2056.
Kenis, M., du Plessis, H., Van den Berg, J., Ba, M.N., Goergen, G., Kwadjo, K.E., Baoua, I.,
Tefera, T., Buddie, A., Cafà, G., Offord, L., Rwomushana, I., Polaszek, A., 2019.
Telenomus remus, a Candidate Parasitoid for the Biological Control of Spodoptera
frugiperda in Africa, is already present on the Continent. Insects 10 (4), 92. https://
doi.org/10.3390/insects10040092.
Khattab, M., 2003. Enhancement and Protection of Baculoviruses Infectivity Against the
Adverse Effect of Sunlight. Ph.D. Thesis. Fac. Agric., Cairo Univ., pp. 177.
Liao, Y.L., Yang, B., Xu, M.F., Lin, W., Wang, D.S., Chen, K.W., Chen, H.Y., 2019. First
report of Telenomus remus parasitizing Spodoptera frugiperda and its field parasitism in
southern China. J. Hymen. Res. 73, 95–102.
Magurran, A.E., 2004. In: Measuring Biological Diversity. Blackwell Publishing, Oxford,
UK, pp. 256.
Mallapur, C.P., Naik, A.K., Hagari, S., Praveen, T., Patil, R.K., 2018. Potentiality of
Nomuraea rileyi (Farlow) Samson against the fall armyworm, Spodoptera frugiperda
(J.E. Smith) infesting maize. J. Entomol. Zool. Stud. 6, 1062–1067.
Matošević, D., Melika, G., 2013. Recruitment of native parasitoids to a new invasive host:
First results of Dryocosmus kuriphilus parasitoid assemblage in Croatia. Bull. Insectol.
66 (2), 231–238.
Maurya, S., Kumar, R., Choudhary, J.S., Das, B., Kumar, S., 2013. New report of Neozygites
sp. infecting red spider mite Tetranychus urticae infesting French bean from Eastern
Plateau and Hill region, India. Arch. Phytopath. Plant Protec. 46, 2278–2280.
Miętkiewicz, R., Dzięgielewska, M., Janowicz, K., 1998. Entomopathogenic fungi isolated
in the vicinity of Szczecin. Acta Mycol. 33, 123–130. https://doi.org/10.5586/am.
1998.011.
Molina-Ochoa, J., Carpenter, J.E., Heinrichs, E.A., Foster, J.E., 2003. Parasitoids and
parasites of Spodoptera frugiperda (Lepidoptera:Noctuidae) in the Americas and
Caribbean basin: an inventory. Fl. Entomol. 86, 254–287.
Molnar, J.L., Gamboa, R.L., Revenga, C., Spalding, M.D., 2008. Assessing the global threat
of invasive species to marine biodiversity. Front. Ecol. Environ. 6, 485–492.
Montezano, D.G., Sosa-Gómez, D.R., Roque-Specht, V.F., 2018. Host plants of Spodoptera
frugiperda (Lepidoptera: Noctuidae) in the Americas. Faculty Publications:
Department of Entomology 718. http://digitalcommons.unl.edu/entomologyfacpub/
718.
Nickle, W.R., 1981. Mermithid parasites of agricultural pest insects. J. Nematol. 13,
262–266.
NMBE World Spider Catalogue, 2019. Taxon details: Oxyopes birmanicus Thorell.
https://wsc.nmbe.ch/species/24646/Oxyopes_birmanicus (Last updated: 05.10.
2019).
NMBE World Spider Catalogue, 2019. Taxon details: Rhene flavicomans Simon. https://
wsc.nmbe.ch/species/32358 (Last updated: 18.09.2019).
D.M. Firake and G.T. Behere
Padanad, M.S., Krishnaraj, P.U., 2009. Pathogenicity of native entomopathogenic fungus
Nomuraea rileyi against Spodoptera litura. Online. Plant Health Prog. https://doi.org/
10.1094/PHP-2009-0807-01-RS.
Patra, S., Rahman, Z., Bhumita, P., Saikia, K., Azad Thakur, N.S., 2013. Study on pest
complex and crop damage in maize in medium altitude hill of Meghalaya. Bioscan 8
(3), 825–828.
Perfecto, I., 1991. Ants (Hymenoptera: Formicidae) as natural control agents of pests in
irrigated maize in Nicaragua. J. Econ. Entomol. 84, 65–70.
Pielou, E.C., 1975. Ecological diversity. New York: Wiley Interscience. 165 p.
Poulin, R., 2017. Invasion ecology meets parasitology: advances and challenges. Int. J.
Parasitol. Parasites Wildlife 6, 361–363.
Poulin, R., Paterson, R.A., Townsend, C.R., Tompkin, S.D.M., Kelly, D.W., 2011.
Biological invasions and the dynamics of endemic diseases in freshwater ecosystems.
Freshwat. Biol. 56, 676–688.
Prasanna, B., Huesing, J., Eddy, R., Peschke, V., 2018. Fall armyworm in Africa: A guide
for integrated pest management. CDMX: CIMMYT. 109 p.
Raghunandan, B.L., Patel, N.M., Dave, H.J., Mehta, D.M., 2019. Natural occurrence of
nucleopolyhedrovirus infecting fall armyworm, Spodoptera frugiperda (J. E. Smith)
(Lepidoptera: Noctuidae) in Gujarat, India. J. Entomol. Zool. Stud. 7, 1040–1043.
Ranga Rao, G., Wightman, J., Ranga Rao, D., 1993. World review of the natural enemies
and diseases of Spodoptera litura (F.) (Lepidoptera: Noctuidae). Insect. Sci. Appl. 14,
273–284.
Rao, B.N., 1972. Studies on the biology of Chelonus formosanus Sonan- egg-larval
parasite of Spodoptera litura (F.). M.Sc. thesis submitted to Gujarat Agriculture
University, Anand, India, 77 p.
Richter, A., Fuxa, J., 1990. Effect of Steinernema feltiae on Spodoptera frugiperda and
Heliothis zea (Lepidoptera: Noctuidae) in corn. J. Econ. Entomol. 83, 1286–1291.
https://doi.org/10.1093/jee/ 83.4.1286.
Ríos-Velasco, C., Gallegos-Morales, G., Cambero-Campos, J., Cerna-Chávezs, E., Del
Rincón-Castro, M., Valenzuela-García, R., 2011. Natural enemies of the fall army-
worm Spodoptera frugiperda (Lepidoptera: Noctuidae) in Coahuila, México. Fla.
Entomol. 94, 723–726.
Rowley, D.L., Farrar, R.R., Blackburn, M.B., Harrison, R.L., 2010. Genetic and biological
variation among nucleopolyhedrovirus isolates from the fall armyworm, Spodoptera
frugiperda (Lepidoptera: Noctuidae). Virus Genes 40, 458–468.
Ruíz-Nájera, R.E., Molina-O, J., Carpenter, J.E., Espinosa, M.J.A., Ruíz, N.J.A., Lezama,
G.R., Foster, J.E., 2007. Survey for hymenopteran and dipteran parasitoids of the fall
armyworm (Lepidoptera: Noctuidae) in Chiapas, México. J. Agric. Urban Entomol.
24, 35–42.
Ruiz-Najera, R., Ruiz-Estudillo, R.A., Sanchez-Yanez, J.M., Molina-Ochoe, J., Skoda, S.R.,
Coutino-Ruiz, R., Pinto-Ruiz, R., Guevara-Hernandez, F., Foster, J.E., 2013.
Occurrence of entomopathogenic fungi and parasitic nematodes on Spodoptera fru-
giperda (Lepidoptera: Noctuidae) larvae collected in Central Chiapas, Maxico. Fla.
Entomol. 96, 498–503.
Shannon, C.E., Weaver, W., 1949. The Mathematical Theory of Communication.
University of Illinois Press, Urbana, IL.
11
Biological Control 148 (2020) 104303
Sharanabasappa, Kalleshwaraswamy, C.M., Poorani, J., Maruthi, M.S., Pavithra, H.B.,
Divaviam, J., 2019. Natural enemies of Spodoptera frugiperda (J. E. Smith)
(Lepidoptera: Noctuidae), a recent invasive pest on maize in South India. Fl. Entomol.
102, 619–623.
Sharma, H.C., Sullivan, D.J., Bhatnagar, V.S., 2002. Population dynamics and natural
mortality factors of the Oriental armyworm, Mythimna separata (Lepidoptera:
Noctuidae), in South Central India. Crop. Prot. 21, 721–732.
Shylesha, A.N., Sravika, A., 2018. Natural occurrence of predatory bugs, Eocanthecona
furcellata (Wolff) and Andrallus spinidens (Fabr.) on Spodoptera frugiperda (Smith)
(Hemiptera:Pentatomidae) in maize and their potential in management of fall army
worm. J. Biol. Control. 32, 209–211.
Simpson, E.H., 1949. Measurement of diversity. Nature 163, 688.
Singh, S.P., 1994. Fifteen years of AICRP on biological control. Technical Bulletin No. 8,
Project Directorate of Biological Control, Bangalore, India.
Singh, R.K., 2019. Journey of the Fall Armyworm: At war (Cover story). Down to earth (1-
15 March 2019, 30-31pp. Available online: https://cdn.downtoearth.org.in/library/
0.74075500_1551766485_at_war_20190315.pdf (accessed on 21.10.2019).
Sisay, B., Simiyu, J., Malusi, P., Likhayo, P., Mendesil, E., Elibariki, N., Wakgari, M.,
Ayalew, G., Tefera, T., 2018. First report of the fall armyworm, Spodoptera frugiperda
(Lepidoptera: Noctuidae), natural enemies from Africa. J. Appl. Entomol. 142,
800–804.
Sosa-Gomez, D., Moscardi, F., 1994. Effect of till and no-till soybean cultivation on dy-
namics of entomopathogenic fungi in the soil. Fl. Entomol. 77, 284. https://doi.org/
10.2307/3495515.
Swamiappan, M., Balasubramanian, M., 1990. Host parasitoid density response to fe-
cundity of Chelonus blackburni Cam. Proc. Indian Nat. Sci. Acad. 48, 214–217.
Van Huis, A., 1981. Integrated pest management in the small farmer’smaize crop in
Nicaragua. Mededelingen Landbouwhogeschool Wageningen 81, 221.
Vänninen, I., 1996. Distribution and occurrence of four entomopathogenic fungi in
Finland: effect of geographical location, habitat type and soil type. Mycol. Res. 100,
93–101. https://doi.org/10.1016/S0953-7562(96)80106-7.
Vercher, R., Costa-Comelles, J., Marzal, C., García-Marí, F., 2005. Recruitment of native
parasitoid species by the invading leafminer Phyllocnistis citrella (Lepidoptera:
Gracillariidae) on citrus in Spain. Environ. Entomol. 34, 1129–1138.
Wheeler, G.S., Ashley, T.R., Andrews, K.L., 1989. Larval parasitoids and pathogens of the
fall armyworm in Honduran maize. Entomophaga 34, 331–340.
Whittaker, R.H., 1977. Evolution of species diversity in land communities. Evol. Biol. 10,
1–67.
Wyckhuys, K.A.G., O’Nei, I.R.J., 2006. Population dynamics of Spodoptera frugiperda
Smith (Lepidoptera: Noctuidae) and associated arthropod natural enemies in
Honduran subsistence maize. Crop. Protec. 25, 1180–1190.
Yaseen, M., 1979. Introduction of exotic parasites for control of Spodoptera and Heliothis
in Trinidad. Symp. on maize and peanut. Paramaribo, Suriname, Nov. 13-18, 1978.
Proc. Caribbean Food Crops Soc. 15, 136-141.
Young, S.Y., Yearian, W.C., 1974. Persistence of Heliothis NPV on foliage of cotton, soy-
bean, and tomato. Environ. Entomol. 3, 253–260.