Introduction
The fall armyworm (FAW) (Spodoptera frugiperda: Lepidoptera: Noctuidae), which is native to the tropical Americas, was first reported in Africa in 2016 (Goergen et al., Reference Goergen, Kumar, Sankung, Togola and Tamò2016) and has since spread to Asia and Australia (Qi et al., Reference Qi, Ma, Wan, Ren, McKirdy, Hu and Zhang2021; Srikanth et al., Reference Srikanth, Geetha, Singaravelu, Ramasubramanian, Mahesh, Saravanan, Salin, Chitra and Muthukumar2018). FAW is a devastating polyphagous pest with over 350 host plant species but is mostly found on maize (Montezano et al., Reference Montezano, Specht, Sosa-Gómez, Roque-Specht, Sousa-Silva, Paula-Moraes, Peterson and Hunt2018). Meanwhile, maize is the main staple food crop for over 300 million Africans and a major source of livelihood and nutritional security across the world (Shiferaw et al., Reference Shiferaw, Prasanna, Hellin and Bänziger2011). In the absence of any control measure, FAW is estimated to cause over 80% yield loss (Abrahams et al., Reference Abrahams, Beale, Cock, Corniani, Day and Godwin2017a). In Ghana, the national yield loss due to FAW was estimated to be 26.6% in 2017 valued at US$ 177 m (Abrahams et al., Reference Abrahams, Beale, Cock, Corniani, Day and Godwin2017a). The distribution of pesticides by many African countries for FAW control has led to their acceptance by farmers as the primary means of FAW management (Kansiime et al., Reference Kansiime, Mugambi, Rwomushana, Nunda, Lamontagne-Godwin, Rware, Phiri, Chipabika, Ndlovu and Day2019; Tambo et al., Reference Tambo, Day, Lamontagne-Godwin, Silvestri, Beseh, Oppong-Mensah, Phiri and Matimelo2020). However, the likely misuse of these hazardous pesticides poses human health and environmental threats and could lead to insecticide resistance in FAW (Abraham et al., Reference Abraham, Benhotons, Krampah, Tagba, Amissah and Abraham2018; Ihara et al., Reference Ihara, Buckingham, Matsuda, Sattelle, Ihara, Buckingham and Matsuda2017; Ullah and Shad, Reference Ullah and Shad2017). Boaventura et al. (Reference Boaventura, Martin, Pozzebon, Mota-Sanchez and Nauen2020) showed high frequency of targeted site mutations conferring insecticide resistance in FAW in Kenya. Recent reports indicate that the application of high doses of insecticides to control FAW has resulted in resurgence of insects in maize farms (Kumar et al., Reference Kumar, Gadratagi, Paramesh, Kumar, Madivalar, Narayanappa and Ullah2022). These suggest that biological control could be a promising alternative to chemical control.
Moreover, biological control of FAW has been considered more sustainable to chemical control because it is environmentally friendly, improves food safety by eliminating chances of pesticides residue, and prevents resistance development (Abbas et al., Reference Abbas, Ullah, Hafeez, Han, Dara, Gul and Zhao2022). To find a sustainable management option for FAW in Africa, scientists across the continent initiated the search for locally occurring natural enemies adapted to the pest, for possible biological control. These studies have identified several predators, parasitoids and a few entomopathogens attacking the pest in the field (Agboyi et al., Reference Agboyi, Goergen, Beseh, Mensah, Clottey, Glikpo, Buddie, Cafà, Offord, Day, Rwomushana and Kenis2020; Ahissou et al., Reference Ahissou, Sawadogo, Bokonon-Ganta, Somda and Verheggen2021a). The majority of parasitoid species reported on FAW in Africa are larval parasitoids, including Coccygidium luteum (Brullé) (Hymenoptera: Braconidae) (Agboyi et al., Reference Agboyi, Mensah, Clottey, Beseh, Glikpo, Rwomushana, Day and Kenis2019; Ahissou et al., Reference Ahissou, Sawadogo, Bokonon-Ganta, Somda and Verheggen2021a; Durocher-Granger et al., Reference Durocher-Granger, Tibonge, Musesha, Lowry, Reynolds, Buddie, Cafà, Offord, Chipabika, Dicke and Kenis2021; Otim et al., Reference Otim, Aropet, Opio, Kanyesigye, Opolot and Tay2021). In Ghana, C. luteum was found in all agro-ecological zones attacking FAW and it was the most dominant parasitoid species found (Agboyi et al., Reference Agboyi, Goergen, Beseh, Mensah, Clottey, Glikpo, Buddie, Cafà, Offord, Day, Rwomushana and Kenis2020). Conversely, in Kenya and Tanzania, field parasitism rate C. luteum was only 9% (Sisay et al., Reference Sisay, Simiyu, Malusi, Likhayo, Mendesil, Elibariki, Wakgari, Ayalew and Tefera2018). Coccygidium luteum belongs to the sub-family Agathidinae with more than 45 genera (Sharkey and Chapman, Reference Sharkey and Chapman2017). It is one of the 26 species of the genus Coccygidium, which consists of a group of solitary koinobiont larval endoparasitoids of Lepidoptera (Ghramh, Reference Ghramh2011). In its distribution range, C. luteum is a parasitoid of other Noctuidae. It is the most widely reported larval parasitoid associated with FAW in Africa and has been reported in several African countries including Ghana and Benin (Agboyi et al., Reference Agboyi, Goergen, Beseh, Mensah, Clottey, Glikpo, Buddie, Cafà, Offord, Day, Rwomushana and Kenis2020), Cameroon (Abang et al., Reference Abang, Nanga, Kuate, Kouebou, Suh, Masso, Saethre and Mokpokpo Fiaboe2021), Uganda (Otim et al., Reference Otim, Aropet, Opio, Kanyesigye, Opolot and Tay2021), Kenya, Ethiopia and Tanzania (Sisay et al., Reference Sisay, Simiyu, Malusi, Likhayo, Mendesil, Elibariki, Wakgari, Ayalew and Tefera2018), Burkina Faso (Ahissou et al., Reference Ahissou, Sawadogo, Bokonon-Ganta, Somda and Verheggen2021a), and Mozambique (Caniço et al., Reference Caniço, Mexia and Santos2020). In Ghana, C. luteum is one of ten parasitoid species attacking FAW (Agboyi et al., Reference Agboyi, Goergen, Beseh, Mensah, Clottey, Glikpo, Buddie, Cafà, Offord, Day, Rwomushana and Kenis2020). To confirm its identity, morphological and molecular identification were conducted by the diagnostic services laboratory of the Centre for Agriculture and Biosciences International (CABI). Voucher specimens were deposited at GenBank (https://www.ncbi.nlm.nih.gov/nuccore/MN900728,MN900739,MN900741).
Until the invasion of the FAW, the biology and ecology of C. luteum were not comprehensively studied. There is very limited information on the main hosts of this parasitoid in Africa and its potential as biological control agent against important lepidopteran pests on the continent. Currently, there is no research on host age preference, parasitism rate, sex ratio, pre-oviposition period, longevity, and effect of superparasitism on this parasitoid thereby hindering its possible use in biological control of FAW. Recently, Agboyi et al. (Reference Agboyi, Mensah, Clottey, Beseh, Glikpo, Rwomushana, Day and Kenis2019) reported a 19% field parasitism rate of FAW by C. luteum and have also demonstrated that the amount of maize leaves consumed by FAW larvae parasitised by C. luteum declined by 89% compared to unparasitised larvae. These studies have demonstrated a high potential of C. luteum as an agent for augmentative biological control of FAW in Africa. However, it could be possible to optimise the level of parasitism if the biology of the parasitoid is better understood. Indeed, understanding the reproductive biology of parasitoids and factors influencing them is a prerequisite for assessing their biological control potential and their efficient use in biological control programmes. For instance, it has been established that percent parasitism of Diaprepes abbreviatus eggs by Ceratogramma etiennei decreases as eggs mature (Amalin et al., Reference Amalin, Peña and Duncan2005). Also, it is known that younger Trichogramma euproctidis females parasitised more Ephestia kuehniella eggs than older ones (Tabebordbar et al., Reference Tabebordbar, Shishehbor, Ebrahimi, Polaszek and Riddick2022). It is unknown if similar relationships exist between the larvae of FAW and their parasitoids because earlier studies did not focus much on the biology and host age preference of C. luteum. It is therefore imperative to study these. In this paper, we provide a detailed report on the host age preference and reproductive biology of C. luteum.
Materials and methods
Laboratory colony of Coccygidium luteum and its host FAW
Rearing of the parasitoid, C. luteum, and its host, FAW, was carried out at the Biological Control Laboratory of the Plant Protection and Regulatory Services Directorate (PPRSD) of the Ministry of Food and Agriculture (MOFA) located in Accra, Ghana. Approximately 500 FAW larvae were collected from infested maize fields in Somanya in the Eastern Region of Ghana during the major maize growing season in May 2021. For the purpose of this study, the collected FAW larvae were categorised as ‘early instars’ (1st–3rd instar) and late instars (4th–6th instar) following the FAW larval identification guide https://www.agric.wa.gov.au/sites/gateway/files/Fall%20armyworm%20larval%20identification%20guide%20DPIRD.pdf (Capinera, Reference Capinera2020) and kept in transparent plastic bowls (18.5 × 12.5 × 4.5 cm; Unipak Ltd, Accra, Ghana). They were provided with maize leaves as feed and transported to the laboratory. In the laboratory, the larvae were separated individually into 80 ml transparent plastic cups (Everpack Ltd, Accra, Ghana) with perforated lids for aeration and provided with fresh young maize leaves as feed. Monitoring of the larvae and changing of the leaves were done every other day until FAW or parasitoids pupated. FAW larvae that were parasitised by C. luteum yielded parasitoid cocoon. Both FAW pupae and parasitoid cocoon were observed daily for adult emergence. After emergence, the adults of C. luteum were used to establish a laboratory culture of the parasitoid. The FAW moths obtained from pupated non-parasitised larvae were used to establish a host culture in 34 × 30 cm locally manufactured oviposition cages made from transparent cylindrical plastic buckets. The inner walls of the cages were cleaned regularly using cellulose paper to avoid contamination. The lids of the cages were ventilated, using white polyester material. Additionally, on one side of the cage, an opening measuring 11 × 12 cm was ventilated with white polyester material and a sleeve located at the opposite side. The parasitoid and FAW cultures were kept at 28 ± 1°C and 29 ± 1°C respectively, with relative humidity of 70 ± 5% and photoperiod of L12: D12. All tests were carried out under 28 ± 1°C environmental conditions. FAW moths were fed with 70% honey solution soaked in cotton wool and placed in oviposition cages. The colony of adult C. luteum was fed with droplets of 100% honey streaked on the internal walls of the cages and provided with water soaked in cotton wool placed in a sauce cup. The cotton wool soaked with water was replaced daily while honey droplets were monitored and replenished when needed. In all the experiments, larvae were exposed to the female parasitoids for oviposition without feed or maize leaves. This was standardised across all experiment with exposure time of 35 minutes.
Parasitism bioassay
In the laboratory, both early instar (1st–3rd instar) and late instar (4th–6th) FAW larvae collected from the field were monitored for parasitoid emergence. No C. luteum emerged from all late instar (4th–6th) larvae (n = 200). Based on this observation, further experiments on parasitism were restricted to early instar (1st–3rd instar) larvae only. To determine the stage among the 1st–3rd instars that is preferred for parasitism by C. luteum, a no-choice experiment was conducted. In the no-choice experiment, 25 individuals of FAW larvae of a particular stage were placed in oviposition containers (500 ml PET bottles with aerated caps) (n = 9) and exposed to a mate female of C. luteum for 35 minutes for parasitism without providing feed or maize leaves. After the 35-minute exposure period, the larvae were placed into aerated cups (80 ml) individually and provided with pieces of fresh young maize leaves as feed. The leaves were changed every other day until pupation. The pupae were maintained under the same experimental conditions and observed regularly until adult emergence in 8–12 days. The number of cocoons and emerged parasitoids observed were counted and recorded. The stages for which no-choice experiments were conducted were first instar (3-day old larvae), early second instar (4-day old larvae), late second instar (5-day old larvae), and third instar (6-day old larvae).
Prior to the no-choice experiments, pairs (male and female) of C. luteum were mated for 24 hours in 50 ml plastic vials covered with cotton wool for aeration. The internal walls of the plastic vials were streaked with droplets of honey and a ball of cotton wool soaked in water in a sauce cup was placed at the bottom of the vial.
Host age preference
Using the susceptible host ages (3-, 4-, 5-, and 6-day old larvae) which correspond to specific stages of early instar FAW larvae from the no-choice experiment, choice experiments were conducted to determine the preferred age (stage of FAW larval instar) by C. luteum. Six combinations of larvae, covering all the susceptible host ages, were used as follows: 3- and 4-day old; 3- and 5-day old; 3- and 6-day old; 4- and 5-day old; 4- and 6-day old; and 5- and 6-day old larvae. Fifteen larvae of each age group making a total of 30 larvae were simultaneously placed in a 500 ml PET bottle as an oviposition cage with an aerated cover, using a camel-hair brush. A single mated C. luteum female was introduced into the oviposition cage to oviposit for 35 minutes. Each combination was replicated five times. Parasitised larvae were immediately transferred into 80 ml sauce cups containing tissue paper and fresh maize leaves. The feed was replenished every other day, as previously described, until pupation by non-parasitised larvae or cocoon formation by the parasitised larvae. The positions of the sauce cups were changed every 2 days to account for any environmental variation. The number of parasitoid cocoons from each age group combination was recorded.
Biology of Coccygidium luteum
To determine the maximum number of host larvae that a single C. luteum can parasitise in a day, an initial test was conducted by exposing 4-day old host larvae to a pair of (one male and one female) parasitoids ad libitum. Immediately after adult parasitoid emergence, 4-day old FAW larvae (n = 25) were exposed to a pair of C. luteum for parasitism in 500 ml PET bottles (10.5 × 7.5 cm; Everpack) without maize leaves for 35 minutes. The PET bottles were covered with cotton wool for aeration and 100% honey was streaked on the internal walls as feed for the parasitoid. After the 35 minutes of exposure and observation, the parasitoids were transferred into new oviposition containers and held for the next day. Each day, a new set of 25 four-day old FAW larvae were introduced to the same set of parasitoids for 35 minutes, until the death of the female parasitoid. Any male parasitoid that died before the female was replaced, in case the female required multiple mating to maximise reproduction. The parasitised FAW larvae were placed individually into aerated plastic cups (80 ml) and fed with fresh young maize leaves as earlier described, until pupation or cocoon formation. This was replicated nine times. From the 6th day after parasitism, the parasitised larvae were observed twice daily to ensure accurate recording of developmental parameters. The parameters assessed were pre-oviposition period, oviposition period, post-oviposition period, egg to prepupal duration, pupal duration, sex ratio, number of offspring, and lifetime duration of ovipositing female.
Longevity of non-ovipositing adult C. luteum was determined by separating unmated male and female parasitoids immediately after emergence into 500 ml PET bottles and kept without mating. The parasitoids were provided with water and honey, as previously described and observed daily. The water and honey were replenished, when necessary, until the parasitoids died. The duration from emergence to death was recorded to estimate the longevity. A total of 18 males and 18 females were observed.
Statistical analysis
All the data were subjected to normality test using Shapiro–Wilk test. Data on the parasitism assay were normally distributed so they were subjected to one-way analysis of variance. Means of the different groups were separated using Student-Newman–Keuls post hoc test at 5% probability threshold. Host age preference data were analysed using a two-sample t-test with equal variances while other reproductive parameters such as lifetime parasitism, pre-ovipositing, ovipositing, post-ovipositing duration as well as longevity and duration of developmental stages of C. luteum were analysed using descriptive statistics. All the data were analysed using STATA/Standard Edition 17.0.
Results
Parasitism assay
The susceptible age of FAW for parasitism by C. luteum was studied in a no-choice experiment. C. luteum was able to parasitise first instar (3-day old) to third instar (6-day old) larvae of FAW with differences in parasitism among the various instars studied. The mean parasitism was highest in 4-day old larvae compared to other age groups (F 3;35 = 10.4; P < 0.001) (Table 1). However, there was no statistically significant difference in parasitism between 3-day old and 4-day old host larvae (F 3;35 = 10.4; P < 0.280). Susceptibility of host larvae to C. luteum parasitism decreased with increasing host age (Table 1). No parasitism or oviposition occurred when 7-day old larvae were exposed to the parasitoid and thus were excluded from the analysis.
Table 1. Parasitism (mean ± SD) of different instars of fall armyworm larvae by Coccygidium luteum under laboratory conditions for 35 minutes at 29 ± 1°C
Percentage parasitism of different ages of fall armyworm larvae by C. luteum expressed as percent of number of emerged parasitoid cocoon over total number of host larvae exposed to the adult parasitoid for oviposition. Means followed same letters are not statistically different at P = 0.05 probability level.
Host age preference
The preferences of C. luteum for different ages of FAW larvae were studied in choice experiments as shown in Table 2. C. luteum oviposited in both host ages in all the six combinations. Host age preference by C. luteum differed significantly in all the combinations except between 3-day and 4-day old larvae and between 4-day and 5-day old larvae. Significantly, 6-day old (3rd instar) larvae were less parasitised in all the age combinations they occurred in (Table 2). Three-day old larvae were preferred to 5-day and 6-day old host larvae when both were presented simultaneously. Similarly, C. luteum parasitised higher numbers of 4-day old larvae than 6-day old larvae when they were presented together (Table 2). C. luteum attacked more 3-day old larvae followed by 4-day old larvae. Consistent with results from host-age susceptibility, host age preference for oviposition by C. luteum decreased with increasing larval age, demonstrating that C. luteum has preference for early instars of host larvae.
Table 2. Host age preference of C. luteum when offered equal numbers of different ages of FAW larvae under laboratory conditions
Mean ± standard error of different host instars of fall armyworm larvae parasitised when introduced simultaneously to C. luteum. Means followed by same letters within same columns are not significant different at P = 0.05 probability level.
Longevity and reproductive parameters of C. luteum
Female C. luteum began ovipositing a few hours after emergence. Pre-oviposition period varied from 0 to 24 hours and with a mean of 0.38 ± 0.51 day (Table 3). Oviposition lasted for ca. 5 days (Table 3). No post-oviposition period was observed, as females continued to lay eggs until they died. Mean lifetime parasitism of the host larvae by C. luteum was 49.24 ± 24 (Table 3). Adult C. luteum survived for ca. 14 days with no significant difference in longevity of male and females (F = −0.887; P = 0.381) (Table 3). Progeny sex ratio was approximately 1.42 (Table 3). Generally, maternal age had no influence on number of female progenies except at 6-day old (t (12) = 0.70; P > 0.05; P = 0.013) (Fig. 1).
Figure 1. Influence of maternal age on the number of male and female progeny produced (n = 9). Female progeny was significantly higher at day 6 (P = 0.013). Parental males were made to mate with parental females in a separate 50 ml plastic vials for 24 hours prior to the females being exposed to FAW larvae. The asterisks * and ** represent no adult female emergence and single count respectively so no analysis was done.
Table 3. Reproductive parameters and longevity of Coccygidium luteum reared on fall armyworm at 28 ± 1°C
Mean duration of different reproductive parameters of C. luteum. N represents number of replications.
Life cycle
The mean developmental time of immature C. luteum from egg (oviposition) to cessation of feeding by the host was 8 days. The cessation of feeding to parasitoid grub (last instar of parasitoid larvae) egression from the host was 2 days. Thus, mean duration from oviposition to egression of final instar of the parasitoid larvae from the host cuticle was 10 days. From cocoon formation to adult parasitoids (wasp) egression lasted for 10 days (Table 4). Mean developmental period from oviposition to adult wasp emergence was 20 days (range 18–23) at a temperature of 28 ± 1°C (Fig. 2).
Figure 2. Life cycle of Coccygidium luteum reared on fall armyworm under laboratory conditions of 28 ± 1°C, 70 ± 5% R.H., and L12:D12 photoperiod.
Table 4. Duration of developmental stages of C. luteum from oviposition to pupal stage (n = 9)
Number of days for various developmental stages of C. luteum within fall armyworm larvae as the host under laboratory conditions of 28 ± 1°C, 70 ± 5% R.H., and L12:D12 photoperiod.
Discussion
The establishment of FAW in places outside of its origin is causing huge yield and economic losses to farmers (Abrahams et al., Reference Abrahams, Beale, Cock, Corniani, Day and Godwin2017a; Kassie et al., Reference Kassie, Wossen, De Groote, Tefera, Sevgan and Balew2020; Overton et al., Reference Overton, Maino, Day, Umina, Bett, Carnovale, Ekesi, Meagher and Reynolds2021; Tambo et al., Reference Tambo, Kansiime, Mugambi, Agboyi, Beseh and Day2023). This has necessitated the quest for sustainable management strategies that could be incorporated into integrated pest management. Coccygidium luteum, a koinobiont parasitoid, has been identified as a promising parasitoid that could help to reduce the damage caused by FAW (Agboyi et al., Reference Agboyi, Mensah, Clottey, Beseh, Glikpo, Rwomushana, Day and Kenis2019). In Ghana, it was among 10 parasitoid species identified as attacking FAW (Agboyi et al., Reference Agboyi, Goergen, Beseh, Mensah, Clottey, Glikpo, Buddie, Cafà, Offord, Day, Rwomushana and Kenis2020). This study has revealed important information about C. luteum that could be utilised for the integrated management of FAW.
After oviposition by C. luteum, parasitised FAW larvae become less active than non-parasitised FAW. This is likely as a result of the injection of symbiotic polydnaviruses or venoms from C. luteum which weakens the host (FAW) defences (Burke, Reference Burke2016; Kacsoh and Schlenke, Reference Kacsoh and Schlenke2012; Wang et al., Reference Wang, Ye, ZhouID, WuID, Hu, Zhu, Chen, HuguetID, ShiID, Drezen, HuangID and ChenID2021). More so, similar to the observation by Agboyi et al. (Reference Agboyi, Mensah, Clottey, Beseh, Glikpo, Rwomushana, Day and Kenis2019), parasitised larvae of FAW exhibited reduced growth rate and feeding compared to non-parasitised FAW. Parasitoid cocoon formation occurred within leaf tissues or beneath paper tissues placed in sauce cups. Exposed last instars of C. luteum larvae that emerged were dehydrated and died. In natural settings, the emergence of the final instars of C. luteum larvae from the host and subsequent cocoon formation likely occur in soil or plant debris.
In our study, C. luteum was able to parasitise and develop in three different larval instars (1st–3rd instars) of FAW. This indicates that C. luteum can parasitise different instars, specifically the early instar larvae of the host. This knowledge is crucial for establishing laboratory cultures of the parasitoid and mass rearing for biological control. It gives information on the susceptible host instar(s) of FAW for oviposition by C. luteum. Earlier studies, such as those on C. gregarium, suggested that Coccygidium spp. parasitise late instar larvae, which contrasts with our findings that C. luteum prefers early instar larvae (Sarmiento et al., Reference Sarmiento, Sharkey and Janzen2004). Our study provides new information that C. luteum prefers early instar larvae (i.e. 1st–3rd instars) of FAW. Both parasitism and preference tests in the present study demonstrated strong preference for early instar host larvae of FAW. Field collections of fourth to sixth instar FAW larvae yielded very few C. luteum, indicating low susceptibility of these late instar larvae to C. luteum attack. Furthermore, C. luteum was not able to parasitise late instar larvae of FAW when exposed to them in the laboratory. This may probably be because the host defence mechanisms might have been very active enabling them to deter the parasitoids or encapsulate them (Vinson, Reference Vinson and Iwantsch1980). Furthermore, the interaction between the age of a host and its acceptance for parasitism by parasitoids has been shown to vary between species (Queiroz et al., Reference Queiroz, Favetti, Hayashida, Grande, Neiva, Panizzi and Bueno2019). It has also been shown that some parasitoid species are able to parasitise multiple host instars (Harvey et al., Reference Harvey1994) while others prefer to parasitise single host instars (King, Reference King1998; Mattiacci and Dicke, Reference Mattiacci and Dicke1995). For example, the parasitoid Tamarixia radiata prefer late 4th–5th nymphal instars of the host Diaphorina citri (Sule et al., Reference Sule, Muhamad, Omar and Kah-Wei Hee2014). In a related study, the larval parasitoid, Cotesia marginiventris, demonstrated preference for the 2nd instar of the host S. litoralis (Hegazi and Khafagi, Reference Hegazi and Khafagi2024).
Our observation that C. luteum has preference for early instar larvae of FAW is good for biological control of FAW. This is because, preference for late instar larvae of FAW, would result in lots of damage to the maize plants by early instar FAW larvae before they are killed by the parasitoid in their late instar.
Coccygidium luteum was observed revisiting and ovipositing in previously parasitised hosts (superparasitism) under laboratory conditions. As a result, higher mortality was observed among 1st instar larvae after oviposition than other instars. This is supported by the fact that cannibalism among FAW larvae of same age is virtually absent in 1st and 2nd instars (Kasige et al., Reference Kasige, Dangalle, Pallewatta and Perera2022). In fact, the defence mechanisms of koinobiont parasitoids could be active and rely on the injection of venom proteins or a virus during oviposition, in order to compromise the immune system of the host (Asgari et al., Reference Asgari, Zareie, Zhang and Schmidt2003; Fang et al., Reference Fang, Wang, Gatehouse, Gatehouse, M., Chen, Hu and Ye2011; Yamanaka et al., Reference Yamanaka, Hayakawa, Noda, Nakashima and Watanabe1996). Multiple oviposition like the case of C. luteum may lead to overdose of venom, which could be lethal for the tiny first instar larvae of FAW. It is therefore presupposed that second instar larvae of FAW would be more suitable to be used in mass parasitism for biological control, as they were able to withstand superparasitism and exhibited very little to no cannibalism. The low parasitism of third instar FAW larvae by C. luteum may result from the larvae’s ability to ward off the parasitoid or encapsulate it. Studies have shown that encapsulation increases with host age (Brodeur and Vet, Reference Brodeur and Vet1995; Niogret et al., Reference Niogret, Sait and Rohani2009). The ability of C. luteum to parasitise early instars of the host larvae, coupled with the massive reduction in feeding by the parasitised larvae (Agboyi et al., Reference Agboyi, Mensah, Clottey, Beseh, Glikpo, Rwomushana, Day and Kenis2019) are desirable attributes making it a suitable candidate among larval parasitoids for augmentative biological control of FAW.
Lifetime parasitism rate of parasitoids is a major criterion for assessing their biological control potential. Parasitoids with high lifetime parasitism rates are advantageous in biological control as their parasitism rate facilitate rapid suppression of target hosts. The number of eggs a female FAW can lay in its lifetime is multiple folds higher than the number a female C. luteum can lay to parasitise larvae in its lifetime (Russianzi et al., Reference Russianzi, Anwar and Triwidodo2021). This notwithstanding, this study demonstrates that C. luteum can effectively parasitise a good number of host larvae. Observed lifetime parasitism may be influenced by the longevity of the parasitoid species (Souza et al., Reference Ueno2014) as well as the parasitoid’s ability to discriminate already parasitised hosts, thereby avoiding superparasitism and its associated egg wastage. Here, although the average longevity of virgin females of C. luteum was about 12 days, actual reproductive longevity under laboratory conditions was 7 days. This is in line with other studies on the negative effect of mating and oviposition on parasitoid longevity due to energy cost and resource allocation (Onagbola et al., Reference Onagbola, Fadamiro and Mbata2007). In the field, the crop environment and availability of preferred host instar among other factors could further influence the realised fecundity and effectiveness of C. luteum. It will be interesting to assess the potential fecundity of C. luteum which was not covered in this study. The variation in the mean development period of 20 days at 28°C to that observed by Agboyi et al. (2019) who reported a mean generation time of 16 days at 32°C was basically due to differences in the temperature at which the two experiments were conducted. Higher temperatures promote rapid developmental process and reduces developmental time hence the shorter developmental time observed at 32°C compared to 28°C.
Progeny sex ratio of parasitoids is influenced by several factors including maternal age. Indeed, several studies have demonstrated that sex ratio increase with maternal age (Santolamazza-Carbone et al., Reference Santolamazza-Carbone, Nieto and Rivera2007; Ueno, Reference Ueno2014). An earlier study has shown that the sex ratio in Campoletis chlorideae was lower when the female was mated just after emergence and became male biased as maternal age increased (Pandey et al., Reference Pandey, Tripathi and Tripathi2009). In this study, no influence of maternal age of C. luteum on progeny sex ratio was observed except on 6th day olds. The progeny sex ratio was highly variable and mainly male biased at the early stage. The highly male biased sex ratio at the early stage could be due to delay in fertilisation resulting in laying of unfertilised eggs and the fact that braconid parasitoids such as C. luteum exhibit haplodiploidy where unfertilised eggs develop into males.
In conclusion, this study provides vital information that can be utilised in exploring C. luteum for biological control. It also serves as a reference in future studies on other members of this untapped genus. Further studies are however needed to understand other biological parameters such as the determinants of sex ratio, release density, and frequency, that may influence the efficacy of C. luteum as a biological control agent.
Acknowledgements
This study was financially supported by the Foreign, Commonwealth and Development Office (FCDO), UK, the Directorate-General for International Cooperation (DGIS), Netherlands, the European Commission Directorate-General for International Cooperation and Development (DEVCO) and the Swiss Agency for Development and Cooperation (SDC) through CABI’s Plantwise Plus Programmes. CABI is an international intergovernmental organisation, and we gratefully acknowledge the core financial support from our member countries and lead agencies. See https://www.cabi.org/aboutcabi/who-we-work-with/key-donors/ for details.
We would like to thank the staff of biological control unit of the Plant Protection and Regulatory Services Directorate of the Ministry of Food and Agriculture Ghana for their support in maintenance of fall armyworm and parasitoid cultures and data collection.
Author contributions
Patrick Beseh: conceptualisation, design, experimentation, and writing of manuscript. Benjamin Mensah: review, editing, and supervision. John Abraham: review, editing, and supervision. Lakpo Koku Agboyi: data analysis, review, editing, and supervision.
Competing interests
We hereby declare that there is no conflict of interest that could have arisen from the work presented in this paper.
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