PhDThesisAlbasiniCanio.pdf

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Dynamics and potential for biological control of fall armyworm Spodoptera
frugiperda (Smith) (Lepidoptera: Noctuidae) in Mozambique
Thesis · January 2023
DOI: 10.13140/RG.2.2.13028.45445
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Baseline studies for the implementation of biological control of diamondback moth (Plutella xylostella) in Mozambique View project
The fall armyworm (Spodoptera frugiperda Smith) in Mozambique: farmers’ knowledge, host range, seasonal occurrence and potential for biological control View project
Albasini Canico
Instituto Superior Politecnico de Manica
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Albasini Joaquim Caniço
Scientific Advisors:
Full Professor António Maria Marques Mexia
Associate Professor Luisa Maria Kingwell Alcântara Santos
Thesis presented to obtain the Doctor degree in Agriculture Engineering
2022

ii
Albasini Joaquim Caniço
Scientific Advisors:
Full Professor António Maria Marques Mexia
Associate Professor Luisa Maria Kingwell Alcântara Santos
Thesis presented to obtain the Doctor degree in Agriculture Engineering
JÚRI:
PRESIDENTE
Doutora Maria Teresa Marques Ferreira, Professora Catedrática do Instituto Superior de Agronomia da
Universidade de Lisboa.
VOGAIS
Doutora Laura Monteiro Torres, Professora Catedrática Aposentada da Escola de Ciências Agrárias e
Veterinárias da Universidade de Trás-os-Montes e Alto Douro;
Doutor David João Horta Lopes, Professor Associado com Agregação da Faculdade de Ciências Agrárias e do
Ambiente da Universidade dos Açores;
Doutora Luisa Maria Kingwell Alcântara Santos, Professora Associada da Faculdade de Agronomia e
Engenharia Florestal da Universidade Eduardo Mondlane, Moçambique;
Doutora Ana Álvares Ribeiro Marques de Aguiar, Professora Auxiliar da Faculdade de Ciências da
Universidade do Porto;
Doutora Elsa Maria Borges da Silva, Técnica Superior do Instituto Superior de Agronomia da Universidade
de Lisboa.
Funded by Fundação para a Ciência e a Tecnologia, I.P., through a PhD scholarship under the grant number SFRH/BD/135260/2017
2022

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Acknowledgments:
I would like to express my gratitude to the following people and institutions for their
contribution to the present thesis:
To my supervisors: for the scientific guidance and for being supportive;
To FCT- Fundação para a Ciência e a Tecnologia, I.P.: for funding my studies through a
PhD scholarship (SFRH/BD/135260/2017) under the Postgraduate Program Science for
Development (PGCD).
To Maria Madinga, Nelson Alferes, Tendai Pita, Milagre Patrocínio, Nicolau José and Isolta
Cadeado (Instituto Superior Politécnico de Manica - ISPM): for their assistance in
conducting both field and laboratory studies.
To Marc Kenis (Centre for Agriculture and Bioscience International- CABI Switzerland): for
identification of parasitoids.
To ISPM: for making its facilities available to undertake laboratory studies.
To Márcio Adamo (ISPM): for the production of the map of the sampling locations;
To the farmers and agricultural services of the districts of Macate, Manica, Sussundenga and
Vanduzi: for their collaboration during the field studies.
To PGCD: for the opportunity
To my family: for the emotional support
To all those who although not mentioned, have significantly contributed to this study

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Abbreviations
ASS: África Sub-Sahariana
CABI: Centre for Agriculture and Bioscience International
FAW: Fall Armyworm
FCT: Fundação para a Ciência e a Tecnologia
INAM: National Institute of Meteorology
ISPM: Instituto Superior Politécnico de Manica
LF: Lagarta-do-funil
PGCD: Postgraduate Program Science for Development
SSA: Sub-Saharan Africa

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Figure captions:
Figure 1.1: Global distribution of FAW as of August 2019
Figure 1.2: Adult moth of FAW
Figure 1.3: Damaged maize leaves due to FAW attack
Figure 1.4: Maize whorl damaged by FAW attack
Figure 1.5: Sampling locations in Mozambique
Figure 2.1: Monthly mean temperatures (°C) and mean precipitation (mm) during the study
period.
Figure 5.1: Reported month of maize planting per district
Figure 5.2: Reported month of highest incidence of FAW in maize fields per district
Figure 5.3: Methods of control of FAW used by smallholder farmers
Figure 5.4: Number of sprays per cropping cycle
Figure 5.5: Decision for application of insecticides
Figure 5.6: Perceived incidence of FAW among smallholder farmers per district
Figure 5.7: Perceived spread of FAW among smallholder farmers per district
Figure 5.8: Reported constraints in the control of FAW among smallholder farmers per
district

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Table captions
Table 2.1: Percentage of infested fields and average infestation of plants per field,
district, and season of sampling.
Table 2.2: Percentage of damaged plants per field and average plant damage score per
field per district and season of sampling.
Table 2.3. Average number of FAW egg masses and larvae per field per district and
season of sampling.
Table 3.1: Crops assessed for the presence of FAW
Table 4.1: Distribution of FAW parasitoids per district and season of sampling.
Table 4.2: Survival rates of different parasitoids emerging from FAW larvae per district and
season of sampling.
Table 4.3. Relative abundance of FAW parasitoids per district and season of sampling.
Table 4.4. Parasitism rates of different FAW parasitoids per district and season of sampling.
Table 4.5. Relative contribution of different FAW parasitoids to total parasitism (N = 1444).
Table 5.1: Socio-economic characteristics of farmers per district
Table 5.2: Farmers’ experience in maize cultivation, seed provenience and cultural practices.
Table 5.3: Identification and recognition of FAW attack symptoms
Table 5.4: Use of insecticides among smallholder farmers per district

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Abstract
The fall armyworm (FAW), is an alien polyphagous insect pest with origin in
Americas, where it has more than 350 host plants. Although polyphagous, FAW has
preference for maize. In 2016, FAW was detected in West and Central Africa and rapidly
spread to all Sub-Saharan Africa (SSA) countries including Mozambique. In SSA, maize is a
staple food, and the presence of FAW is a direct threat to food security. Although well
studied in its native environment, the field behavior of FAW in the new habitat is less
known, which makes it difficult to manage. The objectives of the study were: a) to assess
the seasonal dynamics of FAW; b) to assess the host range of FAW in the invaded areas; c)
to assess the occurrence of native parasitoids of FAW, their parasitism rates and relative
abundance, and; d) to assess smallholder farmers’ knowledge and management practices of
FAW.
To study its seasonality, 622 maize fields were surveyed for the presence of FAW egg
masses and larvae in wet and dry seasons. Population density, infestation and damages
were determined. To assess the host range, 35 different crops distributed in 1291 fields were
checked for the presence of FAW egg masses and larvae. To verify the possible occurrence
of native parasitoids, 101 egg masses and 1444 FAW larvae were collected from maize fields
infested with FAW and checked for parasitism. To assess farmers’ knowledge and
management practices of FAW, 200 farmers were interviewed through a semi-structured
questionnaire
FAW population density, infestation and damages on maize were found to be higher
during the dry season. At the time of this study, no evidence was found suggesting that
FAW was feeding in crops other than maize because out of 35 crops surveyed, FAW was
only recorded on maize. Five larval parasitoids of FAW were recorded but no egg parasitism

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was observed. Coccygidium luteum Brullé (Hymenoptera: Braconidae) and Drino quadrizonula
Thomson (Diptera: Tachinidae) were the primary parasitoid species. Total parasitism was
estimated at 9.49% Although most farmers are aware of FAW and its consequences, they are
unable to morphologically distinguish FAW from other caterpillars and most of them do
not use any method of control against the pest.
Surveys of FAW should be carried out in different parts of the country along several
years to generate consistent data on its seasonality and host range. Cultural practices
enhancing the performance of local occurring FAW parasitoids should be advocated among
smallholder farmers. Farmers should be trained in identification of FAW stages. Results
from this study could support some decisions toward a sustainable pest management
strategy of FAW in Mozambique.
Keywords: invasive species, population dynamics, host plants, biological control,
smallholder farmers.

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Resumo
A lagarta do funil (LF), é uma praga invasora e polífaga originária das américas, onde
possui mais de 350 hospedeiros para além do milho. Apesar da sua natureza polífaga, a LF
tem preferência pelo milho. Em 2016, a LF foi detectada pela primeira vez nas regiões
ocidental e central de áfrica e rapidamente dispersou-se para todos os países da África Sub-
Sahariana (ASS), incluindo Moçambique. Na ASS, o milho é tido como alimento base e, a
presença da LF é uma ameaça directa à segurança alimentar. Apesar de ter sido bem estuda
na sua zona de origem, o comportamento de campo da LF no seu novo habitat é pouco
conhecido, o que dificulta o seu controlo. Os objectivos deste estudo foram: a) avaliar a
sazonalidade da LF; b) determinar o espectro de hospedeiros na área de invasão; c) avaliar
a ocorrência de parasitóides locais da LF, suas taxas de parasitismo e abundância relativa,
e; d) produzir informação de base sobre o conhecimento e as práticas de maneio da LF utilizadas
pelos pequenos agricultores.
Para estudar a sazonalidade da LF, 622 campos de milho foram amostrados para a
presença de massas de ovo e lagartas nas estações seca e chuvosa. Foram determinados a
densidade populacional, infestação e estragos causados pela LF nas plantas de milho. Para
determinar o espectro de hospedeiros, 35 culturas diferentes distribuídas em 1291 campos
foram verificadas para a presença de massas de ovo e de lagartas da LF. Para verificar a
possível ocorrência de parasitóides locais, 101 massas de ovo e 1444 lagartas da LF foram
colectadas em campos de milho infestados com a LF e observadas para parasitismo. Para
avaliar o conhecimento e as práticas de maneio usadas pelos pequenos agricultores sobre a
LF, 200 agricultores foram entrevistados com recurso a um questionário semi-estruturado.
A densidade populacional, a infestacão e os estragos causados pela LF na cultura do
milho foram maiores no tempo seco. Até a altura deste estudo, não havia sido encontrada

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nenhuma evidência indicando que a LF alimentava-se de outras culturas para além do
milho, dado que das 35 culturas amostradas, a LF foi apenas encontrada no milho. Foram
registados cinco parasitóides de lagartas da LF mas nenhum parasitismo foi observado nas
massas de ovo. Os principais parasitóides de lagartas da LF foram a vespa Coccygidium
luteum Brullé (Hymenoptera: Braconidae) e a mosca Drino quadrizonula Thomson (Diptera:
Tachinidae). A percentagem total de parasitismo foi estimada em 9.49%. Apesar de muitos
agricultores estarem conscientes da presença da LF e das suas consequências, estes não
foram capazes de distinguir morfologicamente a LF de outras lagartas e, muitos deles não
usam nenhum método de controlo contra esta praga.
Para a produção de dados consistentes relacionados com a sazonalidade e o espectro
de hospedeiros da LF em Moçambique, a amostragem deve ser feita em diferentes regiões
do país e ao longo de vários anos. Adicionalmente, devem ser promovidas, entre os
pequenos agricultores, práticas culturais que favoreçam o desempenho dos parasitóides da
LF que ocorrem localmente. Outrossim, os agricultores devem ser treinados na identificação
dos diferentes estágios da LF. Os resultados deste estudo poderão ser usados como base de
apoio para estratégias de maneio sustentável da LF em Moçambique.
Palavras-chaves: pragas invasoras, dinâmica populacional, plantas hospedeiras, controlo
biológico, pequenos agricultores.

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Resumo alargado
A praga invasora Spodoptera frugiperda Smith (Lepidoptera: Noctuidae), também
conhecida como lagarta-do-funil (LF), é um inseto polífago originário das Américas, onde
possui mais de 350 hospedeiros para além do milho que é tido como o principal. Em 2016, a
LF foi detetada pela primeira vez nas regiões ocidental e central do continente Africano
atacando a cultura do milho. Devido à elevada capacidade migratória, a praga dispersou-se
rapidamente para os restantes países da África Sub-Sahariana (ASS), incluindo
Moçambique.
Por causa da sua voracidade e da sua natureza polífaga, a LF tornou-se a principal
praga do milho em campo, reduzindo significativamente os rendimentos esperados na
cultura do milho. Acontece que na região da ASS, o milho é tido como alimento base e, a
presença da LF é uma ameaça a segurança alimentar de milhões de pessoas dessa região.
Por ser uma praga nova na região, a presença da LF em campos de milho passou
despercebida entre extensionistas e agricultores, chegando em certos casos a ser confundida
com as brocas do colmo do milho por causa da similaridade dos estragos, como aconteceu
em Moçambique.
A falta de conhecimento sobre a biologia e comportamento da LF no novo habitat,
combinado com a severidade dos estragos em campos de milho, deixou as autoridades
agrárias sem um plano específico relativamente aos passos a serem tomados. Como medida
de emergência para conter os prejuízos causados pela LF, governos de vários países da ASS,
incluindo Moçambique, distribuíram e/ou promoveram o uso de inseticidas entre os
pequenos agricultores, mesmo quando tradicionalmente a prática de uso de inseticidas no
controlo de pragas de milho não era comum. No caso concreto de Moçambique, as
autoridades agrárias recomendaram o uso de 23 ingredientes activos diferentes

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pertencentes aos principais grupos de inseticidas que são os piretróides, organofosforados,
carbamatos e organoclorados, incluindo também inseticidas altamente selectivos como o
Spinosad e outros à base de microorganismos entomopatogénicos como Beauvaria bassiana e
Bacillus thuringiensis. Esta situação fez com que agricultores mal equipados e sem nenhum
treinamento sobre o uso correto de pesticidas, aplicassem indiscriminadamente diferentes
pesticidas sem ter em conta as dosagens recomendadas. Igualmente, foram recomendados
vários métodos de controlo que nunca tinham sido testados e nem validados.
Posteriormente, começou uma série de estudos, muitos deles voltados exclusivamente a
métodos de controlo, sem, no entanto, levar em consideração aspetos relativos a biologia e
comportamento da praga no seu novo habitat.
Apesar do conhecimento existente sobre a natureza polífaga da LF na sua zona de
origem, alguns aspetos críticos sobre o seu comportamento em campo no novo habitat são
pouco conhecidos, o que dificulta as autoridades agrárias de emitir instruções precisas sobre
como a praga deve ser combatida. Esses aspetos incluem a sua dinâmica populacional ao
longo do ano, os seus hospedeiros alternativos, os seus inimigos naturais e como os
pequenos agricultores lidam com a praga. Por conta disso, houve a necessidade de trazer
informação de base para dar suporte aos serviços de extensão agrária e as instituições de
investigação no desenho de alternativas sustentáveis e de fácil aplicação ao nível dos
pequenos agricultores. Tendo em conta esse cenário, foram definidos os seguintes objetivos:
a) avaliar a sazonalidade da LF em campos de milho; b) verificar a existência de hospedeiros
alternativos da LF; c) avaliar a ocorrência de parasitoides nativos da LF, suas taxas de
parasitismo e abundância relativa e; d) produzir informação de base sobre o conhecimento
e as práticas de maneio da LF utilizadas pelos pequenos agricultores.
Para a avaliação da sazonalidade da LF, foi verificada a presença de massas de ovos
e/ou lagartas da LF em 622 campos de milho nas estações seca e chuvosa. Além da densidade
populacional, também foram determinados os índices de severidade de estragos e

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percentagem de plantas infestadas por campo. Para verificar a existência de hospedeiros
alternativos da LF, foi feito um levantamento de massas de ovos e/ou lagartas da LF em 35
culturas diferentes, distribuídas em 1291 campos incluindo o milho e culturas normalmente
consociadas com o milho, ou que se encontravam nas proximidades de campos de milho.
Para avaliar a ocorrência de parasitóides nativos, suas taxas de parasitismo e abundância
relativa, foram coletadas 101 massas de ovos e 1444 lagartas da LF em campos de milho
infestados pela LF e levadas ao laboratório de entomologia do ISPM. No laboratório, as
massas de ovos e as lagartas foram individualmente colocadas em frascos, alimentados e
monitorados para a emergência de parasitóides. Para produzir informação de base sobre o
conhecimento e as práticas de maneio da LF utilizadas por pequenos agricultores, foram
entrevistados 200 agricultores experientes na produção de milho com recurso a um
questionário semiestruturado. O questionário incluía diversos aspetos como questões
socioeconómicas, capacidade de identificação da LF e métodos de controlo.
Os resultados sobre a sazonalidade da LF indicam um aumento de densidade
populacional e consequente aumento de infestação e prejuízos durante a estação seca.
Relativamente aos hospedeiros alternativos, não foi encontrada nenhuma evidência,
aquando deste estudo, que sugere que a LF esteja atacando outras culturas para além do
milho, dado que das 35 culturas avaliadas, a LF foi apenas encontrada no milho. Para o caso
dos parasitóides nativos, foi registada a ocorrência de cinco espécies de parasitóides de
lagartas da LF, mas não houve registo de parasitóides de ovos. Os parasitóides mais comuns
foram Coccygidium luteum Brullé (Hymenoptera: Braconidae) e Drino quadrizonula Thomson
(Diptera: Tachinidae) com os máximos de 23,68% e 8,86% de parasitismo e 100% e 96,3% de
abundância relativa respetivamente. A mortalidade combinada da LF como consequência
da ação dos diferentes parasitóides foi estimada em 9,49%.
Entretanto, a grande maioria dos agricultores entrevistados não é capaz de distinguir
morfologicamente a LF de outras lagartas (entre 93,88 % e 98,04% dos agricultores), mas

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reconhecem os sintomas do seu ataque no milho. Entre 92,0% e 98,04% dos agricultores
afirmaram terem tido problemas nos seus campos devido ao ataque da LF. O milho é
semeado principalmente nos meses de Outubro e Novembro mas, segundo os agricultores,
o pico de infestação acontece entre os meses de Novembro e Fevereiro. A maioria dos
agricultores não usa nenhum método de controlo da LF. Dos poucos que aplicam
inseticidas, a maioria acredita na eficácia dos mesmos no combate a LF. Há uma perceção
generalizada entre os agricultores de que a LF esteja se dispersando para novas áreas. A
falta de recursos financeiros que possibilitem a aquisição de inseticidas e outros meios de
protecção, foi apontada como o principal constrangimento no combate da LF.
Os resultados obtidos sugerem que a sementeira precoce na principal campanha
agrícola pode reduzir de forma significativa a infestação e prejuízos da LF no milho. O facto
de não se ter registado a presença de massas de ovos e nem de lagartas da LF em culturas
que não sejam o milho, levanta a possibilidade de que a estirpe da LF atualmente presente
na província de Manica seja a especializada no milho, mas devem ser realizadas
caracterizações moleculares para confirmar essa hipótese. Apesar do reduzido número de
campos de milho durante o período seco, é possível que a disponibilidade contínua de
campos de milho ao longo do ano, esteja a influenciar as escolhas da LF, fazendo que ela se
confine ao milho, evitando assim hospedeiros não preferenciais. Por causa da presença de
parasitóides nativos da LF em Moçambique, é necessário promover práticas culturais que
favorecem o desempenho desses parasitóides no campo. É necessário intensificar os
treinamentos dos agricultores sobre a identificação das diferentes fases da LF, incluindo as
fases mais suscetíveis do milho e métodos de controlo sustentáveis.
Palavras-chaves: pragas invasoras, dinâmica populacional, plantas hospedeiras, controlo
biológico, pequenos agricultores.

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Table of contents
Contents Page
Acknowledgments: .......................................................................................................................... ii
Abbreviations................................................................................................................................... iii
Figure captions:................................................................................................................................ iv
Table captions ....................................................................................................................................v
Abstract............................................................................................................................................. vi
Resumo............................................................................................................................................viii
Resumo alargado...............................................................................................................................x
Chapter 1: Background.................................................................................................................2
1.1. Origin and distribution of fall armyworm .........................................................................2
1.2. Biology and ecology of FAW...............................................................................................3
1.3. Damages caused by fall armyworm ....................................................................................4
1.4. Host plants of fall armyworm ..............................................................................................6
1.5. Host strains of FAW...............................................................................................................6
1.6. Awareness of FAW in Africa................................................................................................7
1.7. Methods of control of FAW...............................................................................................8
1.7.1. Chemical control..........................................................................................................8
1.7.2. Potential for biological control of FAW ...................................................................9
1.7.3. Integrated Pest Management of FAW......................................................................9
1.8. Study locations..................................................................................................................10
Chapter 2: Seasonal dynamics of the alien invasive insect pest Spodoptera frugiperda
(Smith) (Lepidoptera: Noctuidae) in Manica province, Mozambique.................................13
2.1. Introduction...........................................................................................................................13
2.1.1. Objective .........................................................................................................................14
2.2. Materials and methods ........................................................................................................14
2.2.1. Survey of FAW...............................................................................................................14
2.2.2. Variables .........................................................................................................................15

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2.2.3. Meteorological data.......................................................................................................17
2.2.4. Data analysis ..................................................................................................................18
2.3. Results....................................................................................................................................18
2.3.1. Infestation.......................................................................................................................18
2.3.2. Damage ...........................................................................................................................19
2.3.3. Number of FAW egg masses and larvae per field....................................................20
2.3.4. Temperature and precipitation during the survey...................................................21
2.4. Discussion..............................................................................................................................22
2.5. Study Limitations .................................................................................................................27
Chapter 3: Host range of fall armyworm Spodoptera frugiperda (Smith) (Lepidoptera:
Noctuidae) in Manica Province, Mozambique.........................................................................29
3.1. Introduction...........................................................................................................................29
3.1.1. Objective .........................................................................................................................29
3.2.1. Field survey....................................................................................................................30
3.3. Results....................................................................................................................................31
3.4. Discussion..............................................................................................................................33
Chapter 4: Native parasitoids of fall armyworm Spodoptera frugiperda (Smith)
(Lepidoptera: Noctuidae) in Mozambique................................................................................37
4.1. Introduction...........................................................................................................................37
4.1.1. Objective .........................................................................................................................39
4.2.1. Field collection of FAW egg masses and larvae........................................................39
4.2.2. Laboratory handling of field-collected material.......................................................40
4.2.3. Relative abundance of FAW parasitoids....................................................................41
4.2.4. Parasitism rates..............................................................................................................42
4.2.5. Survival of parasitoids..................................................................................................42
4.2.6. Relative contribution to total parasitism....................................................................42
4.3. Results....................................................................................................................................43
4.3.1. Distribution of FAW parasitoids.................................................................................43

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4.3.2. Survival of parasitoid species......................................................................................43
4.3.3. Relative abundance of parasitoids..............................................................................45
4.3.4. Parasitism rates..............................................................................................................45
4.3.5. Relative contribution to total parasitism....................................................................46
4.4. Discussion..............................................................................................................................47
Chapter 5: Farmers’ knowledge, perception and management practices of fall armyworm
Spodoptera frugiperda (Smith) in Manica province, Mozambique ......................................51
5.1. Introduction...........................................................................................................................51
5.1.1. Objective .........................................................................................................................52
5.2.1. Farmers’ selection and questionnaire delivery .........................................................52
5.2.2. Data analysis ..................................................................................................................53
5.3. Results....................................................................................................................................54
5.3.1. Socio-economic characteristics ....................................................................................54
5.3.2. Cropping systems, maize varieties and purpose of production ............................55
5.3.3. Identification and recognition of FAW attack symptoms .......................................56
5.3.4. Maize planting and FAW infestation periods...........................................................57
5.3.5. Methods of control of FAW used by smallholder farmers......................................59
5.3.6. Management and application of insecticides............................................................59
5.3.7. Perceived incidence, spread and constraints in the control of FAW .....................63
5.4. Discussion..............................................................................................................................65
Chapter 6: Conclusions..................................................................................................................70
References........................................................................................................................................72

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Chapter 1: Background
1.1. Origin and distribution of fall armyworm
The fall armyworm (FAW) Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) is
an alien polyphagous insect pest originating from the Americas, where it has more than 350
different host plants including both crop and non-crop species (Montezano et al., 2018). In
Africa, FAW was reported for the first time in West and Central Africa in 2016 (Goergen et
al., 2016). Shortly after, several countries of Southern Africa region as the cases of
Mozambique and Zambia, reported the presence of the pest within their borders (Cugala et
al., 2017; Uzayisenga et al., 2018). In 2018, FAW was also reported in Asia (Sharanabasappa
et al., 2018). The rapid spread of FAW is largely attributed to its migratory potential
(Meagher et al., 2004) and high dispersal capacity (Kumela et al., 2018). Due to favorable
climatic conditions of SSA to FAW, the pest is believed to occur all year-round (Early et al.,
2018). Currently, FAW is mainly distributed in the tropics (Fig. 1.1).
Fig. 1.1: Global distribution of FAW as of August 2019 (source: Wang et al. (2020))

3
1.2. Biology and ecology of FAW
FAW egg masses are laid hours after mating take place usually on the underside of
leaves (Abrahams et al., 2017). Larvae generally emerge simultaneously three to five days
following oviposition, and migrate to the whorl. The larval stage consists of six instars and
the second and third instars are often cannibalistic, resulting in only one larva in the whorl
(FAO and CABI, 2019). Larger FAW larvae have characteristic marks consisting mainly of
four dark spots forming a square on the second-to-last body segment and an inverted “Y”
in the head (FAO and CABI, 2019).
Pupae are usually found in the soil (FAO and CABI, 2019). Adult moths (Fig. 1.2)
mostly live for two to three weeks. Mated females will lay multiple egg masses, with a
potential fecundity of up to 1000 eggs per female (Abrahams et al., 2017). Temperature and
rainfall are believed to be the main climatologic factors that significantly affect pest density
(Murua et al., 2006) and distribution (Early et al., 2018).
Fig. 1.2: Adult moth of FAW (source: Goergen et al. (2016))

4
1.3. Damages caused by fall armyworm
Differently from the Americas where maize is primarily used for animal feed and
ethanol production, in Africa, most maize is produced primarily for family consumption
and planted from saved seed (Hruska, 2019). The invasion of FAW in Africa caused
devastating consequences on maize production (Feldmann et al., 2019). FAW caterpillars
feed on the leaves, stems and reproductive parts of its host plants and is categorized as one
of the most damaging pests in the Americas (Abrahams et al., 2017). FAW can attack maize
from the young stages to tasseling and ear stages (FAO and CABI, 2019), leaving the plant
with skeletonized leaves and heavily windowed whorls loaded with larval frass (Figs. 1.3
and 1.4). When left unmanaged, FAW can cause significant yield loss (FAO and CABI, 2019).
Fig. 1.3: Damaged maize leaves due to FAW attack

5
The problem of FAW in Sub-Saharan Africa exacerbated because its preferred host
plant, maize, is a staple food in the region (Midega et al., 2018; Prasanna et al., 2018; Harrison
et al., 2019). In Mozambique, for example, 21–90% of the households depend on maize for
daily subsistence (MASA, 2016). Frequent weeding and minimum- and zero-tillage seem to
reduce FAW damages in maize fields (Baudron et al., 2019). Although the foliar damage
caused by FAW does not necessarily result in dramatic yield reduction (Hruska, 2019), its
polyphagous and voracious nature constitute a lasting threat to several important crops
(Goergen et al., 2016).
Fig. 1.4: Maize whorl damaged by FAW attack

6
1.4. Host plants of fall armyworm
The FAW is one of the highly polyphagous insect pests because it has more than 350
different host plants (Montezano et al., 2018). Economically important and cultivated grasses
belonging to Poaceae family (maize, rice, sorghum, sugar cane, etc) are the main attacked
species (Bateman et al., 2018). Out of 353 known host species, 106 belong to Poaceae family
while species from Asteraceae family (e.g. lettuce and sunflower) and Fabaceae family (e.g.
peanut, pigeon pea, soybean and cowpea) are ranked in the second position both with 31
species each (Montezano et al., 2018). In Africa, FAW is reported to attack maize and
sorghum (Nagoshi et al., 2018)
1.5. Host strains of FAW
The FAW consists of two genetically distinct but morphologically undistinguishable
strains (Dumas et al., 2015). There is the maize-strain feeding primarily on maize, and the
rice-strain feeding primarily on forage grasses and rice (Veenstra et al., 1995). The biology of
these host strains is poorly understood, which makes it difficult to accurately predict its field
behavior (Nagoshi and Meagher, 2004). Although morphologically identical, FAW host
strains can be distinguished through molecular techniques (Nagoshi et al., 2007). Otim et al.
(2018), claimed that both FAW host strains were present in Africa, but this claim was
contradicted by Nagoshi et al. (2018) who suggested that the marker frequently used to
identify the host strains of FAW is compromised, not allowing precise separation of strains.
To address this issue, it would be interesting to continue genetic characterizations of African
FAW populations (Nagoshi et al., 2017).

7
1.6. Awareness of FAW in Africa
The FAW is somewhat difficult for farmers to distinguish from other local caterpillar
pest species, therefore, it may initially remain unidentified by farmers on their fields, aiding
the build-up of pest populations (Feldmann et al., 2019). In Ethiopia, Assefa and Ayalew
(2019), recommended the agricultural extension services to increase awareness among
farmers about the life stages, scouting, natural enemies of the pest, and the more susceptible
stages of maize. In Zimbabwe, Chimweta et al. (2019) recommended the training of farmers
on FAW biology and correct use of insecticides. In Mozambique, Cugala et al. (2017)
recommended that extension service workers and farmers should be trained in
identification and biology and methods of control of FAW together with a list of 22 active
ingredients for the management of FAW. A similar approach has been advocated in Zambia
(Kansiime et al., 2019) and in Kenya and Ethiopia (Kumela et al., 2018). Integrated Pest
Management (IPM) strategies were also recommended (Hailu et al., 2018; Midega et al., 2018;
Prasanna et al., 2018; Harrison et al., 2019; Meagher et al., 2019).
In addition to above-mentioned recommendations, a series of studies were initiated
including the prospect of natural enemies (Sisay et al., 2018; Kenis et al., 2019; Agboyi et al.,
2020; Koffi et al., 2020; Ngangambe and Mwatawala, 2020) assessment of damages (Sisay,
Simiyu, et al., 2019), efficacy of synthetic and botanical insecticides (Sisay et al., 2019), its
dynamics (Nboyine et al., 2020), forecasting of its distribution (Early et al., 2018), farmers
knowledge and methods of control (Kumela et al., 2018; Hruska, 2019; Kansiime et al., 2019;
Tambo et al., 2019; Toepfer et al., 2019), case studies (Wightman, 2018) and genetic
characterization (Otim et al., 2018; Meagher et al., 2019). Harrison et al. (2019), pointed out
the importance of conducting research on current pest management strategies used by
smallholder farmers against FAW which can help to fill the existing knowledge gap for a
sustainable management of the pest.

8
1.7. Methods of control of FAW
1.7.1. Chemical control
Arthropod pests are one of the major constraints to agricultural production in Africa,
but economic and social constraints have kept pesticide use the lowest among all the world
regions (Abate et al., 2000). Low yields, unstable prices, and lack of affordability of pesticides
are also possible reasons (Prasanna et al., 2018).
Before the arrival of FAW in Africa, the primary insect pests of maize were the
stemborers Busseola fusca and Chilo partellus (Abate et al., 2000). Then, the overwhelming
majority of farmers did not use pesticides, but have instead used cultural control methods
to deter or kill insect pests (Hruska, 2019). Pesticides were applied mostly against pests of
commercial crops such as vegetables (Abate et al., 2000). But, currently, the management
options of FAW are heavily based on synthetic insecticides (Agboyi et al., 2020).
After the detection of FAW, farmers increased the use of insecticides partially
motivated by the free supply of these products from the government as an emergency
response to the outbreak of FAW (Kansiime et al., 2019). The experience of Puerto Rico,
where the reliance on synthetic insecticides to control FAW led to the development of
resistance of the pest making it difficult to control (Gutiérrez-Moreno et al., 2018) should be
considered. Due to this fact, they advised that in regions with recent invasions of FAW such
as the case of Africa and Asia, synthetic insecticides should be used with caution. Bateman
et al. (2018), suggested that the use of biopesticides may be a viable alternative in the
management of FAW due to its low toxicity, and recommended the national regulators to
consider modifying the current policies for the registration of these products in order to fast-
track their availability to smallholder farmers.

9
1.7.2. Potential for biological control of FAW
In 2018, Sisay et al. (2018) published the first study on FAW natural enemies from
Africa mainly comprised of parasitoids. A total of 10 different parasitoid species were
recorded in Ghana and Benin attacking different stages of FAW with larval parasitoids
being the most common species (Agboyi et al., 2020). It was proofed that larval parasitoids
can significantly reduce herbivory of FAW (Agboyi et al., 2019). Therefore, enhancing the
effectiveness of parasitoids may benefit subsistence farmers (Hoballah et al., 2004). For good
results, parasitoids attacking different stages of FAW should be used simultaneously
(Faithpraise et al., 2015). The occurrence of local parasitoids and entomopathogens reported
in various countries (Sisay et al., 2018; Kenis et al., 2019; Ngangambe and Mwatawala, 2020)
suggest that biological control through conservation of existing natural enemies can be
employed (Estrada-Virgen et al., 2013).
1.7.3. Integrated Pest Management of FAW
Considering the biology and ecology of FAW, Integrated Pest Management (IPM)
approach is strongly recommended. Reliance on single control methods may, in the long
run, either be unsustainable or ineffective and, in the worst cases, increase the likelihood of
FAW resistance (Abrahams et al., 2017). In Africa, several IPM strategies for FAW have been
tested including maize-legume intercrop (Hailu et al., 2018), push-pull (Hailu et al., 2018;
Midega et al., 2018) and genetically modified maize varieties (Bt maize) (Botha et al., 2019).
Because the end user of these solutions are smallholder farmers, the innovations designed
to control FAW in maize should consider farmers’ knowledge of the pest, socioeconomic
circumstances, and current pest management practices (Kumela et al., 2018). Also, it is
important to study FAW population dynamics and its interaction with other species (Early
et al., 2018).

10
1.8. Study locations
Surveys were carried out from May to August 2019 (dry season of 2018/2019 cropping
season) and in December 2019 and January 2020 (rainy season of 2019/2020 cropping season)
in the districts of Macate (19o
24’50.9” South and 33o
30’54.6” East), Manica (18o
56’13.2” South
and 32o52’33.6” East), Sussundenga (19o24’39.0” South and 33o16’33.0” East) and Vanduzi
(18o
57’09.4” South and 33o
15’51.6” East) in the central province of Manica (Fig. 1.5). Districts
were selected based on their potential for maize production combined with the reported
occurrence of FAW. According to MASA (2016), the area of the survey belongs to the Agro-
Ecological Region (AER) number 4, which is characterized by the large occurrence of
ferralsoils and litosoils with an annual mean temperature around 24oC and annual mean
precipitation ranging between 800 and 1000 mm.
In Mozambique, maize is the main food crop and is cultivated in both dry and rainy
seasons. The rainy season starts from mid-November to late March. During the dry season,
maize is cultivated mainly in areas with irrigation systems or in valleys and river banks.
Maize is often grown in small plots (less than 1ha), in different cropping systems and mainly
for family consumption. In general, no fertilizers and chemicals are used for the production
of maize at smallholder farmers’ level. It is usually intercropped with roots (cassava and
sweet potato), tubers, legumes (cowpea, pigeon pea, groundnut and common beans) and
cucurbits (pumpkin, watermelon, melon).

11
Fig. 1.5: Sampling locations in Mozambique

13
The following chapter is a modified version of the manuscript published in
Insects 2020, 11(8), 512; https://doi.org/10.3390/insects11080512
Chapter 2: Seasonal dynamics of the alien invasive insect
pest Spodoptera frugiperda (Smith) (Lepidoptera:
Noctuidae) in Manica province, Mozambique
2.1. Introduction
Similarly to other insect pests, FAW is known to be affected by weather conditions of
different seasons. The number of FAW individuals in a given area is believed to be directly
influenced, among other factors, by the time of the year, weather conditions, and availability
of host plants (Mitchell, 1979). In its native habitat, for example, FAW can be found in maize
fields in all cropping seasons (Hruska and Gladstone, 1988). But in other places, such as the
southeast region of the United States, FAW is considered a sporadic pest due to weather
conditions of those regions which are not suitable in some periods of the year (Hogg et al.,
1982). When weather conditions are not favorable for its development and reproduction,
FAW is forced to migrate to more suitable locations for its survival (Johnson, 1987;
Westbrook et al., 2015).
Being originally a tropical insect (Johnson, 1987), FAW performs better in hot climates
(Tingle and Mitchell, 1977; FAO and CABI, 2019). The lower and upper limits of tolerance
of temperature are 10 (Simmons, 1993) and 42 °C (Brown et al., 1969), respectively. The
optimal range of temperature for its development is between 30 and 35 °C, and its survival

14
and development rates do not seem to be affected by humidity (Simmons, 1993). Depending
on the temperature, the development cycle of FAW can be significantly affected (Garcia et
al., 2018).
In Sub-Saharan Africa, where the temperatures are similar to those of its native area, it
is believed that FAW also occurs all year long (Early et al., 2018). A study on the seasonality
of FAW in Northern Ghana (Nboyine et al., 2020) suggested that the abundance of the pest
was influenced by temperature, rain, and relative humidity of different seasons. In
Mozambique, where FAW is a new insect pest, there are no published studies of its
seasonality which could assist smallholder farmers in concentrating and probably
coordinate control options in periods of higher infestations and damages.
2.1.1. Objective
To assess the seasonal dynamics of fall armyworm in maize fields in the central
province of Manica, Mozambique.
2.2. Materials and methods
2.2.1. Survey of FAW
A total of 622 fields were surveyed in dry and rainy seasons including 25 and 131 in
Macate, 29 and 137 in Manica, 27 and 141 in Sussundenga, and 59 and 73 in Vanduzi,
respectively. Districts were visited once per month. Each field was visited once during the
study period. Fields were selected using a snowball sampling technique. Only fields with at
least 200 plants were selected. Based on the illustration of maize growth stages by
Beckingham (2007), only fields in which plants were in stages 1 to 5 were sampled.

15
To avoid border effects, in fields in which maize was planted in rows, the first two
border rows were excluded from the survey. In fields in which maize was not planted in
rows, an estimated distance of 1 m from the border was excluded from the survey on either
side of the field. In each field, 20 plants were selected in a “W” pattern and checked for the
presence of FAW egg masses and/or larvae. A distance of 3m between plants was observed.
Stalks and both upper and lower surfaces of plant leaves were inspected.
The number of egg masses and larvae present in each plant was recorded. The number
of infested plants and plants damaged as a consequence of FAW attack was also recorded.
Foliar damage was assessed based on a visual scale ranging from 0 to 5 scores as described:
0 = plant with no visual foliar damage; 1 = up to 10% of foliar damage; 2 = foliar damage
between 10 to 25%; 3 = foliar damage between 25 to 50%; 4 = foliar damage between 50 to
75%; 5 = more than 75% of foliar damage or a dead plant due to FAW attack. Field surveys
were carried out during the daylight period, from 7 h to 17 h, and no trap was used to
monitor adult moths. Given that the pupal stage of FAW normally occurs in the soil, this
stage was deliberately excluded from the survey. In very few cases which came to our
attention, sprayed fields were also excluded from the survey.
2.2.2. Variables
2.2.2.1. Percentage of infested fields
The percentage of infested fields per district (FI) was determined by dividing the
number of fields in which FAW egg masses and/or larvae were recorded (Fi) by the total
number of fields surveyed (Ft) and converted to per cent values (Equation (2.1.)). Fields
were considered as being infested whenever at least 1 out of 20 plants observed per field
contained FAW egg masses and/or larvae.

16
𝐹𝐼 =
Fi
Ft
∗ 100% (2.1.)
2.2.2.2. Percentage of infested plants
The percentage of infested plants per field (PI) was determined by dividing the number
of plants found to contain FAW egg masses and/or larvae (Pi) by the total number of plants
surveyed (Pt) and converted to per cent values (Equation (2.2.)). Plants were considered as
being infested whenever FAW egg masses and/or larvae were recorded.
𝑃𝐼 =
Pi
Pt
∗ 100%
(2.2.)
2.2.2.3. Percentage of damaged plants
The percentage of damaged plants per field (PD) was determined by dividing the
number of plants with visual symptoms of FAW attack (Pd) by the total number of plants
surveyed (Pt) and converted to per cent values (Equation (2.3.)). Plants were considered as
being damaged every time visual symptoms of FAW attack were recorded, regardless of the
presence or absence of feeding larvae.
𝑃𝐷 =
Pd
Pt
∗ 100%
(2.3.)
2.2.2.4. Average plant damage
The average plant damage per field (LD) was determined by dividing the sum of scores
of individual plants (∑Di) by the total number of plants surveyed (Pt) (Equation (2.4.)).
𝐿𝐷 =
∑ Di
Pt (2.4.)

17
2.2.2.5. Number of FAW egg masses per field
The average number of FAW egg masses per field (EG) was determined by dividing the
number of recorded egg masses per district (Er) by the total number of fields surveyed in
the district (Fd) (Equation (2.5.)).
𝐸𝐺 =
Er
Fd (2.5.)
2.2.2.6. Number of FAW larvae per field
The average number of FAW larvae per field (LD) was determined by dividing the
number of larvae recorded per district (Lr) by the total number of fields surveyed in the
district (Fd) (Equation (2.6.)).
LD =
Lr
Fd (2.6.)
2.2.3. Meteorological data
Monthly mean temperatures and precipitation of the study period were obtained from
the office of the National Institute of Meteorology (INAM) in Manica province, which is
responsible for monitoring the weather in the study area. Due to the unavailability of
meteorological data from the districts of Vanduzi and Macate, we used data from the closest
weather stations of Chimoio and Gondola, respectively.

18
2.2.4. Data analysis
Data analysis was performed through R Statistical Software version 3.6.1 (Action of the
Toes). Mean differences of the percentage of damaged and infested plants and the average
number of egg masses and larvae per field between seasons in the same district were
assessed through a t-test at 95% confidence interval. One-way analysis of variance (α = 0.05)
was performed to detect differences on the percentage of damaged and infested plants and
the average number of egg masses and larvae per field among districts within the same
season of sampling. Mean separation on these variables was performed through a Tukey
honestly significant difference test (Tukey HSD) at 95% family-wise confidence level.
Differences in damage scores per field within the same district in different seasons, and
among districts in the same season, were assessed based on the points of the scale used.
2.3. Results
2.3.1. Infestation
Table 2.1. (below) shows the percentage of infested fields and infested plants per field
per district and season of sampling. In the dry season, the percentage of infested fields
ranged from 60 to 82.76%, while in the rainy season, the values ranged from 14.18 to 34.25%.
The percentage of infested plants per field was higher in the districts of Sussundenga and
Manica (p = 0.008), although Manica did not differ from Macate and Vanduzi. For the rainy
season, a higher percentage of infested plants was recorded in the district of Vanduzi (p <
0.001). When comparisons were made between seasons, the percentage of infested plants
per field was higher in the dry season in all districts.

19
Table 2.1. Percentage of infested fields and average infestation of plants per field, district, and season
of sampling.
District
% of Infested Fields % of Infested Plants Per Field (Mean ± SD)
Dry Season Rainy Season Dry Season Rainy Season
Macate 60.00 16.15 31.00 ± (38.94) Ba 2.62 ± (7.02) Bb
Manica 82.76 23.36 48.45 ± (35.36) ABa 5.62 ± (14.49) Bb
Sussundenga 81.48 14.18 66.48 ± (37.95) Aa 3.23 ± (9.64) Bb
Vanduzi 71.19 34.25 42.63 ± (38.43) Ba 11.99 ± (21.03) Ab
SD = Standard Deviation. Means ± (SD) followed by the same capital letter in the column are not
statistically different. Means ± (SD) followed by the same small letter between columns are not
statistically different.
2.3.2. Damage
Table 2.2. shows the percentage of damaged plants per field and average plant damage
scores per field per district and season of sampling. No differences were observed in the
percentage of damaged plants per field among districts in the dry season (p = 0.117) but, in
the rainy season, the district of Sussundenga exhibited a lower percentage of damaged
plants per field (p = 0.004), which in turn was not different from Macate and Manica.
Between seasons, the percentage of damaged plants per field was higher in the dry season
than in the rainy season in all districts.
In the dry season, the average plant damage was more intense in the district of
Sussundenga 3 scores, which means that between 25 and 50% of the plant surface appeared
to be damaged by FAW larvae. Still, no differences were observed on damage intensity in
the rainy season among districts. When damage intensity was compared within the same
district between seasons, dry season once again showed higher values than those recorded
in the rainy season.

20
Table 2.2. Percentage of damaged plants per field and average plant damage score per field per
district and season of sampling.
District
% of damaged plants per field (Mean ± SD)
Plant damage score per field (Scale 0–5)
(Mean ± SD)
Macate 62.4 ± (40.03) Aa 19.35 ± (38.47) ABb 1.33 ± (1.16) Ba 0.33 ± (0.66) Ab
Manica 79.14 ± (35.71) Aa 18.61 ± (33.40) ABb 1.62 ± (0.95) Ba 0.34 ± (0.63) Ab
Sussundenga 81.48 ± (31.31) Aa 11.88 ± (28.43) Bb 2.88 ± (5.04) Aa 0.25 ± (0.61) Ab
Vanduzi 80.59 ± (30.39) Aa 30.27 ± (42.34) Ab 1.51 ± (0.90) Ba 0.69 ± (1.03) Ab
2.3.3. Number of FAW egg masses and larvae per field
Table 2.3 shows the average number of FAW egg masses and larvae per field per
district and season of sampling. No differences were observed in the number of FAW egg
masses per field within the same season among districts, nor between seasons in the same
district. While the number of FAW larvae per field was higher in the district of Sussundenga
during the dry season (p < 0.001), in the rainy season, the district of Vanduzi was the one
with higher values (p < 0.001). Between seasons, all districts had a higher number of larvae
per field in the dry season.
Table 2.3. Average number of fall armyworm (FAW) egg masses and larvae per field per district and
season of sampling.
District
Number of Egg Masses (mean ± SD) Number of Larvae (Mean ± SD)
Macate 0.16 ± (0.62) Aa 0.03 ± (0.35) Aa 7.92 ± (10.36) Ba 0.52 ± (1.40) Bb
Manica 0.69 ± (1.63) Aa 0.01 ± (0.09) Aa 11.76 ± (9.75) Ba 1.25 ± (3.33) Bb
Sussundenga 1 ± (2.56) Aa 0 ± (0.0) Aa 26.19 ± (24.73) Aa 0.74 ± (2.32) Bb
Vanduzi 0.44 ± (1.60) Aa 0 ± (0.0) Aa 10.56 ± (11.16) Ba 2.75 ± (5.59) Ab

21
2.3.4. Temperature and precipitation during the survey
An increase in the average monthly temperatures can be observed during the rainy
season when compared with the dry season. A similar pattern was also observed in the case
of rain, where huge differences were recorded between seasons (Figure 2.1).
Figure 2.1. Monthly mean temperatures (°C) and mean precipitation (mm) in the districts of Macate,
Manica, Sussundenga, and Vanduzi in the dry season (May to August) and in the rainy season
(December and January).

22
In Macate, the temperatures of the dry season varied from 18.7 to 24.4 °C, while in
the rainy season ranged from 26.3 to 26.9 °C. While the precipitation varied from 1.2 to 10.9
mm in the dry season, in the rainy season, it varied from 212.2 to 241.8 mm. In Manica, the
temperatures ranged from 15.4 to 20.7 °C during the dry season and from 23.3 to 23.9 °C in
the rainy season. However, the precipitation varied from 0 to 10.9 mm during the dry season
and from 80.5 to 186.8 mm during the rainy season. In Sussundenga, the temperatures of
the dry season ranged from 13.9 to 19.7 °C. In contrast, for the rainy season, the temperatures
varied from 20.5 to 22.5 °C. The precipitation for Sussundenga ranged from 0 to 8.7 mm in
the dry season and from 134.9 to 279.4 mm in the rainy season. In Vanduzi, the temperatures
of the dry season varied from 17.4 to 20.5 °C, while in the rainy season varied from 24.2 to
25.5 °C. The precipitation of the dry season varied from 0 to 8.2 mm, while that of the rainy
season varied from 193.2 to 220.6 mm.
2.4. Discussion
In this study, the number of infested plants per field (Table 2.1) was lower than the
number of damaged plants (Table 2.2). This result was likely due to the short period of larval
development when compared to the length of the period of maize vegetative stage, as larvae
might have reached the adult stage and abandoned damaged plants. Some plants which
were found to be damaged were not necessarily infested at the time of the sampling.
Although we did not record the growth stages of maize plants in each field, growth
stages at the time of the sampling might have played a role in the levels of infestation and
damages observed among districts and between seasons. In their study, Murua et al. (2006)
found that at the plant level, the infestation by FAW was age-dependent because younger
stages of maize were found to be more infested than older stages. The sampling interval

23
observed during this study might also have affected the results as conditions varied in
different months.
We expected to record higher numbers of FAW egg masses and larvae during the
rainy season due to more availability of food in this period compared to the dry season,
which would result in more significant foliar damages and infestation. However, we
observed a contrary tendency as the number of egg masses and larvae recorded in the rainy
season were much lower than those found on the dry season, although the number of maize
fields sampled in the rainy season was by far higher than during the dry season.
There was a slight difference in temperatures between seasons (Fig. 2.1). Unlike
temperature, the difference in rainfall between seasons was noticeably big. Our results
suggest that rainfall was a key factor influencing the differences observed in the number of
FAW egg masses and larvae per field between seasons in all districts and that temperature
did not affect the survival of FAW.
Climatic factors are believed to directly affect the survival and abundance of pest
species (Cammell and Knight, 1992) as was observed in Nicaragua (van Huis et al., 1982)
when they recorded an increase of FAW population during the dry season. Precipitation is
another critical factor which has a direct negative effect on larval and pupal survival of FAW
(Early et al., 2018).
Concerning the rain, several studies (Early et al., 2018; Garcia et al., 2018) suggested
that the population density of FAW is negatively influenced by pluviometric conditions
because when the maize whorl is filled up with water, the larvae of FAW are forced to
abandon the whorl. In contrast, egg masses and small larvae are washed off onto the ground,
reducing, by consequence, the pest population. Our results on FAW population during the

24
rainy season seem to follow the hypothesis of reduction of its population as a consequence
of the rainy weather which occurs from mid-November to late March as it might have
significantly affected the survival rate of FAW. Our findings suggest that the dynamics of
FAW seems to be more influenced by the prevailing climatic conditions rather than by the
number of maize fields available.
Among several weather factors, temperature plays a key role in the survival and
development of FAW (Nboyine et al., 2020). Studying the seasonality of FAW and other
noctuid species, it was observed that an increase in the temperature resulted in the build-
up of its population (Tingle and Mitchell, 1977). Our results suggest that the potential effects
of temperature on FAW population are nullified by the amount of rain occurring in the same
period, as rain has adverse impacts on FAW population. The differences in the mean
temperatures between seasons are not significant enough to create specific conditions which
could have influenced FAW population differently, as in both seasons, the mean
temperatures are situated within the favorable range for its development.
In East Africa (Kenya, Tanzania, and Uganda), a close relative of FAW, the noctuid
Spodoptera exempta Walker, seems to exhibit a contrasting behavior as its peak occurs
between December and May (Brown et al., 1969). However, the weather conditions are not
very different from those of Mozambique in the same period. In their study of seasonal
abundance of FAW in Florida, USA, Waddill et al. (1982) recorded very low numbers of
moths between December and April in two consecutive years. Studying the seasonal
distribution of FAW in southern Florida, Nagoshi and Meagher (2004) concluded that the
reduction of the amount of rain had a positive effect on the population of FAW. Although
Florida is in the northern hemisphere, its rainy season occurs in the same period as in the
southern hemisphere where Mozambique is located. Therefore, the hypothesis that rain

25
affects FAW abundance might explain the numbers of FAW recorded in both seasons of our
study.
Another important factor affecting FAW dynamics in maize fields is altitude.
Analyzing the influence of altitude in the abundance of FAW, Wyckhuys and O’Neil (2006)
concluded that there was a negative correlation between the abundance of FAW and
altitude, as fields located in higher altitudes were less infested than those located in lower
altitudes. Despite the existence of slight differences in altitude among sampling locations
(from 542 m above sea level in Sussundenga to 679 m above sea level in Manica), differences
observed might have been caused by factors other than altitude as the sampling locations
are considered as being in the same range of altitude.
While different levels of infestation and damage may affect the yield differently
(Cruz and Turpin, 1983), in our study, both infestation and damage were higher in the dry
season. They might have had a different influence on the yield when compared with the
rainy season. Based on the relationship between the percentage of FAW-infested plants and
yield on maize (Hruska and Gladstone, 1988), the infestation recorded in our study during
the dry season might have caused a yield reduction ranging from 11% in the district of
Macate to 27% in the district of Sussundenga compared to potential yield reduction ranging
from around 2% in the district of Macate to 8% in the district of Vanduzi in the rainy season.
The knowledge of the dynamics of a pest population is a fundamental tool for the
implementation of integrated pest management strategies. In temperate climates, where
winter temperatures are shallow and not suitable for development and reproduction of
FAW, its population is limited to the summer (Chowdhury et al., 1987). Monitoring the
populations of two Lepidopteran Noctuid species in the United States, it was found that the
peak of the populations of both species occurred in the spring (Stadelbacher et al., 1972).

26
This trend was also confirmed for FAW (Pair et al., 1986). It is important to note that during
the spring in some regions of the United States, the weather conditions are similar to those
of winter (dry season) in tropical countries like Mozambique
Our results show that the population density of FAW is higher in the dry season than
in the rainy season. Nevertheless, Silvain and Ti-A-Hing (1985) reported a contradicting
scenario in their study about the infestation of FAW in pasture grasses in French Guiana,
where the highest number of FAW larvae was observed during the rainy season and the
lowest in the dry season. Another contradicting scenario was also reported in Northern
Ghana, where the rainy season positively influenced the population of FAW in maize fields
(Nboyine et al., 2020). These conflicting scenarios reinforce the hypothesis that the dynamic
of a pest population is a complex issue, given that the pest itself is influenced by climate and
weather which in turn are also complex and dynamic (Cammell and Knight, 1992).
For unknown reasons, FAW is differently affected by rain. While in some places rain
has positive effects on FAW population, in other locations the very same element acts in the
opposite direction. Although there may exist other factors contributing to the regulation of
FAW population which we may not be aware of, the continuous availability of maize
throughout the year combined with weather conditions seem to play a more significant role
in the dynamics of FAW in Manica province.
Agricultural practices and cropping patterns that may change with the season are
believed to influence the evolution and population dynamics of insect pests (Kennedy and
Storer, 2000). However, our results do not fit in this assumption as, traditionally, cropping
patterns used by smallholder farmers in Mozambique do not change that much, given that
same crops are cultivated in both dry and rainy seasons, varying only in the number of fields

27
per season. Therefore, cropping patterns do not appear to be a determinant factor of FAW
dynamics in Manica province.
2.5. Study Limitations
Results from this study should not be taken as conclusive given the limited period in
which it was carried out. Although our results are preliminary, they shed light on the field-
behavior of FAW in the country, considering its pest status and that FAW is a new pest in
Mozambique. Given the complexity of the dynamics of insect pests and to generate detailed
information about the seasonality of FAW, future surveys should be carried out across years
and include both on-farm and on-station experiments in different AER’s of the country. On-
farm and on-station experiments would allow multiple visits to the same fields during the
growth cycle of the crop and the gathering of data related to the monthly fluctuation of FAW
population throughout the year.

29
The following chapter is a modified version of the manuscript published as a preprint in
Preprints 2021; https://doi.org/10.20944/preprints202101.0102.v1
Chapter 3: Host range of fall armyworm Spodoptera
frugiperda (Smith) (Lepidoptera: Noctuidae) in Manica
Province, Mozambique
3.1. Introduction
Despite its ability to survive in different host plants, fall armyworm (FAW) is known
to have a high preference for maize (Molina-Ochoa et al., 2001; Nagoshi et al., 2018). Since
the detection of FAW in Africa, the majority of studies have been concentrated on options
for management of the pest on maize (Bateman et al., 2018; Hailu et al., 2018; Midega et al.,
2018; Assefa and Ayalew, 2019; Tambo et al., 2019; Chimweta et al., 2019; Feldmann et al.,
2019; Kansiime et al., 2019; Sisay et al., 2019; Agboyi et al., 2020; Ngangambe and Mwatawala,
2020) and little is known about its alternative host plants.
Economically important crops such as cabbage, cassava, tomato and common bean
which are among the reported host plants of FAW (Montezano et al., 2018) are largely grown
in Mozambique by smallholder farmers. Being a polyphagous insect pest, the knowledge of
the population dynamics of FAW in various host plants can be used as a tool for the design
of effective pest management strategies (Fuxa, 1989; Montezano et al., 2018).
3.1.1. Objective
To assess the host range of fall armyworm in food crops usually mixed with maize
or located in the vicinity of maize fields in the central province of Manica, Mozambique.

30
3.2.1. Field survey
Maize fields and crops normally mixed with maize or located in the proximity of
maize fields were surveyed. Fields were selected through snowball sampling technique.
Each field was visited once during the study period. To avoid border effects, the first two
border rows were excluded from the survey in fields where crops were planted in rows. In
fields where crops were not planted in rows, an estimated distance of 1 meter from the
border was excluded from the survey on either side of the field.
Based on the illustration of maize growth stages by Beckingham (2007), only maize
fields in which the plants were in stages 1 to 5 were sampled as described: (stage 1): five
leaves fully emerged; (stage 2): eight leaves fully emerged; (stage 3): 12 leaves; (stage 4): 16
leaves and; (stage 5): Tasseling/Silking. In crops different from maize, plants in vegetative
stages were sampled. In each field, 20 plants were selected in a “W” pattern and checked for
the presence of FAW egg masses and/or larvae. A distance of 3 meters between plants was
observed.
Stalks and both upper and lower surfaces of the plant leaves were inspected. Field
surveys were carried out during the daylight period from 7h to 17h. The names of the crops
assessed were recorded. Where crops were found to be mixed or intercropped in the same
field, a separate survey was carried out for each crop according to the number of crops in
the field.

31
3.3. Results
Table 3.1 shows the crops assessed for the presence or absence of FAW per district and season of sampling. A total of
1291 fields with different food crops were surveyed. Thirty-five different crops belonging to 14 families were covered. The
top 3 most cultivated crops in Manica province are, in order of their importance: maize with 622 fields, pumpkin with 134
fields and cassava with 99 fields.
Table 3.1: Crops assessed for the presence of FAW
Family name Common name Scientific name
Number of fields/district Absence or
Presence
of FAW
Macate Manica Sussundenga Vanduzi
Total
DS RS DR RS DS RS DS RS
Amaranthaceae Beetroot Beta vulgaris L. 1 1 a
Amaryllidaceae Garlic Allium sativum L. 1 6 7 a
Onion Allium cepa L. 2 1 3 6 a
Apiaceae Carrot Daucus carota L. subsp. sativus 1 1 a
Araceae Madumbe Colocasia esculenta (L.) Schott 1 2 1 1 5 a
Asteraceae Lettuce Lactuca sativa L. 5 1 1 7 a
Sunflower Helianthus annuus L. 1 1 2 a
Brassicaceae Cabbage Brassica oleracea L. var. capitata 3 17 5 7 12 4 48 a
Chinese
cabbage
Brassica rapa L. subsp. pekinensis 1 4 3 8 a
Portuguese
kale
Brassica oleracea L.var. acephala 7 16 5 5 1 4 2 40 a
Rape Brassica napus L. 1 4 1 1 7 a
Convolvulaceae Sweet poptato Ipomoea batatas (L.) Lam 5 3 2 5 1 11 27 a
Cucurbitaceae Cucumber Cucumis sativus L. 2 7 2 11 a
Melon Cucumis melo L. 6 3 9 a
Pumpkin Cucurbita moschata Duchesne 5 23 3 18 4 53 1 27 134 a

32
Table 3.1 (continued)
Family name
Common
name
Scientific name
Number of fields/district Absence or
Presence
of FAW
Total
DS RS DR RS DS RS DS RS
Watermelon Citrullus lanatus (Thunb.) 1 5 9 15 a
Euphorbiaceae Cassava Manihot esculenta Crantz 9 31 4 5 7 24 19 99 a
Fabaceae
Common
bean
Phaseolus vulgaris L. 2 1 10 2 4 1 20 a
Cowpea Vigna unguiculata (L.) Walp. 1 8 1 4 4 15 13 46 a
Green bean Phaseolus vulgaris L. 1 2 1 3 1 8 a
Peanut Arachis hypogaea L. 1 4 3 4 12 a
Peas Pisum sativum L. 2 2 4 a
Pigeon pea Cajanus cajan L. 6 6 1 2 2 8 2 27 a
Yoke beans
Vigna aconitifolia (Jacq.)
Maréchal
2 2 4 a
Malvaceae Okra
Abelmoschus esculentus (L.)
Moench
1 2 1 10 11 25 a
Pedaliaceae Sesame Sesamum indicum L. 7 7 a
Poaceae Maize Zea mays L. 25 130 29 137 28 141 59 73 622 present
Rice Oryza sativa L. 1 1 a
Sorghum Sorghum bicolor (L.) Moench 3 5 8 a
Wheat Triticum aestivum L. 3 3 a
Solanaceae Eggplant Solanum melongena L. 1 1 a
Irish potato Solanum tuberosum L. 5 1 3 7 16 a
Piri Piri Capsicum frutescens L. 1 2 3 a
Sweet
peeper
Capsicum annuum L. 2 3 1 1 3 10 a
Tomato Solanum lycopersicum L. 13 27 2 3 1 1 47 a
DS = Dry Season, RS = Rainy Season, a = absent

33
3.4. Discussion
Out of 35 different crops belonging to 14 families surveyed, maize was the only
crop in which FAW was recorded. Although FAW can attack many crops of different
families including cabbage, pumpkin, cassava, pigeon pea, cowpea and okra as stated by
Montezano et al. (2018), our study could not confirm this behavior as all of the above-
mentioned crops were surveyed but with no recorded presence of FAW. Several studies
(Leuck et al., 1974; Pitre et al., 1983; Buntin, 1986) have suggested that despite its ability to
survive in different host plants, FAW has a preference for gramineous plants such as
maize and sorghum. Being in the group of the most preferred host plants like maize, we
expected to record FAW on sorghum, wheat and rice, but we failed to record any egg
mass and larvae in these crops.
Most polyphagous insect exhibit distinct preferences for particular plant species
and plant growth stages (Kennedy and Storer, 2000). The simultaneous occurrence of the
most preferred host with alternative hosts may lead to the concentration of the pest
population in fields where the most preferred host is located (Kennedy and Storer, 2000).
Johnson (1987) suggested that in case of continuous availability of the most preferred host
plant, FAW may confine its attack to that host. Our results seem to be aligned with these
statements as in addition to the fact that maize is the most preferred host plant, it happens
that it is also grown throughout the year regardless of the season, making it easier for
FAW to keep feeding solely on it continually, avoiding thus its alternative host plants.
Another important aspect to be noted is the fact that FAW is composed of two
genetically differentiated but morphologically identical strains, each exhibiting different
host specificity (Pashley, 1986). The claim of the existence of two different host-strains of
FAW was also confirmed by Nagoshi et al. (2012). There is the maize-strain feeding

34
primarily on maize and the rice-strain feeding primarily on forage grasses and rice
(Veenstra et al., 1995). Shortly after the presence of FAW was confirmed in Africa, both
maize-strain and rice-strain were detected in Uganda feeding on maize fields (Otim et al.,
2018). In the African continent, the maize strain is believed to be the most predominant
of the two (Early et al., 2018) which may explain the fact that FAW was only recorded in
maize fields during our study. While the strain development is strongly influenced by
the host plant (Whitford et al., 1988), it should be observed that host plant per se does not
determine the identity of colonizing strain (Virla et al., 2008). Due to the existence of these
morphologically identical strains, it is hard to understand the field behavior of FAW as
suggested by Nagoshi and Meagher (2004).
When host-specific strains feed and reproduce on alternative host plants, its
development can be compromised. Meagher et al. (2004) observed poor larval
development and high mortality rates on FAW larvae of a maize-specific strain fed on
different hosts. Studying the behavior and distribution of the FAW host strains, Nagoshi
and Meagher (2004) concluded that the maize-specific strain was primarily found in
agricultural areas. Fuxa (1989) suggested that when maize reaches the maturation stage
becoming thus unsuitable for oviposition, maize-specific strain populations may migrate
to other locations where maize is still in its vegetative stages avoiding different host
plants.
Prevailing climatic conditions of the regions where FAW occurs may have a certain
influence on its behavior. Within this line, Groot et al. (2010) questioned if there was a
geographic variation in host preference of FAW. Although we did not study the
distribution or occurrence of the two reported host-strains of FAW, it seems that the
population of FAW occurring in Manica province might be a geographical distinct strain
and it may explain why we did not record its presence in different crops other than maize.

35
As a surviving instinct, insects choose the best conditions possible including their
host plant species for a successful offspring. Wiseman and Davis (1979) noted that the
lack of certain substances or qualities for oviposition, food and/or shelter may lead an
insect pest to avoid some plants. Most of the plant species recorded in this study have a
very different architecture compared to that of maize. Depending on the ecology of the
pest, plant architecture may also play an important role when choosing its host plants as
it may define the suitability of the plant for shelter. Pumpkins for example, according to
Baudron et al. (2019), may provide better shelter habitat for FAW than maize due to its
closed-canopy leaves. Based on this assumption, we should have recorded FAW feeding
in plants with closed-canopy leaves such as sweet potato and pumpkins, but we were
unsuccessful in doing so.

37
The following chapter is a modified version of the manuscript published in
Insects 2020, 11(9), 615; https://doi.org/10.3390/insects11090615
Chapter 4: Native parasitoids of fall armyworm
Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae)
in Mozambique
4.1. Introduction
Before the arrival of FAW in Africa, it was estimated that more than 97% of
smallholder farmers did not use any chemicals for pest management on maize
production. However, that scenario changed immediately after the detection of FAW,
because governments in various countries started distributing and/or promoting the use
of synthetic insecticides as an emergency response (Kumela et al., 2018; Hruska, 2019;
Sisay et al., 2019). As farmers did not receive accurate information from agricultural
services on which insecticides to apply and how and when to apply, they mostly decided
on their own, leading to indiscriminate use of insecticides both in terms of type and dose
of application.
The continuous and arbitrary use of synthetic insecticides by farmers with no
adequate training on pesticides management and application may induce the
development of resistance of FAW to these insecticides as was the case in Puerto Rico and
Mexico (Gutiérrez-Moreno et al., 2018). Additionally, it contributes to environmental
pollution and the killing of beneficial insects. It also raises public health concerns as most
farmers do not use adequate application and protection equipment when spraying their
fields. Furthermore, the effective application of insecticides requires some knowledge of

38
the biology and ecology of the pest being targeted, and that was not the case for FAW in
Africa (Tambo et al., 2019). For these reasons, the use of insecticides should not be viewed
as a stand-alone technique, but as a component of an Integrated Pest Management (IPM)
scheme (Abrahams et al., 2017). In the IPM approach, natural enemies can play an
important role in the management of FAW (Dequech et al., 2013).
In its native habitat, FAW is attacked by several natural enemies including
parasitoids and entomopathogenic fungi (Lezama-Gutiérrez et al., 2001; Rios-Velasco et
al., 2011; Estrada-Virgen et al., 2013; Thomazoni et al., 2014) which target different
development stages (Ruiz-Najera et al., 2007; Dequech et al., 2013; Hay-Roe et al., 2016;
Meagher Jr et al., 2016) causing significant mortality on its population (Ashley, 1986;
Wheeler et al., 1989; Hoballah et al., 2004). Around 17 different parasitoid species of FAW
are known in its native range (Ashley, 1986). In Mexico, a complex of larval parasitoids
belonging to Ichneumonidae, Braconidae, Eulophidae, and Tachinidae families were
reported (Molina-Ochoa et al., 2001; Hoballah et al., 2004; Ruiz-Najera et al., 2007; Rios-
Velasco et al., 2011; Estrada-Virgen et al., 2013). In Florida, larval parasitoids of FAW were
also reported (Hay-Roe et al., 2016; Meagher Jr et al., 2016). In Honduras, the main natural
enemies of FAW are also larval parasitoids (Wheeler et al., 1989). In Brazil, FAW eggs are
primarily parasitized by Trichogramma spp. (Hymenoptera: Trichogrammatidae)
(Dequech et al., 2013).
In Africa, several parasitoids attacking different stages of FAW were reported in
various countries. Six larval parasitoids were collected in Ethiopia, four larval parasitoids
and one egg parasitoid were collected in Kenya, and four larval parasitoids were collected
in Tanzania (Sisay et al., 2018). Telenomus remus Nixon (Hymenoptera: Scelionidae), an
important egg parasitoid of Spodoptera spp. (Lepidoptera: Noctuidae) was found
parasitizing eggs of FAW in South Africa, Côte d’Ivoire, Niger, Benin and Kenya (Kenis

39
et al., 2019) and also in Ghana (Agboyi et al., 2020). A complex of egg, egg–larval, larval,
and larval–pupal parasitoids of FAW including T. remus, Trichogramma sp., Chelonus
bifoveolatos Szépligeti (Hymenoptera: Braconidae), Coccygidium luteum (Brullé)
(Hymenoptera: Braconidae), Cotesia icipe Fernandez-Triana and Fiaboe (Hymenoptera:
Braconidae), Meteoridea cf. testacea (Granger) (Hymenoptera: Braconidae), Charops sp.
(Hymenoptera: Ichneumonidae), Metopius discolor Tosquinet (Hymenoptera:
Ichneumonidae), Pristomerus pallidus (Kriechbaumer) (Hymenoptera: Ichneumonidae),
and Drino quadrizonula (Thomson) (Diptera: Tachinidae) were reported in Ghana and
Benin (Agboyi et al., 2020). Different parasitoid species including Bracon sp.
(Hymenoptera: Braconidae), Anatrichus erinaceus Loew (Diptera: Chloropidae), and an
unidentified tachinid were also reported in Ghana (Koffi et al., 2020).
In Mozambique, no information is available regarding the potential for biological
control through native parasitoids. Biological control has the potential to bring economic,
health, and environmental benefits in the long term.
4.1.1. Objective
To assess the occurrence of native parasitoids of FAW, their parasitism rates, and
relative abundance for potential application in biological control programs.
4.2.1. Field collection of FAW egg masses and larvae
A total of 622 maize fields were surveyed including 25 and 131 fields in Macate,
29 and 137 fields in Manica, 27 and 141 fields in Sussundenga, and 59 and 73 fields in
Vanduzi in the dry and rainy seasons, respectively. Districts were selected based on their

40
potential for maize production combined with the reported occurrence of FAW. Each
field was visited once during the study period. Fields were selected through snowball
sampling techniques. Only fields with at least 200 plants were selected. Based on the
illustration of maize growth stages by Beckingham (2007), only maize fields in which
plants were in stages 1–5 were sampled as described: (stage 1): five leaves fully emerged;
(stage 2): eight leaves fully emerged; (stage 3): 12 leaves; (stage 4): 16 leaves; (stage 5):
Tasseling/Silking.
In each field, plants with visible FAW attack symptoms were intentionally selected
and checked for the presence of FAW egg masses and larvae. Stalks, whorls, and both
upper and lower surfaces of plant leaves were inspected. The number of plants inspected
and the number of FAW egg masses and larvae collected varied among fields, as a
consequence of the number of damaged/infested plants per field. FAW egg masses and
different larval stages were collected from infested maize plants together with a piece of
a fresh leaf so that larvae could continue feeding. Egg masses were temporarily placed in
bulk into 50 mL transparent plastic vials. FAW larvae were placed in a transparent plastic
bowl covered with a mesh and transferred to the entomology laboratory at Instituto
Superior Politécnico de Manica. Given that the pupal stage of FAW occurs typically in
the soil, this stage was deliberately excluded from the survey. Sprayed fields were also
excluded from the survey.
4.2.2. Laboratory handling of field-collected material
In the laboratory, FAW egg masses and larvae were counted and separated per
district and date of collection. Individual egg masses were transferred to 2.5 mL
Eppendorf tubes and covered with cotton wool. Larvae were transferred to individual
plastic vials with small holes in the lid to allow ventilation. Larvae were fed with clean

41
and non-treated pieces of fresh maize leaves grown in a greenhouse. Both egg masses
and larvae were reared at an ambient temperature varying between 26 and 30 °C. Every
48 h, feces of feeding larvae were removed from the vials and vials were cleaned with
cotton wool before adding new pieces of fresh maize leaves.
Daily, egg masses and larvae were checked for parasitism. After the emergence of
parasitoids, dead FAW larvae were removed from the vials. Unparasitized FAW larvae
were allowed to reach the adult stage and used for a separate study. FAW larvae hatching
from unparasitized egg masses were also used in a separate study. The number of
individuals of each parasitoid species emerged from parasitized larvae was recorded. The
behavior (endo/ectoparasitic) and trait (solitary/gregarious) of each parasitoid species
were recorded. The behavior and trait of each parasitoid were determined based on
laboratory observations.
Emerged adult parasitoids were preserved in 70% alcohol and frozen at −27 °C.
The parasitoids were sent for morphological identification to CABI Switzerland, which
hosts a collection of parasitoids attacking FAW in Africa and is presently preparing an
identification key and descriptions for all recorded species (M. Kenis, personal
communication). Voucher specimens are preserved at CABI Switzerland.
4.2.3. Relative abundance of FAW parasitoids
The relative abundance of each parasitoid species (RA) was determined by dividing
the number of individuals of a given parasitoid species (ni) by the total number of
individuals of all parasitoid species (N) and converted to percent values (Equation (4.1)).
𝑅𝐴 =
ni
N
∗ 100% (4.1)

42
4.2.4. Parasitism rates
The parasitism rate of each parasitoid species (Pp) was determined by dividing the
number of parasitized larvae (Lp) by the number of collected larvae (TL) and converted
to percent values (Equation (4.2)). Gregarious parasitoids emerging from a single larva
were considered as being only one. Parasitism rate of the egg masses was not calculated
as none were parasitized.
𝑃𝑝 =
Lp
TL
∗ 100% (4.2)
4.2.5. Survival of parasitoids
Larvae of different parasitoids emerging from FAW larvae were counted and
monitored until the emergence of adult individuals. Larvae of parasitoids were reared at
ambient temperature described in Section 4.2.2. Not a single FAW larvae or pupa was
dissected to search for dead parasitoids. The survival rates of different larval parasitoids
(SR) were determined by dividing the number of individuals reaching the adult stage
(Pa) by the number of individuals emerging from field collect FAW larvae (Pe) and
converted to percent values (Equation (4.3)).
𝑆𝑅 =
𝑃𝑎
𝑃𝑒
∗ 100% (4.3)
4.2.6. Relative contribution to total parasitism
The relative contribution of each parasitoid species to total parasitism (RP) was
determined by dividing the total number of FAW larvae parasitized by each parasitoids
species in both seasons (PS), by the total number of FAW larvae collected in both seasons
(LS) and converted to percent values (Equation (4.4))

43
𝑅𝑃 =
PS
LS
∗ 100% (4.4)
4.3. Results
4.3.1. Distribution of FAW parasitoids
A total of 101 FAW egg masses were collected, but no egg parasitoids were detected.
Five different larval parasitoids were collected from 1444 FAW larvae. Recorded
parasitoids were distributed in three different families: C. luteum, Charops sp., M. cf.
discolor, Unidentified (Diptera: Tachinidae), and D. quadrizonula. M. cf. discolor and the
unidentified tachinid could not be identified with certainty because only one male
specimen was collected. Parasitoids were found to be differently distributed among
districts and between seasons. Three parasitoid species were recorded in Macate, three in
Manica, four in Sussundenga, and two in Vanduzi. Out of all five parasitoid species, C.
luteum was the only parasitoid recorded in all districts in both seasons (Table 4.1).
4.3.2. Survival of parasitoid species
Table 4.2 shows the survival rates of different parasitoid species emerging from field-
collected FAW larvae. The two most common species C. luteum and D. quadrizonula
reached maximum survival rates of 52.63% and 88.44% respectively. The numbers shown
in Table 4.2 suggest that C. luteum suffers high mortality when compared to D.
quadrizonula as the majority of its larvae or cocoons did not reach the adult stage.

44
Table 4.1. Distribution of fall armyworm (FAW) parasitoids per district and season of sampling.
Parasitoid Species Host Stage Attacked Behavior and Trait
DS RS DS RS DS RS DS RS
Coccygidium luteum Larva
Endoparasitoid and solitary + + + + + + + +
Charops sp. Larva Endoparasitoid and solitary + − + − + − − −
Metopius cf. discolor Larva *** − − − − + − − −
Unidentified tachinid Larva *** − − + − − − − −
Drino quadrizonula Larva Endoparasitoid and solitary-gregarious + − − − + − + +
*** The behavior and trait could not be determined because only one specimen was collected. DS = dry season; RS = rainy season; (−) = no record; (+) = present.
Table 4.2. Survival rates of different parasitoids emerging from FAW larvae per district and season of sampling.
Parasitoid Species
DS RS DS RS DS RS DS RS
Coccygidium luteum 0 (n = 8) 44.44 (n = 9) 0 (n = 3) 52.63 (n = 19) 10 (n = 10) 20 (n = 5) 100 (n = 1)
31.58 (n =
19)
Charops sp. 100 (n = 1) − 100 (n = 1) − 100 (n = 1) − − −
Metopius cf. discolor − − − − 100 (n = 1) − − −
Unidentified tachinid − − 100 (n = 1) − − − − −
Drino quadrizonula 100 (n = 3) − − − 85.71 (n = 28) −
88.46 (n =
26)
100 (n = 1)
DS = dry season; RS = rainy season; n= number of larvae of different parasitoid species emerging from FAW larvae.

45
4.3.3. Relative abundance of parasitoids
Table 4.3 shows the relative abundance of different FAW parasitoid species
recorded in all districts in different seasons. The braconid C. luteum and the tachinid D.
quadrizonula were the two most abundant species. While in the dry season the relative
abundance of C. luteum oscillated from 3.7% in Vanduzi to 66.67% in Macate, in the
rainy season, its relative abundance oscillated from 95% in Vanduzi to 100% in Macate,
Manica, and Sussundenga. In the dry season, the abundance of D. quadrizonula varied
from 25% in Macate to 96.3% in Vanduzi.
Table 4.3. Relative abundance of FAW parasitoids per district and season of sampling.
Parasitoid
Species
DS (n
= 12)
RS (n =
9)
DS (n =
5)
RS (n
= 19)
DS (n =
40)
RS (n =
5)
DS (n =
27)
RS (n =
20)
Coccygidium
luteum
66.67 100 60.00 100 25.00 100 3.70 95.00
Charops sp. 8.33 − 20.00 − 2.50 − − −
Metopius cf.
discolor
−
−
−
−
2.50
− −
−
Unidentified
tachinid
−
−
20.00
−
− − − −
Drino
quadrizonula
25.00
−
− − 70.00 − 96.30 5.00
DS = dry season; RS = rainy season; n = total number of individuals of different parasitoid species.
4.3.4. Parasitism rates
Table 4.4 shows the parasitism rates of different parasitoid species of FAW.
Parasitism rates varied both per district and season of sampling. Parasitism rates also
varied among species with C. luteum reaching a maximum of 23.68% in the district of
Macate during the rainy season, and D. quadrizonula reaching 8.86% in the district of
Sussundenga during the dry season. The parasitism rates of C. luteum appeared to be
higher during the rainy season in all districts when compared to the dry season.

46
Table 4.4. Parasitism rates of different FAW parasitoids per district and season of sampling.
Parasitoid
Species
DS (n =
188)
RS (n =
38)
DS (n =
247)
RS (n =
115)
DS (n =
316)
RS (n =
63)
DS (n =
303)
RS (n =
174)
Coccygidium
luteum
4.26 23.68 1.21 16.52 3.16 7.94 0.33 10.92
Charops sp. 0.53 − 0.40 − 0.32 − − −
Metopius cf.
discolor
−
−
− − 0.32
−
−
−
Unidentified
tachinid
−
−
0.40 − −
−
− −
Drino
quadrizonula
1.6 − − − 8.86
−
8.58 0.57
DS = dry season; RS = rainy season; n = number of FAW larvae collected.
4.3.5. Relative contribution to total parasitism
The total parasitism of FAW larvae as the result of the individual contribution of
different parasitoid species was estimated at 9.49%. The braconid C. luteum and the
tachinid D. quadrizonula were the main contributors for the total parasitism with 5.12%
and 4.02%, respectively (Table 4.5).
Table 4.5. Relative contribution of different FAW parasitoids to total parasitism (N = 1444).
Parasitoid Species Relative Parasitism
Coccygidium luteum (n = 74) 5.12
Charops sp. (n = 3) 0.21
Metopius cf. discolor (n = 1) 0.07
Unidentified tachinid (n = 1) 0.07
Drino quadrizonula (n = 58) 4.02
Total (n = 137) 9.49
n = number of FAW larvae parasitized by different parasitoid species; N = number of FAW larvae
collected.

47
4.4. Discussion
Jourdie et al. (2008) experienced a serious problem with incomplete development
of hymenopteran parasitoids emerging from fall armyworm larvae. However, a
different scenario was reported by Agboyi et al. (2020) in which around 95% of C. luteum
individuals completed their development. From Table 4.2, it can be observed that C.
luteum individuals which emerged from FAW larvae collected during the dry season
suffered higher mortality than those emerging from FAW larvae collected in the rainy
season. Based only in this observation, we were unable to determine the possible cause
for such behavior.
A survey conducted in Ghana and Benin by Agboyi et al. (2020), found a complex
of braconid, ichneumonid, and tachinid parasitoids including D. quadrizonula, C. luteum,
and Charops sp. occurring in both countries and M. cf. discolor occurring only in Ghana.
In East Africa—Ethiopia, Kenya, and Tanzania—C. luteum and Charops sp. were also
found parasitizing FAW larvae with relatively high rates (Sisay et al., 2018). The
braconid C. luteum is known to attack the following species: Spodoptera exempta Walker,
Spodoptera exigua Hubner, Condica capensis Guenée all of them belonging to Lepidoptera:
Noctuidae, and Crypsotidia mesosema Hampson (Lepidoptera: Erebidae) and Cydia
ptychora (Meyrick) (Lepidoptera: Tortricidae). The ichneumonid M. cf. discolor is known
to attack other species of Lepidoptera: Noctuidae namely: Helicoverpa armigera
(Hubner), Helicoverpa zea Boddie, and Spodoptera litura Fabricius.
Braconid wasps seem to be good parasitoids for exhibiting high parasitism rates
(Estrada-Virgen et al., 2013). In this study, the braconid C. luteum was among the most
common species and major contributors to the total parasitism. The importance of the
endoparasitoid C. luteum as a biocontrol agent of FAW larvae in Africa was evidenced
by Agboyi et al. (2019) when they observed a decrease in the leaf consumption in
parasitized individuals by 89%.

48
Dipteran parasitoids are also reported as being important biocontrol agents of FAW
in Argentina (Murua et al., 2006) and of S. exempta, a close relative of FAW in Nigeria
(Faithpraise et al., 2015). Between the two recorded tachinid parasitoids, D. quadrizonula
was the most common and also the major contributor to the total parasitism.
In our study, both ichneumonid M. cf. discolor and Charops sp. had low parasitism
rates of 0.73% and 0.21%, respectively. Low parasitism rates of ichneumonid parasitoids
on FAW larvae were also reported in Mexico (Molina-Ochoa et al., 2001; Rios-Velasco et
al., 2011) and Argentina (Murua et al., 2006). However, in Tanzania, Charops sp. was
found parasitizing up to 75% of the larvae of other lepidopteran pests such as Spodoptera
litoralis Boisduval (Lepidoptera: Noctuidae) (Robertson, 1973) and Orgyia mixta Snellen
(Lepidoptera: Erebidae) (Migunda, 1970), which are both close relatives of FAW. In
another study, M. cf. discolor and Charops sp. were also reported as being parasitoids of
H. armigera, another close relative of FAW (van den Berg et al., 1988).
Murua et al. (2006), reported total parasitism of FAW by larval parasitoids as being
around 35%. In our study, we recorded total parasitism of 9.49%, which is around four-
fold lower. Pest species with similar characteristics as FAW namely, broad geographic
distribution, wide host range, and high migratory behavior can easily escape, at least
initially, from the constraints imposed by their native natural enemies (Cammell and
Knight, 1992). This fact may explain low parasitism levels recorded in our study, given
that FAW is a new pest in Mozambique. High parasitism rates of FAW in its native
environment can be attributed to a large number of parasitoid species attacking
targeting several stages, which was not the case observed in this study.
It is believed that biological control through habitat management may lead to a
more sustainable pest control approach (Akter et al., 2019). The fact that most
smallholder farmers do not use insecticides in maize production should be considered

49
as an advantage for the implementation of IPM programs based on biological control
of FAW. Although it may take a considerable time to achieve a balanced relationship
between FAW and its native parasitoids, the implementation of cultural practices
favoring the action of parasitoids should be advocated.

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