Advancing Sustainable Agriculture: Potential of Life Story Strategies of Solitary and Gregarious Microgastrinae Parasitoids (Hymenoptera: Braconidae) to Enhance Biological Control

Abstract

The life history strategies of solitary and gregarious Microgastrinae parasitoids are both valued for their potential in biological control, but they have rarely been directly compared to fully understand their roles in integrated pest management (IPM) programs. This paper provides a detailed comparison of these two strategies, focusing on critical traits, such as host specialisation, mating behaviour, and the mechanisms used to overcome host immune defences. Instead of treating these strategies holistically, the study isolates and examines each trait while also identifying synergistic interactions and their underlying causes. Key IPM success factors, including parasitism efficiency, host acceptance, and susceptibility to natural enemies, are defined to assess the effectiveness of each strategy. The results show that while gregarious parasitoids tend to have broader host ranges and higher fecundity, solitary parasitoids offer greater host specificity and reduced vulnerability to predators. Despite both strategies receiving similar overall performance scores, this study identifies monophagy as a particularly significant factor, offering insight into why some IPM programs succeed more effectively than others under seemingly identical environmental conditions. This study highlights host specificity and ecological adaptability as essential for effective, sustainable pest management, supporting the integration of both parasitoid types to enhance IPM efficacy.

1. Introduction

Parasitoid wasps have evolved distinct life history strategies for host utilisation. These strategies, particularly regarding the number of larvae developing within a single host, have diverged into two primary directions: solitary and gregarious parasitism. In solitary parasitism, a single parasitoid larva develops and feeds on the host, while in gregarious parasitism, multiple larvae develop concurrently within the host, sharing its resources [1]. The ancestral life history mode was probably solitary, whereas the gregarious development evolved several times [2,3]. Therefore, solitary species are predominant among the majority of living species today [2]. In gregarious species, the siblings exhibit a certain level of tolerance, allowing for multiple individuals to successfully develop. In contrast, larvae of solitary species are intolerant of each other and often engage in siblicide, resulting in the survival of only one individual [4]. Notably, most solitary endoparasitoids possess first instar larvae with heavily sclerotised head capsules and large, sickle-shaped mandibles, which are specifically adapted for combat against competing parasitoid larvae [5]. Rare cases of siblicide behaviour have also been reported in typically gregarious species, such as the braconid Cotesia vanessae (Reinhard) developing within the noctuids Trichoplusia ni (Hübner), Mythimna unipuncta (Haworth), and Helicoverpa zea (Boddie) [6]. It is suggested that this behaviour reflects a trade-off between the limited resources within the host, the number of eggs laid, and the optimisation of resource use. In such cases, siblicide enables self-regulation of brood size when host resources are insufficient to support the development of all initially laid eggs.

Based on their life history strategies and biology, parasitoids can be classified as either idiobionts or koinobionts [7,8]. Another key distinction refers to the location of the wasp larval development, with parasitoids developing externally on the host body termed ectoparasitoids, while those developing internally are known as endoparasitoids (e.g., [7,8]). Most idiobionts exhibit ectoparasitism, which attacks and induces long-term paralysis in their hosts, preventing further growth and development after parasitisation [9]. The parasitoid larva then feeds externally on the immobilised host until its development is complete (e.g., Chalcididae, Torymidae, Perilampidae, but also Braconidae and Ichneumonidae). In contrast, koinobionts, which are typically endoparasitoids, lay their eggs inside the host, allowing it to continue their development after parasitisation. Co-development of both the host and the parasitoid is often highly synchronised and influenced by environmental factors. Koinobiont endoparasitoids may temporarily paralyse their host during egg insertion, but the host remains alive and continues to develop during the parasitoids’ early stages, often until the adult wasps emerge. Families such as Agaonidae, Braconidae, Ichneumonidae, Chalcididae, Encyrtidae, Eulophidae, Pteromalidae (sensu lato), and Trichogrammatidae include many koinobiont endoparasitoids.

Solitary parasitism is common in many Hymenoptera families, including Braconidae, Chalcididae, Cynipidae, Ceraphronidae, Drynidae, Ichneumonidae, Stephanidae, as well as Eulophidae and Pteromalidae. Within the Braconidae subfamilies, solitary parasitism is consistently observed in endoparasitic koinobionts, such as Acampsohelconinae, Agathidinae, Amicrocentrinae, Aphidiinae, Brachistinae, some Braconinae, Cardiochilinae, Cenocoeliinae, Charmontinae, Cheloninae, Dirrhopinae, Ecnomiinae, Gnamptodontinae, Helconinae, Homolobinae, Ichneutinae, and many Microgastrinae, Miracinae, Opiinae, and Zelinae. Also, solitary parasitism is found in the ectoparasitic idiobionts subfamily Exothecinae ([10,11], but also see [12]). In subfamilies that are predominantly ectoparasitic idiobionts, such as Braconinae, most Doryctinae, and Rogadinae, as well as in the endoparasitic koinobiont subfamily Alysiinae, solitary parasitism is predominant, though there are a few exceptions.

Gregarious species are more frequently found among endoparasitic koinobiont subfamilies, such as Euphorinae, Sigalphinae, Histeromeriinae (now part of Rhyssalinae, according to [13]), some Macrocentrinae, and many Microgastrinae. In ectoparasitic idiobionts, gregariousness has been recorded in some Rogadinae and Hormiinae, as well as in ectoparasitic koinobionts from Rhysipolinae. Information on other subfamilies, such as Pambolinae or Meteorideinae, is currently limited. Among Braconidae, gregariousness in the subfamily Macrocentrinae is uniquely a result of polyembryony, where multiple individuals develop from a single egg [14]. In all other listed subfamilies, gregariousness arises as a consequence of superparasitism. In Ichneumonidae, the sister group of Braconidae, gregariousness among endoparasitic koinobiont species is rare [15].

Microgastrinae are recognised as one of the most species-rich subfamilies within Braconidae and represent one of the most diverse groups of all animals in general [16]. Primarily, they are koinobiont endoparasitoids of lepidopteran larvae. While oviposition in the egg stage does occur in some species, it is an exception within this subfamily, whereas parasitism of the pupae and adults is not documented [11]. Roughly half of Microgastrinae species (in cases in which the biology is known) exhibit gregarious development, a trait that has likely evolved independently in many genera, predominantly in Cotesia Cameron, Diolcogaster Ashmead, Glyptapanteles Ashmead, as well as in Apanteles Förster, Microplitis Förster, and many others. Typically, the eggs oviposited in one host originate from a single female and are deposited in a single insertion; however, some species have been reported to oviposit multiple times [17]. Offspring emerging from the same host are generally referred to as a brood. Depending on the parasitoid species and the ‘carrying capacity’ of the host, brood size in gregarious species can range from ten to a few hundred individuals. In contrast, Microgastrinae targeting smaller hosts, such as stem or leaf miners, are predominantly solitary, e.g., Buluka de Saeger, Pholetesor Mason, Choeras Mason, Rasivalva Mason, Napamus Papp, etc.

According to historical references (compiled in [18]), the ratio of solitary to gregarious parasitism within the subfamily Microgastrinae appears to be approximately equal, at least in some genera, where relatively comprehensive data are available (e.g., [19,20]).

This study discusses representative examples of successful integrated pest management (IPM) practices involving some of the 3000+ species of Microgastrinae worldwide. It includes detailed evaluations of relevant literature presenting significant laboratory experiments on parasitoids, targeting both autochthonous and allochthonous hosts, to identify and select promising candidates for biological control. Additionally, a comparative analysis of solitary and gregarious parasitoids is conducted to outline the advantages and disadvantages of each type for use in IPM programs. The primary objective is to determine which life history strategy, solitary or gregarious, is better suited for IPM implementation in various contexts. By assessing these parasitoid traits across multiple categories, this study seeks to ascertain which approach is more effective under specific conditions, with the hope of facilitating informed decisions in pest management strategies. Thorough understanding of the biology of biological control agents (BCA) benefits researchers, practitioners, and policymakers in the agriculture domain. Promoting more sustainable, customised pest control methods, an overview of all relevant factors will provide essential guidance, supporting the effective adaptation and implementation of these strategies, and thus development of environmentally friendly practices that reduce reliance on chemical pesticides and align with long-term agricultural sustainability goals.

2. Selection of Biological Control Agents for IPM Programs

Biological control involves the use of natural enemies, such as predators, parasites, parasitoids, and pathogens, to regulate pest populations, thereby reducing their impact on crops and ecosystems of human interest [21]. The exceptional species richness and significant ecological role of Microgastrinae make them ideal candidates for inclusion in biological control experiments and pest management programs. Due to their great diversity, abundance, host range, and broad distribution, microgastrines are especially important in controlling lepidopteran pest populations, particularly from species-rich families, such as Geometridae, Noctuidae, and Tortricidae, which also include many agricultural and forestry pests worldwide. Microgastrinae are usually highly host-specific, with many species being specialists that target only one or a few closely related host species (e.g., [22]). This specificity makes them suitable for targeted pest management. Consequently, IPM programs often rely on Microgastrinae to reduce the need for chemical pesticides, promoting sustainability in agroecosystems. In the following section, we present several examples of the study and use of microgastrine parasitoid wasps in the biological control of economically important caterpillar pests across all biogeographical regions.

The cosmopolitan Apanteles carpatus (Say) is a solitary parasitoid of larvae from the Tineidae family (Lepidoptera), targeting species such as the webbing clothes moth Tineola bisselliella (Hummel) and the case-making clothes moth Tinea pellionella L. [8,23]. This parasitoid reproduces exclusively through obligatory parthenogenesis (thelytoky), producing only females [24]. This mode of reproduction, combined with its ability to complete development across all larval stages of T. bisselliella, makes A. carpatus an ideal candidate for biological control, and studies have been conducted to determine the optimal host age for oviposition, reproductive rate and capacity, host preference, and other biological traits [24]. To enhance clarity, the following sections will transition from cosmopolitan examples to region-specific examples of pest control strategies.

2.1. Europe

Kaiser et al. [25] introduced a newly described African species, the gregarious Cotesia typhae Fernández-Triana, to Mediterranean Europe. This wasp is capable of parasitising both African and European populations of Sesamia nonagrioides (Lefèbvre), a major Noctuidae pest affecting maize in Africa and Mediterranean Europe. The species was distinguished from C. sesamiae (Cameron), another parasitoid of the same pest, based on detailed morphological, molecular, ecological, and geographical analyses, and notable reproductive isolation. In related research, Kaiser et al. [26] underscored the utility of both C. typhae and C. sesamiae as BCA, particularly highlighting C. typhae’s ability to adapt across diverse geographic regions and significantly mitigate the impact of S. nonagrioides on corn crops.

Kenis and Li [27] proposed the introduction in Europe of the gregarious Dolichogenidea stantoni (Ashmead) as a potential biological control agent to target the box tree moth Cydalima perspectalis (Walker) (Crambidae), a significant pest that dominantly feeds on various species of Buxus L. This parasitoid was selected due to its effective parasitism rates on the larvae of the box tree moth in its native Asian habitats, showing promise for controlling the rapidly spreading pest in other regions.

2.2. America

Several examples of biological control in North America involve the management of Spodoptera frugiperda (J.E. Smith) (Noctuidae), a significant worldwide pest that impacts corn cultivation, especially across the southern, central, and eastern regions of the United States [28]. The effectiveness of biological control strategies against this pest has been well documented, notably in a detailed study by Meagher et al. [29], in which Cotesia marginiventris (Cresson), a solitary parasitoid, has proven highly effective, significantly reducing populations of the pest. The study of parasitoids of this pest in Mexico [30,31] observed a low percentage of parasitism by the gregarious parasitoid, Glyptapantels militaris (Walsh), compared to the other parasitoids. Other Microgastrinae parasitoids that have been used or considered for the biological control of S. frugiperda, either in North America or other regions, are listed in the work of Wyckhuys et al. [28].

The gregarious parasitoid Cotesia glomerata (L.) and the solitary Cotesia rubecula (Marshall) have been introduced to the USA to control the small white butterfly Pieris rapae (L.) (Pieridae), which is also an introduced species. Cotesia glomerata was initially introduced from Europe in 1883 [32] and, subsequently, five more times, although it did not control the targeted pest as expected. Cotesia rubecula was first introduced to the USA in 1988, but it was not until the introduction of a strain from China that a significant reduction in the population density of Pieris rapae was achieved [33]. In 2012, Apanteles opuntiarum Bertha & Martínez, a gregarious parasitoid of the cactus-feeding moth Cactoblastis cactorum (Berg) (Pyralidae), was described from Argentina and recognised as a highly host-specific parasitoid [34]. Subsequently, in 2013, a classical biological control program was initiated in the USA using this wasp to control lepidopteran cactophagous pests attacking Opuntia Mill. plants, with minimal risk to non-target species [35]. This chronological sequence illustrates the careful assessment and implementation process in biological control initiatives. It is important to note that while C. cactorum was initially introduced to the Caribbean to serve as a biological control agent for native Opuntia species, it subsequently became an invasive species in the region [36].

The gregarious Cotesia flavipes (Cameron) was introduced to combat the invasive sugarcane borer, Diatraea saccharalis (F.) (Crambidae), and its release aimed to achieve high levels of parasitism, significantly reducing the borer population through augmentative releases [37]. This approach proved successful in controlling the sugarcane borer and has been replicated in different regions to effectively manage pest populations. The successful establishment and long-term control of C. flavipes host populations within a short period has dramatically decreased sugar cane infestation rates [38].

Two Microgastrinae, the solitary Microgaster messoria Nees and the gregarious Glypthapanteles thomsoni Lyle, were introduced from Europe to America with the aim of controlling populations of the European corn borer, Ostrinia nubilalis (Hübner) (Crambidae) [39].

The solitary Diolcogaster claritibia (Papp), an important parasitoid of the diamondback moth, Plutella xylostella (L.) (Plutellidae), was recently reported from North America [40]. Originally from the Palearctic region, this species may have been accidentally introduced to Canada, suggesting its potential for widespread distribution across both the Palearctic and Nearctic regions.

The biology of two braconid parasitoids, the solitary Apanteles polychrosidis Viereck and the solitary, facultatively gregarious Macrocentrus linearis (Nees) (Macrocentrinae), was studied by Cossentine et al. [41]. These parasitoids attack the oblique banded leafroller, Choristoneura rosaceana (Harris), and the three-lined leafrollers, Pandemis limitata (Robinson), both Tortricidae pests in organically managed apple orchards. Macrocentrus linearis was observed to parasitise early to mid-instar leafrollers but did not accept a sympatric leafroller species as a host. In contrast, A. polychrosidis parasitised both the oblique banded and three-lined leafrollers across several instars, showing a preference for cooler temperatures, which also led to higher parasitism rates. The study highlighted differences in host specificity, survival, and impact on host feeding between the two parasitoids, providing insights for their potential use in biological control programs.

The solitary Diolcogaster flammeus Salgado-Neto & Fernández-Triana was described as a potentially important biocontrol agent of Agaraea minuta Schaus (Erebidae), a pest of the economically important Costus spicatus (Jacq.) Sw. and C. spiralis (Jacq.) Roscoe var. spiralis from the Brazilian Atlantic Rainforest, known for their pharmacological, medicinal, and ornamental values. Studies have highlighted the biological and ecological aspects of this interaction, noting a high parasitism rate of approximately 90% in field conditions, significantly reducing the pest population and contributing to the understanding of natural pest control mechanisms within their native ecosystem [42,43].

2.3. Asia

Gupta [44] mentions four Microgastrinae species that were introduced to India, of which only one was successfully established, while the others were not detected after introduction. Among the newly recorded wasp species that could be utilised for IPM in India are Apanteles mamitus Nixon, a solitary endoparasitoid parasitoid on larvae of Spoladea recurvalis (F.) (Crambidae) found on Amaranthus sp., and Apanteles javensis Rohwer, a gregarious parasitoid of Pleuroptya balteata (F.) (Crambidae) found on the cashew leafroller, Anacardium occidentale L.

The solitary parasitoid, Microplitis bicoloratus Chen, targeting the cotton leafworm Spodoptera litura (F.) (Noctuidae), was studied in China [45]. This parasitoid was the first Microgastrinae to be successfully reared and assessed in a laboratory setting as a potential biological control agent for this pest. Two gregarious parasitoids, Parapanteles hyposidrae (Wilkinson) and Protapanteles immunis (Haliday), were studied by Wang et al. [46] as potential biological control agents against the tea grey geometrid, Ectropis grisescens Warren (Geometridae). Long and Dzung [47] described a new solitary species, Cotesia clethrogynae Long, which could potentially be used as a biological control agent for managing populations of Clethrogynae turbata Butler (Lymantriidae), a significant pest of cabbage in Vietnam. Additionally, Dolichogenidea persica, a new species with potential for biological control against Leucoma wiltshirei Collenette (Erebidae), was described by Abdoli et al. [48].

2.4. Africa

The solitary Cotesia icipe Fernández-Triana & Fiaboe was described from Kenya and considered for its potential use in the biological control of two significant Noctuidae pests of Amaranthus sp., Spodoptera littoralis (Boisd.) and S. exigua (Hübner) [49]. Subsequently, Agbodzavu et al. [50] focused on the host range of C. icipe across the five most common lepidopteran defoliators of amaranth and found that it successfully parasitised (up to 95%) the two noctuid pests, but it was unable to parasitise the other three species, Herpetogramma bipunctalis (F.), Spoladea recurvalis, and Udea ferrugalis (Hübner), all of which belong to the Crambidae family and are associated with amaranth plants. Conversely, the solitary Apanteles hemara Nixon has been proposed as a biological control agent against amaranth leaf-webbers across Africa [51], as it was found to successfully parasitise two of the crambid pests (S. recurvalis and U. ferrugalis) that C. icipe did not attack. These studies emphasised the importance of conducting studies on parasitoid biology and ecology before successful programs can be implemented.

The solitary Apanteles xanthostigmus (Haliday) has been studied in Egypt as a potential biological control agent targeting Prays oleae (Bernard) (Lepidoptera: Yponomeutidae), a prevalent pest in olive orchards [52].

The solitary parasitoid Dolichogenidea gelechiidivoris (Marsh), one of the most important biocontrol agents of the South American tomato pinworm Tuta absoluta (Meyrick) (Gelechiidae), was subsequently reported from Europe (Spain) and Africa (Algeria), from tomato grown in open fields and greenhouses [53,54]. This case exemplifies a parasitoid that has been moved, apparently accidentally, with its host from the Neotropical to the Palaearctic and Afrotropical regions.

2.5. Oceania

One of the few native species used for biological control in Australia is Dolichogenidea tasmanica Cameron, a solitary parasitoid that targets the light brown apple moth, Epiphyas postvittana (Walker) (Tortricidae) [55,56]. In the Australian fauna, the genus Cotesia is represented by 21 species [57], of which four species, all of them solitary parasitoids, were introduced as biological control agents: C. glomerata, C. kazak (Telenga), C. rubecula, and C. vestalis (Haliday). Another species introduced to Australia was Apanteles subandinus Blanchard, a solitary parasitoid of the potato tuber moth, Phthorimaea operculella (Zeller) (Gelechiidae) [58]. Additionally, A. subandinus became widespread in South Africa after its release from 1965 to 1969 to enhance the biological control of P. operculella [58].

Research conducted in Pakistan on the parasitoids of the noctuid larvae of Mythimna separata (Walker) and several species of the genus Agrotis Ochsenheimer aimed to identify parasitoid species suitable for introduction to New Zealand to control the same pests. Mohyuddin & Shah [59] documented several parasitoid species, among them the gregarious Cotesia ruficrus Haliday, which demonstrated the highest parasitism rate, particularly on M. separata, leading to significant economic benefits. Interestingly, while C. ruficrus was already present in New Zealand, it had not previously been found to parasitise M. separata until the introduction of the strain from Pakistan. The success of the Pakistani strain of C. ruficrus in parasitising M. separata has spurred considerable interest among experts in IPM [60,61].

In 2010, the Environmental Protection Authority of New Zealand approved the release of Cotesia urabae Austin & Allen, a solitary parasitoid from Australia, as a control agent for the gum leaf skeletoniser, Uraba lugens Walker (Nolidae), in New Zealand [62].

3. Life History Strategies of Solitary and Gregarious Microgastrinae

Life history strategies shared by both solitary and gregarious Microgastrinae are numerous, but there are also some that are more specific. Parasitoids from both groups share the ability to directly exploit the host and its behaviour to enhance their survival chances. This direct exploitation includes the host’s ability to actively defend emerging parasitoid larvae and later pupae from enemies [63]. Additionally, parasitoids indirectly benefit from the shelters provided by their hosts.

Although 82 genera of Microgastrinae have been described so far [64,65], detailed biological information for a vast number of species is still lacking. Genera with high species richness and predominantly cosmopolitan distribution have been observed to employ both reproductive strategies, with some species being solitary and others gregarious. In certain genera, only one strategy has been observed. For example, all species within the genera Choeras or Pholetesor are solitary endoparasitoids, while known species of Paroplitis Mason are exclusively gregarious.

3.1. Comparative Analysis of Parasitoid Behaviour

3.1.1. Host Range

The host range of parasitic wasps varies widely, encompassing a spectrum from a single host species to multiple hosts across different genera or even families. Depending on their host specificity, species can be classified as monophagous, oligophagous, or polyphagous. In many cases, particularly among koinobiont parasitoids, the host range is restricted to a limited number of species. This restriction is often due to the endoparasitic nature of many koinobionts, necessitating specialised mechanisms to overcome the host’s immune defences (e.g., [9,66]).

In the subfamily Microgastrinae, a similar pattern of specialisation is observed. Although the literature occasionally reports extremely polyphagous species, recent findings suggest that such reports may be the result of host misidentifications [67,68]. Generally, Microgastrinae parasitoids exhibit a host range confined to a specific lepidopteran family, tribe, or even genus. Recent studies incorporating morphological, molecular, and ecological data have revealed a higher degree of specialisation among Microgastrinae than previously recognised, attributable to an overly broad species concept (e.g., [69]).

According to the literature, solitary parasitoids generally tend to have a narrower host range, often behaving as specialists compared to gregarious species. For example, in Microgastrinae, Cotesia rubecula, a solitary parasitoid, exhibits a more specialised host range when compared to its gregarious relative C. glomerata [70]. However, laboratory experiments comparing Aphaereta genevensis Fischer (solitary) and A. pallipes (Say) (gregarious) (Braconidae; Alysiinae) on multiple Drosophila Fallen species showed similar parasitisation success across hosts, with no significant difference in the host range [71]. While solitary species may sometimes specialise on fewer hosts, these findings suggest that host range differences between solitary and gregarious parasitoids are not universal and may depend on specific ecological and physiological factors, such as host body size or host defence mechanisms. Even if the gregarious Microgastrinae are characterised as generalists, their host range is limited to a few species of lepidopterans of a single genus or family. For instance, a phylogenetic lineage of gregarious Cotesia species that produce ball-like mass cocoons is associated predominantly with the Noctuidae family. This lineage includes species such as C. tibialis (Curtis), C. berberis (Nixon), C. trivaliae Žikić & Shaw, C. vanessae, C. xylina (Say), and C. yakutatensis (Ashmead), which primarily parasitise lepidopterans of the subfamily Noctuinae, particularly those from the tribes Noctuini, Leucaniini, and Orthosiini. Conversely, their relative C. ofella (Nixon) is mainly associated with the noctuid subfamily Acronictinae [72].

Among solitary parasitoids, there are instances where a broader host range is observed. For example, Cotesia margiventris (Cresson) has been documented to parasitise dozens of lepidopteran species, particularly from the Noctuidae family [73]. In studies of intrinsic competition, De Moraes and Mescher [74] found that the generalist C. margiventris outcompeted the more host-specific Microplitis croceipes (Cresson) when oviposition occurred simultaneously. M. croceipes is known as a parasitoid of Helicoverpa armigera (Hübner), H. zea, and Heliothis virescens (F.).

The ecology of parasitoid species plays a crucial role in defining their host range. In terms of voltinism, species may be either plurivoltine or univoltine. Plurivoltine species produce multiple generations per year and often exploit different hosts throughout the year, resulting in a broader host range. For instance, Nixon [75] observed colour variations in the cocoon masses of the gregarious C. tibialis between early and late summer, potentially reflecting the use of different hosts in different seasons. In contrast, univoltine species, which produce only one generation per year, tend to have a narrower host range and are often solitary, e.g., several species of Microgaster (M. fulvicrus Thomson, M. luctuosa Haliday, and M. nervosae Shaw) are univoltine and parasitise species from the genus Agonopterix Hübner (Depressariidae), with the majority of species in this genus being solitary parasitoids [76].

3.1.2. Host Acceptance

Following emergence and copulation, a female parasitoid must locate a suitable host for oviposition. The process of host acceptance involves evaluating whether the identified host is of the correct species and assessing its suitability for egg deposition. Host suitability can range from optimal to marginal, with varying likelihoods of acceptance by the parasitoid [77]. Time-limited parasitoids are more likely to accept less suitable hosts, while egg-limited parasitoids tend to reject them [78].

Parasitoid species with shorter lifespans may lay eggs in moderately or poorly suitable hosts due to the constraints of limited time for host searching. For example, Microplitis rufiventris (Kok.), a solitary parasitoid of several Spodoptera Guenée species, primarily oviposits in the first larval instar (L1) to third larval instar (L3) of Spodoptera littoralis, when the larvae are still clustered near the eggs. Oviposition in later larval instars (L4–L6) was not observed, likely due to the risk of injury to the parasitoid and the reduced ability of its offspring to overcome the host’s immune defences [79,80]. In contrast, the gregarious parasitoid Cotesia vanessae prefers to oviposit in L4 or later larval instars [81].

Comparative studies of two congeneric and sympatric Cotesia species, C. glomerata, a gregarious parasitoid, and C. rubecula, a solitary parasitoid, have demonstrated differing behaviours in host species acceptance and larval stage preference. Cotesia glomerata is a generalist parasitoid that targets several Pieris species, including P. brassicae (L.), P. napi (L.), and P. rapae, as well as other species from Pieridae, such as Aporia crataegi (L.), Pontia daplidice (L.), etc. [18]. In contrast, C. rubecula specialises on P. rapae and exhibits greater specificity in host selection. It was found that C. glomerata exhibits greater plasticity in host acceptance compared to C. rubecula, equally attacking L1, L2, and L3 in all three Pieris species. In no-choice tests, host acceptance by C. rubecula was higher for P. rapae, as females oviposited in all offered larval instars (L1–L6). However, when offered larvae of the other two Pieris species, females only accepted L1 [70]. The same group of authors indicated that the success of oviposition is also influenced by the defensive behaviour of the host, with older, larger hosts exhibiting reduced parasitism rates.

Host sizes must be carefully managed, as they should not become too large or too small. Thus, most solitary endoparasitoids of macrolepidopteran hosts have likely evolved to regulate host growth to meet their nutritional needs, regardless of their phylogenetic background [82]. However, this pattern may not apply to Cotesia vestalis, which targets small microlepidopteran hosts, such as Plutella xylostella, where the caterpillars must nearly reach full size to satisfy the parasitoids’ minimal nutritional requirements.

3.1.3. Egg-Laying Capacity

The exact number of eggs laid by a female Microgastrinae varies among species, but also among individuals of the same species. The fecundity and egg-laying capacity of female solitary and gregarious parasitoids vary significantly due to their distinct reproductive strategies and ecological niches. It ranges from a few dozen to several hundred eggs produced during the female’s lifetime. Certain species within the genus Cotesia exhibit remarkably high reproductive potential, with females capable of laying hundreds of eggs. For example, C. congregata (Say), a parasitoid of the tobacco hornworm, Manduca sexta L. [83], can produce broods ranging from 50 to over 200 individuals per host [84]. Harvey et al. [85] reported that C. congregata females lay between 20 and 300 eggs per host. In contrast, solitary parasitoids, such as Microplitis rufiventris, which parasitise Spodoptera littoralis, have been observed to have an average egg load of approximately 57 to potentially 70 eggs per female [86]. Hegazi and colleagues also noted that the egg load per female varies based on the availability of host and food resources. In the absence of food, potential fecundity is significantly lower compared to females fed with honeydew. Conversely, an increase in available hosts leads to a decrease in potential fecundity, independent of food resource availability. In comparing the maximum egg load between Cotesia and Microplitis, Harvey et al. [87] observed a smaller egg capacity in the predominantly solitary species of Microplitis studied, as compared to the mostly gregarious Cotesia species.

Iwasa et al. [88] explored the optimal oviposition strategies of parasitoids, considering the effects of mortality and egg limitation on host range and oviposition behaviour, to maximise their lifetime reproductive success. According to their theory, solitary parasitoids are more cautious and prefer safer hosts (lower risk of dying while laying eggs). If they have many eggs left and do not face high mortality while laying eggs, they will use a broader range of hosts. However, the balance between the risk of dying and the number of eggs they have affects their choices. Gregarious parasitoids hesitate less in host selection since they lay multiple eggs per host anyway.

3.1.4. Oviposition Speed

The speed of oviposition in parasitoids has not been extensively studied, although Godfray [66] provided detailed information on the oviposition behaviour of various parasitoids. In essence, it is important for the parasitoid to lay its egg/s as quickly as possible, preventing the host from mounting a defence or attempting to escape. Generally, the oviposition speed varies significantly among species, irrespective of the parasitoid group and the host’s ecology, i.e., whether the host is exposed or concealed. It can be inferred that the oviposition speed differs between solitary and gregarious parasitoids. Observations from existing studies suggest that gregarious parasitoids tend to oviposit more quickly, as they lay multiple eggs per host. It is likely that this extended oviposition duration could increase the likelihood of attracting predators. In contrast, solitary parasitoids typically take more time during oviposition, as they are more selective when laying a single egg per host. Since precise data on the time parasitoids spend ovipositing within hosts are lacking, it is not possible to favour one group over the other based on oviposition speed alone.

3.1.5. Overcoming the Host’s Immune System

Host manipulation is a strategy used by parasitoids to ensure the development of their offspring at the expense of their host. This can be achieved through various mechanisms, such as neuroimmunological responses, genomic changes, encapsulation, and the involvement of endosymbionts. Gregarious parasitoids employ the strategy of laying large numbers of eggs per host, often exceeding the optimal number, to increase the likelihood that as many offspring as possible will survive the host’s immune response. As Hervet et al. [6] stated in their paper, “flooding” the host with eggs induces multiple physiological changes, allowing the parasitoid female to fully exploit limited host resources, regardless of host size. This strategy may also enhance the offspring’s ability to compete with other larvae of the same or different parasitoid species in cases of super- or multiparasitism occurring simultaneously within the host body [6].

The physiological changes induced in the host by solitary parasitoids are less understood. However, the solitary struggle of a single egg or larva against the host’s immune system is certainly challenging. Mohan and Sinu [89] conducted experiments on the solitary parasitoid Microplitis pennatulae Ranjith & Rajesh, a natural enemy of Psalis pennatula F. (Erebidae), and suggested that the polydnavirus (injected by the female wasp when ovipositing) effectively defends the parasitoid larva by inducing multiple physiological changes in the host, similar to the effects observed in hosts of gregarious parasitoids.

The mutualistic relationship between Microgastrinae and polydnaviruses (PDVs) exemplifies a conspicuous case of coevolution. All Microgastrinae, both solitary and gregarious, possess PDVs [90]. During the oviposition act, Microgastrinae inject their eggs along with PDVs into the host’s caterpillar cells. The viruses infect the nuclei of the host’s cells, leading to the expression of virus-encoded genes and the production of defensive protein particles [16]. These products serve to compromise the host’s immunity, preventing it from killing the parasitoid larvae, and to alter the caterpillar’s metabolism and growth, promoting parasitoid development.

3.1.6. Host Instar Attacked

Microgastrinae parasitoids, both solitary and gregarious, exhibit preferences for specific host instars, which can be linked to their reproductive strategies and the developmental requirements of their larvae (i.e., [91,92]).

Solitary parasitoids typically prefer younger host larval instars for oviposition. This is because younger larvae are less likely to mount strong immune responses and provide a longer developmental period for the parasitoid larva. Generally, larvae that develop in very small-sized hosts, such as early instars, often encounter a scarcity of nutrients. Consequently, they must delay their development until the host has grown sufficiently. It is crucial that the host remains alive until it can supply adequate nutrition for the parasitoid to attain a minimum viable body size necessary for survival [91,92]. Examples within Microgastrinae include Glyptapanteles porthetriae (Muesebeck), which primarily targets L2 of Lymantria dispar L. caterpillars, rarely L3 or L4 [93], Cotesia kazak, which prefers L1 and L2 of the tobacco budworm Heliothis virescens larvae [94,95], and Microplitis pallidipes Szépligeti, which attacks L2 of Spodoptera litura [96]. Another solitary parasitoid, Microplitis croceipes, prefers L2 and L3 of H. virescens [97], although it can, under laboratory conditions, successfully parasitises all five larval instars [98]. Usually, Apanteles galleriae Wilkinson parasitises L2 and L3, but it has been observed that it can also parasitise L1 and L4 of Galleria mellonella (L.) under laboratory conditions [99].

Gregarious microgastrines show more flexibility in their host larval instar selection. For example, Cotesia glomerata typically targets early larval stages, preferring L1 and L3 of Pieris brassicae and P. rapae, respectively [100]. On the other hand, Cotesia flavipes prefers later instars, such as L3 to L6 of Diatraea saccharalis [101]. This strategy maximises the use of host resources while balancing the risks of host immune defences and the benefits of ensuring the successful development of multiple larvae.

3.1.7. Host Instar Preference for the Emergence

For many insects, including parasitoids, rapid development is crucial early in the season when populations are growing and competition for resources is fierce [66]. Microgastrinae species exhibit distinct preferences for emerging from specific host instars, tailored to their developmental needs and the resource availability of the host. Generally, gregarious species target late instar larvae, maximising the use of the host’s size to enhance the survival prospects of numerous parasitoid individuals. These late-instar hosts may exhibit behaviours manipulated by parasitoids, such as altered feeding patterns or constructing protective shelters, which indirectly benefit the developing parasitoids. For example, Cotesia glomerata emerges from fully grown hosts of Pieris brassicae [102,103], Microplitis demolitor Wilkinson from L4 and L5 of Heliothis virescens [104], and Glyptapanteles liparidis (Bouché) from late larval instars of Lymantria dispar [105].

Contrary to gregarious species, solitary Microgastrinae typically favour emerging from early instars to avoid intense competition and minimise damage to the host. For instance, Glyptapanteles porthetriae generally emerges from L2 of Lymantria dispar, less frequently from L3 or L4 [93]. There are some exceptions among solitary parasitoids, including those that parasitise Microlepidoptera. For example, Apanteles fumiferanae Viereck, which parasitises the spruce budworm Choristoneura fumiferana (Clemens) (Tortricidae), emerges from its L4 instar [106,107]. Another example is Pholetesor ornigis (Weed), which parasitises L1–L3 of the apple leaf miner Phyllonorycter blancardella (F.) (Gracillariidae) in the field, but under laboratory conditions, it oviposits and emerges from L4 or even L5 [108].

3.1.8. Exposure to Natural Enemies

Some caterpillars, especially from the Microlepidoptera group, live in shelters, e.g., Choreutidae, Coleophoridae, Elachistidae, Gracillariidae, or Tortricidae. Primarily, shelters are made of leaves or various plant organs and tissues, made of silk, or they are simply leaf mines. Microgastrinae that target concealed hosts usually possess elongated ovipositors, as seen in the genera Apanteles, Dolichogenidea Viereck, Sathon Mason, Pholetesor, Iconella Mason, Choeras, Microgaster, etc., enabling them to reach the host. Pupating within the host’s shelter undoubtedly offers camouflage and protection to the wasps from other potential enemies, making it challenging for them to locate the parasitoid pupa.

Although endoparasitoid larvae are hidden in the host’s body, the host itself can be more or less exposed to various natural enemies, primarily predators and hyperparasitoids. However, the rate of exposure to enemies for solitary and gregarious parasitoids varies based on several ecological factors, including their life history strategies, host interactions, and environmental conditions. Certainly, the amount (number) of parasitoids per host has a significant role in attractiveness for other natural enemies. The clustering of parasitoid larvae can be more easily detected as a consequence of the emission of kairomone in a higher concentration. Additionally, the large size and exposure of hosts typically parasitised by gregarious parasitoids, especially those in the families Sphingidae, Saturniidae, and others, increase the risk of easy detection by predators and hyperparasitoids [16].

In contrast, it has been observed that some parasitoid species, particularly those attacking low-feeding noctuids, such as Cotesia tibialis and its close relatives, manipulate their caterpillar hosts to move towards the tops of plant stems before the parasitoids emerge. At these elevated positions, the parasitoid larvae form ball-like common cocoons. These cocoons are often hyperparasitised [109] (personal communication V.Ž.). Solitary parasitoids send less visible signals, indicating their lower overall presence in the environment, which may reduce detection by natural enemies. Also, they often use hosts that are less exposed, which have cryptic lifestyles, such as leaf or stem miners attacked by Pholetesor, species of which are specialised to parasitise some Gracillariidae, in particular, as well as Elachistidae [110]. Concealed hosts are also targets of solitary parasitoids from other genera; for instance, Apanteles hemara parasitises Tebenna micalis (Mann) from the Choreutidae family, which mines several species within the Asteraceae family. Similarly, Dolichogenidea artissima (Papp) parasitises Coleophora larvae (Coleophoridae) that inhabit solid cases made of silk. Additionally, Dolichogenidea halidayi (Marshall) targets Glyphipterix simpliciella (Stephens) (Glyphipterigidae) found in the dry stems of the grass Dactylis glomerata L. [110]. In the case of the species Glyptapanteles porthetriae, it is common for the emerging larva of the parasitoid to pupate under the body of its host, Lymantria dispar (Erebidae), which is usually an L2 [105]. Typically, the caterpillar moves to the underside of the leaf, where it becomes less noticeable to enemies.

3.1.9. Protection from Natural Enemies

Parasitoids employ various mechanisms to protect themselves from other natural enemies. These mechanisms primarily focus on safeguarding the juvenile stage. By regulating the host’s behaviour, parasitoids can influence the host’s protective actions. One of the simplest protective strategies involves the host hiding on the underside of a leaf. Other strategies include constructing shelters from materials in the surrounding environment or the caterpillar actively defending the parasitoid brood from hyperparasitoids by body movements (e.g., [111]).

The presence of additional silk over cocoons spun by parasitised caterpillars significantly increases parasitoids’ safety. Depending on the species, gregarious Microgastrinae spin their cocoons either individually on or around the host’s body or connect them into a communal structure. For instance, larvae of Cotesia congregata and C. spuria (Wesmael) independently spin cocoons attached to the host’s skin without connections. However, many Microgastrinae species cooperate in spinning common cocoons, linking their individual cocoons more or less strongly for pupation. The architecture and colour of the silk threads produced by the parasitoid larvae often allow for species identification [72].

The most compact, and most architecturally organised, mass cocoons are found in species such as Glyptapanteles fraternus (Riley), Diolcogaster alvearia (Nixon) (see the photo at: https://www.inaturalist.org/taxa/374069-Diolcogaster, accessed on 8 October 2024), and several closely related Cotesia species, including C. tibialis, C. ofella, C. berberis, C. trivaliae, C. vanessae, C. yakutatensis, and C. xylina. [72]. Specifically, larvae of the first two species exhibit remarkable precision in spinning their cocoons, aligning them in multiple rows beneath the host’s body. This strategic arrangement conceals the cocoons from visually oriented predators by closely adhering to the host’s body contours, typically observed in Geometridae caterpillars.

Harvey et al. [85] examined the rate of hyperparasitism in the association Cotesia glomerata/Pieris brassicae and found a lower number of the hyperparasitoid Lysibia nana (Gravenhorst) per brood in the protected cocoon than when the microgastrine cocoons were unprotected. On the other hand, Tanaka and Ohsaki [112] reported that the additional silk layer produced by parasitised caterpillars of P. brassicae over C. glomerata cocoons did not effectively reduce hyperparasitism rates by Trichomalopsis apanteloctena (Crawford).

It is common for parasitoids from the same brood to leave the host almost simultaneously, within a short period. This synchronised emergence is an adaptive strategy that enhances the survival of parasitoid offspring. Synchronised emergence increases the chances of brood survival against hyperparasitoid attacks by benefiting from safety in numbers [113].

Being attached to a living host may increase the likelihood that primary parasitoids will avoid parasitisation by secondary ones. A well-documented case involves the caterpillar of Mythimna separata Walker (Noctuidae), which exhibits aggressive behaviour in response to the hyperparasitoid Gelis agilis (F.) (Ichneumonidae) trying to attack the cocoons of Microplitis sp. [103]. Such protection is provided only by those parasitoids that do not consume the entire host tissue before pupation but leave the vital organs intact. In this way, the parasitoid enables the host to live as long as possible and not move far away from the pupation site to provide the greatest protection against hyperparasitoids and predators.

3.1.10. Pre-Mating Behaviour and Finding Partners

The reproductive success of a male is limited by the number of females it can mate with [114]. In many parasitoid species, including Microgastrinae, males often emerge before females. This phenomenon is known as protandry. This ensures that males are present and ready to mate as soon as females emerge, increasing their chances of reproductive success. This strategy is particularly important in species where females are receptive to mating shortly after emergence, releasing pheromones to attract males. These chemical cues are crucial for mate location, especially in dense environments where visual cues might be less effective. The specificity and range of these pheromones can vary among species, playing a critical role in ensuring that males find females of the correct species. Using chromatography-mass spectrometry analyses, Prazapati et al. [114] revealed that Nasonia vitripennis (Walker) (Hymenoptera: Chalcidoidea: Pteromalidae) can distinguish which hosts have adult females, indicating a species-specific reproductive strategy. Studying the mating behaviour of Cotesia glomerata, Tagawa and Kitano [115] recorded that the first emergence from the cocoons are always males. Confirmed examples of protandry include two solitary endoparasitoids of the diamondback moth Plutella xylostella: the well-known C. vestalis and the lesser-studied Dolichogenidea sicaria Viereck [116]. Here, we mention that acoustic signals also play an important role in mate selection, as observed in C. flavipes [117].

3.1.11. Inbreeding

Gregarious parasitoids are biologically inclined to mate with relatives since male and female individuals from the same brood, typically produced by a single mother, hatch in quick succession. Protandry, common in Hymenoptera, helps mitigate this by allowing males to emerge earlier, disperse, and find unrelated mates. Additionally, some gregarious species have developed a higher tolerance for inbreeding, which may offer genetic advantages by preserving specific adaptations within closely related groups, despite the risks of brood-mating. Trevisan et al. [118] found that in the gregarious Cotesia flavipes that were under extreme inbreeding pressure for 10 generations, no harmful effect was shown. This parasitoid has been continuously cultivated for 40 years in laboratories in Brazil on the sugarcane borer Diatraea saccharalis, without any introduction of new specimens during that period. On the other hand, Tagawa and Kitano [115] recorded a high percentage (58.6%) of inbreeding in C. glomerata.

The incidence of diploid males, which are produced at the expense of females, increases with inbreeding. Typically, diploid males are either unviable or effectively sterile, imposing a significant genetic load on populations. However, recent research has shown that diploid males can be reproductive in the gregarious parasitoid wasp C. glomerata, thereby mitigating the genetic burden [119]. The authors propose that the frequent occurrence of inbreeding has driven the evolution of diploid male fertility in this species.

3.1.12. Lifespan

Parasitoid lifespan is closely tied to nutrient availability, as demonstrated by Miksanek and Heimpel [120] in their study on Aphelinus certus Yanosh, a chalcid parasitoid of the soybean aphid, where lifespan varied with host density. Based on the available literature, solitary parasitoids, being generally larger-bodied, are suggested to have longer lifespans compared to gregarious parasitoids. This correlation is supported by the notion that body size often influences lifespan, with smaller-bodied gregarious species having shorter lifespans relative to their solitary counterparts. This difference aligns with the reproductive strategies and ecological adaptations of each group, where solitary parasitoids invest more in longevity and fewer offspring, whereas gregarious parasitoids focus on rapid reproduction and shorter lifespans. Adult body mass exhibited sexual dimorphism in all Cotesia species studied, with females being larger than males. However, this pattern was not observed in Microplitis species. In one particular species of Microplitis, males were found to be the larger sex [84]. In the study by Hegazi et al. [121], the body size, egg load dynamics, oviposition, and longevity of adult M. rufiventris were influenced by the larval instar of their host, Spodoptera littoralis (Noctuidae), at the start of development. The wasps showed the best performance when they parasitised L3 (the desirable instar), followed by L1 and L2 stages, with L4 being the least favourable (undesirable instar). According to this experiment, females that did not lay eggs and emerged from older hosts lived longer than those that developed from younger hosts. Working with Cotesia and Microplitis, Harvey et al. [87] showed that parasitised hosts exhibited a 90% reduction in growth compared to healthy hosts, with the maximum host size being closely related to the size of the adult parasitoid. Additionally, the development time was longer for the more generalist parasitoids than for the specialists.

4. Discussion

This comprehensive analysis compared 12 selected life history strategy categories, as we contrasted the ecological and reproductive dynamics of solitary and gregarious Microgastrinae parasitoids, reflecting on how each strategy impacts parasitism efficiency. Although the current understanding of the biology of Microgastrinae, particularly their interactions with hosts, natural enemies, and competitors, remains limited, the available data allow for some preliminary conclusions regarding the solitary and gregarious parasitism strategies, and their strengths and weaknesses in IPM programs. The assessment assigns relative advantages to either group, with a score of (1) indicating an advantage, (0) indicating a disadvantage, and (?) indicating insufficient knowledge (

Table 1. Assessment of the parasitism success of solitary vs. gregarious parasitoids evaluated through defined categories: (1) indicates advantage, (0) disadvantage, and (?) insufficient knowledge to conclude.

Strategy	Parasitism Type
	Solitary		Gregarious
	Note	Mark	Note	Mark
Host range	Narrow	1	Broad	1
Host acceptance	Low	0	High	1
Egg-laying capacity	Low	0	High	1
Oviposition speed	Slow	?	Fast	?
Overcoming the host’s immune system	Lower	0	Higher	1
Host instar attacked	Early	1	Late	0
Host instar preference for the emergence	Early	1	Late	0
Rate of exposure to enemies	Lower	1	Higher	0
Protection from enemies	Lower	0	Higher	1
Pre-mating behaviour and finding partners	Low	0	High	1
Chance to inbreed	Low	1	High	0
Lifespan	Long	1	Short	0
Score		6		6

). Across the evaluated categories and strategies, IPM-related beneficial traits are nearly evenly distributed between the two groups, with neither solitary nor gregarious Microgastrinae showing an overall advantage.

The broad host range of gregarious parasitoids allows for their application against multiple lepidopteran species, making them more versatile in biological control programs. A good example would be Apanteles xanthostigma (Haliday), a species that can potentially be used in biological control against 68 species of semi-concealed arboreal microlepidopterans from 11 families, primarily Tortricidae (28 species), but also Gracillaridae, Yponomeutidae, and others [122]. Even though some of these host identifications may be incorrect, this range still indicates a broad host selection for the parasitoids. Although many host species are utilised by multiple parasitoid species [63], they rarely coexist in the same ecosystem due to their identical resource requirements. Consequently, direct competition between them is rare [123]. In classical biological control theory, a critical consideration is the host specificity of introduced natural enemies. Effective control agents are generally expected to have a narrow host range to minimise non-target impacts. However, in the case of gregarious parasitoids with broader host ranges, additional evaluations are necessary to assess potential risks to non-target species and ensure that they align with conservation and environmental safety standards. In summary, both solitary and gregarious parasitoids offer unique advantages: solitary parasitoids, with their specialised host preferences, can effectively control a single or limited number of pest species, while gregarious parasitoids are valuable for managing a broader array of hosts. This versatility also facilitates their mass production, enabling application across a range of pest control scenarios [124,125].

Parasitoid acceptance of the host individuals depends on the physiological conditions of both the parasitoid and host. However, it has been shown that gregarious parasitoids take greater risks compared to solitary ones. Hopper et al. [126] reported that Cotesia glomerata females carrying large numbers of eggs and not laying them in time are more willing to accept hosts with low suitability for offspring development than females with low egg loads and longer lifespans. As already shown in experiments with these types of parasitoids, which can normally parasitise later stages of the host (unlike solitary parasitoids), this will compromise the choice of host quality.

The fecundity and egg-laying capacity of solitary and gregarious parasitoids vary not only due to their different reproductive strategies but also at the intraspecies level, as determined by Hegazi et al. [80]. Therefore, the quality of the host from which the female parasitoid emerges will affect the fecundity of the individual itself.

From an economic perspective, it is essential in agriculture to prevent or mitigate pest damage to crops as early as possible. Targeting the youngest larval instars is particularly advantageous, as it minimises the harm caused by pests. Larger caterpillars pose a greater threat to crops due to their higher consumption of plant material. Solitary microgastrine species, which prefer to emerge from earlier larval stages, help to significantly reduce the damage caused by caterpillars, thereby protecting agricultural yields. This preference for early to mid-instar larvae among solitary microgastrines is influenced by a combination of ecological and biological factors that optimise their development and survival. Early instars offer a host that is not yet heavily compromised by damage or depletion, ensuring a more stable environment for parasitoid larvae to develop. Unlike gregarious parasitoids, which face competition from their siblings, solitary parasitoids benefit from reduced competition and a minimised risk of encountering predators and hyperparasitoids that are more prevalent in later host stages. Moreover, early instar hosts are more susceptible to manipulation by parasitoids, allowing them to exert greater control over the host’s behaviour and development. This strategic targeting of younger instars results in a significant reduction in the host’s body weight, delays moulting, and ultimately prevents pupation, as noted by Strand [90]. In contrast, hosts parasitised by gregarious parasitoids experience less drastic changes in behaviour and weight but are similarly unable to pupate. Therefore, when selecting candidates for biological control, it is crucial to consider the host instar stage that is attacked and the timing of parasitoid emergence, as this will influence the effectiveness and timeliness of pest population reduction. This comprehensive approach ensures that the biological control agent not only targets the most vulnerable host stage but also emerges at a time that maximises the suppression of pest populations, contributing to more effective pest management strategies.

The contrasting strategies of solitary and gregarious parasitoids underscore their distinct ecological adaptations. Prime examples are Cotesia glomerata and C. rubecula, both parasitoids of Pieris rapae. A gregarious species, C. glomerata allows its host to reach L5, during which parasitised caterpillars may increase their feeding, potentially leading to greater crop damage [127]. This increased feeding reduces its overall effectiveness in agricultural contexts. In contrast, C. rubecula, a solitary parasitoid, emerges from its host mostly at L4, reducing significant feeding and thereby minimising crop losses [128,129]. This comparison emphasises how different life history strategies can influence biological control outcomes in agricultural ecosystems.

Given that the lifespan of a parasitoid largely depends on its size, which is closely related to the preferred instar of the host for parasitisation, it is crucial to not only select the appropriate parasitoid species for biological control of a specific pest but also to time the intervention correctly. Effective monitoring is essential to ensure that the host stage is targeted with an adequate parasitoid, whether solitary or gregarious. This approach maximises the effectiveness of biological control efforts.

Due to the similarity in overall advantages between solitary and gregarious parasitoids, certain traits become more critical than others when determining their effectiveness in integrated pest management (IPM) programs. As demonstrated in most cases, monophagy is highly promising, positioning these parasitoids as prime candidates for biological control. The primary advantage of monophagy is the significantly reduced risk of affecting non-target species, effectively eliminating the potential for invasiveness. Due to their high specialisation, monophagous parasitoids may be more adept at locating and parasitising their specific hosts, leading to more effective control of pest populations. Their specialised biology and ecology, characterised by fewer interactions with other organisms and a smaller number of trophic associations, make monophagous parasitoids more predictable and easier to manage in biological control programs. Generally, specialisation is crucial in ecology and serves as a key trait in parasitoids. Highly specialised parasitoids typically utilise hosts more efficiently than their generalised counterparts, likely due to a trade-off between host range breadth and host-use efficiency [130]. However, the decision to use a monophagous parasitoid also depends on the availability of the host in the target environment and the possibilities of parasitoids adapting to a closely related species, which might broaden its host range over time.

Selecting the optimal parasitoid species is crucial, but equally important is recognising the significant intraspecific variability these biocontrol agents often exhibit. Many parasitoid species experience strong selective pressures from their hosts, leading to genetically distinct populations, or host races. Environmental factors and reproductive traits that impede gene flow can cause these races to diverge into separate species [26]. This phenomenon has been observed in cases where traditional biological control introductions have failed. For example, molecular methods have revealed that Cotesia flavipes, known for parasitising Sesamia nonagrioides, actually comprises a species complex. Phylogenetic analyses by Muirhead et al. [131] supported the monophyly of this complex, identifying at least four distinct species: C. chilonis (Muesebeck) (from China and Japan), C. flavipes (originally from the Indo-Asia region but introduced into Africa and the New World), C. nonagriae (Viereck) (from Australia and Papua New Guinea), and C. sesamiae (from Africa), with the discovery of a fifth species, C. typhae [26]. Laboratory experiments on a strain of C. typhae from Kenya, reared on a Kenyan strain of S. nonagrioides following Overholt et al. [132], proved successful against both Kenyan and European strains of S. nonagrioides. Similarly, in New Zealand, effective suppression of Mythimna separata was achieved only with a specific strain of C. ruficrus introduced from Pakistan, as well as in the USA, which was required to effectively control the cabbage worm P. rapae [59].

The levels of specialisation in parasitoids extend beyond species complexes and strain variations. Recent advancements have allowed insights into the mechanisms underlying their life strategies, revealing the conditionality imposed by endosymbionts. Some endosymbiotic bacteria, such as Wolbachia, not only influence gene flow between populations but also drive speciation through reproductive barriers. In some Cotesia species parasitising Melitaeini lepidopterans, Wolbachia Hertig can impact the immune systems of its hosts, influencing the success of parasitism and the survival of parasitoid larvae within their hosts [133]. This relationship comes at a price, though, as Wolbachia is known to change the odour of parasitised caterpillars, and thus enable hyperparasitoids to locate potential hosts [134]. The variation in bracovirus genes allows different wasp populations to specialise in local lepidopteran communities, providing clear evidence of contribution to ecological success [135]. These processes are additionally influenced by PDVs, which, as documented in the case of Cotesia sesamiae, coevolve with the wasp’s genome [26]. Since many ecological interactions, including successful parasitism, are influenced at the microbial level, it is crucial to explore the complex, potentially bidirectional, alterations between host and parasitoid microbiomes [136]. These dynamics could help explain why some IPM programs are less effective or vary depending on geographic location. Additionally, it is important to recognise that the microbiomes of natural host populations and lab-reared hosts used for preliminary BCA testing differ significantly, as Gloder et al. [137] demonstrated for Pieris brassicae. These composition variations may be behind the discrepancies between lab-based trials and field performance.

No universal conclusion can be drawn regarding the overall superiority of solitary versus gregarious Microgastrinae parasitoids in controlling pest caterpillars. Both groups possess distinct advantages in their respective life strategies, requiring careful evaluation for specific biological control needs and projects. Utilising both solitary and gregarious parasitoids, or generally introducing multiple parasitoids to capitalise on their differing biological and ecological responses, has been a topic of long-standing debates. This strategy aims to optimise pest management and ensure sustainability (e.g., [138]). In scenarios of low host abundance, solitary parasitoids are advantageous due to their enhanced performance with dispersed hosts. In internal competition tests with a well-studied pest, Pieris rapae, Laing and Corrigan [139] observed that the solitary parasitoid Cotesia rubecula outperformed the gregarious C. glomerata. This occurred when an egg of C. rubecula was oviposited in the host approximately 48 h before those of C. glomerata. In such cases, C. rubecula consistently won the competition among parasitoids, succeeding in over 90% of interactions.

In environments with high caterpillar density, gregarious parasitoids are more effective due to their adaptation to parasitising hosts en masse. On the other hand, in field experiments, Paull et al. [140] demonstrated that natural enemies, which respond positively to the density of host populations, can swiftly suppress them, thereby preventing significant economic losses. They discovered that the response of the solitary parasitoid Dolichogenidea tasmanica to the population density of Epiphyas postvittana (Tortricidae) on grapevines was inversely density-dependent, with notably higher rates of parasitisation in Cabernet Sauvignon grapes compared to Chardonnay grapes. This indicates that the host plant (grape variety), as the third component of the trophic chain, significantly influences the level of parasitism.

5. Conclusions

In conclusion, both solitary and gregarious Microgastrinae are critical components in integrated pest management (IPM), each bringing unique features to maximise their effectiveness in sustainable agriculture. A deep understanding of their ecological interactions, competitive behaviours, and the impact of environmental factors is crucial for optimising their deployment in biological control strategies. The practice of introducing multiple parasitoid species to combat a single pest often stems from the challenge of identifying the most effective parasitoid from a very diverse pool. While there is a prevailing belief that the target environment will naturally select the most effective species for biological control [141], concerns persist that introducing multiple species may lead to confusion and undermine pest control efforts, potentially reducing the overall effectiveness of the strategy [142]. This highlights the importance of strategic planning and evaluation in the deployment of parasitoids within IPM frameworks.