A Review of Franklinothrips vespiformis (Thysanoptera: Aeolothripidae): Life History, Distribution, and Prospects as a Biological Control Agent

Simple Summary Predatory species are a small but significant part of the Thysanoptera, which is often overlooked. Franklinothrips are found throughout the tropics and are regarded as major natural enemies of thrips and other small arthropod prey. In this review, we summarized the geographical background, morphology, and prey associations, with an emphasis on Franklinothrips vespiformis, the most widely distributed predatory thrips species. This literature review could serve as a foundation for future research into Franklinothrips as biocontrol agents for economically important insect and mite pests in China. Abstract Predatory species comprise a small but important and often overlooked component of the Thysanoptera. A case in point, the ant-mimicking Franklinothrips are widely distributed in the tropics and are considered important generalist natural enemies for thrips and some other small arthropod prey. Franklinothrips present an addition to biocontrol applications, i.e., greenhouse or commercial application for certain target pests and situations. Current knowledge, including distribution, biological features, life history pa rameters, prey specificity, host plant associations and lass production is yet insufficient to decide to what extent Franklinothrips could contribute for biological control programs. In this review, we summarized the geographical background, morphology, and prey associations, with a focus on F. vespiformis, the most widely distributed species of predatory thrips. This literature review serves as the basis for future research into the use of Franklinothrips as biocontrol agents for economically significant insect and mite pests in China and elsewhere.


Introduction
The Thysanoptera (thrips) constitute approximately 6500 species that are globally distributed and represent many of the smallest winged insects [1,2]. Several thrips species are globally important, due to their capacity to disperse through the plant trade and vector plant tospoviruses, which cause significant agricultural losses [3]. While most of the thrips are detritivores (mainly fungal feeders) and herbivores (feeders of flowers, fruits, and leaves) [4,5], approximately 300 species have evolved a predatory lifestyle [6].
Predatory thrips are known from several families. Surveys in three districts of northern Thailand revealed 10 species of predatory Phlaeothripidae in five genera, including Aleurodothrips fasciapennis, which were present throughout the year and contributed to

of 13
In Latin America, F. vespiformis was first described in 1909 [22] and subsequently noted as abundant in avocado agroecosystems in Mexico [23]. This species has been found in Taiwan [32], India [33,34], and many Caribbean, Central, and South American countries, including Nicaragua, Peru, and Brazil [24,25]. Finally, in Oceania, F. vespiformis was recorded from Fiji, New Caledonia, as well as the eastern coast of Australia [10], also found in Japan, Thailand and mainland of China [7,11,36].   In Latin America, F. vespiformis was first described in 1909 [22] and subsequently noted as abundant in avocado agroecosystems in Mexico [23]. This species has been found in Taiwan [32], India [33,34], and many Caribbean, Central, and South American countries, including Nicaragua, Peru, and Brazil [24,25]. Finally, in Oceania, F. vespiformis was recorded from Fiji, New Caledonia, as well as the eastern coast of Australia [10], also found in Japan, Thailand and mainland of China [7,11,36].

Morphological Characteristics
F. vespiformis experiences partial metamorphosis, developing through egg, larva, pupa, and adult stages ( Figure 2). The following is based on the authors' observations, which is supplemented with published findings [36,44,45].

Eggs
Eggs are produced singly inside the leaf tissue, and they can be distinguished by yellow-green projections. Eggs are kidney-shaped and transparent white, with dimensions of 0.4 ± 0.01 mm by 0.1 ± 0.003 mm (Figure 2a).

Larva
Two instars are included in the larval period. The newly emergent first instars are pale white, with the third antennal segment about 3.5 to 4.5 times as long as wide ( Figure 2b). After feeding for 1 or 2 days, the mesothorax and abdomen segments III-VII develop a red coloration (Figure 2c). The second instars have a distinctive hump-back. In addition, the head and prothorax develop a red coloration as the mesothorax. The second instar in the third antennal segment is about 7.0 to 8.0 times as long as wide, and the fore tibia and tarsus are dark (Figure 2d). Both of the instars possess seven segmented antennae with three distal segments, which are closely fused. The red hypodermal pigments are only present on the femora.

Eggs
Eggs are produced singly inside the leaf tissue, and they can be distinguished by yellow-green projections. Eggs are kidney-shaped and transparent white, with dimensions of 0.4 ± 0.01 mm by 0.1 ± 0.003 mm (Figure 2a).

Larva
Two instars are included in the larval period. The newly emergent first instars are pale white, with the third antennal segment about 3.5 to 4.5 times as long as wide ( Figure 2b). After feeding for 1 or 2 days, the mesothorax and abdomen segments III-VII develop a red coloration (Figure 2c). The second instars have a distinctive hump-back. In addition, the head and prothorax develop a red coloration as the mesothorax. The second instar in the third antennal segment is about 7.0 to 8.0 times as long as wide, and the fore tibia and tarsus are dark ( Figure 2d). Both of the instars possess seven segmented antennae with three distal segments, which are closely fused. The red hypodermal pigments are only present on the femora.

Pupa
Pupae are found underneath the leaves, inside a white silk cocoon constructed by the larva (2e). The pupa are red in color with three stages, pre-pupal stage, pupal stage 1 ( Figure 2f) and pupal stage 2 ( Figure 2g). Wing buds are well developed, but shorter in pre-pupal stage (show non-obvious movement, prepared for cocoon construction). The pupal skin of the appendages is segmented only in pre-pupa. The antennal sheaths do not reach the metathorax (pupa 1), but reach the abdomen (pupa 2). In addition, posterior wing buds reach abdominal segment III (pupa 1), while both the anterior and posterior wing buds reach abdominal segment V (pupa 2). The legs and hind tibiotarsus are shorter than pterothorax (pupa 1), and the legs and hind tibiotarsus are longer than pterothorax (pupa 2).

Adult Female
Female F. vespiformis (myrmici) are common and have a body length of 2.5-3.0 mm ( Figure 3a). Females are fully winged and their forewing is slender with a rounded apex. The body is black with white bands on the second and third segments, and an anteriorly narrowed abdomen. The abdomen is broadest at segment five or six. The body, legs, and antennae are brown. However, antennal segments I-III and abdominal segments II and III are yellow. Moreover, the anterior margins are brown and the femora is often yellowish at distal end. Legs brown with femora yellowish at distal end. Fore-wing brown with three paler areas in the base, middle and sub-apex.
pre-pupal stage (show non-obvious movement, prepared for cocoon construction). The pupal skin of the appendages is segmented only in pre-pupa. The antennal sheaths do not reach the metathorax (pupa 1), but reach the abdomen (pupa 2). In addition, posterior wing buds reach abdominal segment III (pupa 1), while both the anterior and posterior wing buds reach abdominal segment V (pupa 2). The legs and hind tibiotarsus are shorter than pterothorax (pupa 1), and the legs and hind tibiotarsus are longer than pterothorax (pupa 2).

Adult Female
Female F. vespiformis (myrmici) are common and have a body length of 2.5-3.0 mm (Figure 3a). Females are fully winged and their forewing is slender with a rounded apex. The body is black with white bands on the second and third segments, and an anteriorly narrowed abdomen. The abdomen is broadest at segment five or six. The body, legs, and antennae are brown. However, antennal segments I-III and abdominal segments II and III are yellow. Moreover, the anterior margins are brown and the femora is often yellowish at distal end. Legs brown with femora yellowish at distal end. Fore-wing brown with three paler areas in the base, middle and sub-apex.

Adult Male
Male F. vespiformis are rare, similar to female in colour with a smaller and less antlike appearance (Figure 3b). Males have a longer and darker antennae, a less constricted waist, and commonly paler wings. The second and third antennal segment is approximately as long as the head, with a long sensory metanotum formed of irregular scallops. The head is broader than long, the eyes are prolonged ventrally, and the posterior ocelli a r e larger than t h e anterior. The prothorax i s narrower towards t h e base, and the metanotum has no sculpture medially, with long and slender legs. Abdominal sternite II with two pairs of discal setae; sternites III-VIII with two pairs of posteromarginal setae and one pair of discal setae in a line.

Adult Male
Male F. vespiformis are rare, similar to female in colour with a smaller and less ant-like appearance ( Figure 3b). Males have a longer and darker antennae, a less constricted waist, and commonly paler wings. The second and third antennal segment is approximately as long as the head, with a long sensory metanotum formed of irregular scallops. The head is broader than long, the eyes are prolonged ventrally, and the posterior ocelli are larger than the anterior. The prothorax is narrower towards the base, and the metanotum has no sculpture medially, with long and slender legs. Abdominal sternite II with two pairs of discal setae; sternites III-VIII with two pairs of posteromarginal setae and one pair of discal setae in a line.

Developmental Parameters
F. vespiformis is active at temperatures over 18 • C and develop from egg to adult within roughly 3 weeks at 27 • C. Moreover, it survives up to 60 days as an adult (Table 2), with no reported diapause. Previous studies of mass storage suggest a differential cold tolerance among the different life stages. In general, the viability of the eggs declines when stored below 7.0 • C, although storing eggs at 12.5 • C for 4-5 weeks was possible [15,16]. The potential to store eggs may assist the mass rearing and dissemination of F. vespiformis as a biological control agent.

Sex Ratio
Although F. vespiformis consists of both males and females, it is usually an unisexual species. Males were not found in Japan [36] and appear to be rare in populations from other countries [14,20]. Wolbachia-mediated parthenogenesis has been reported in F. vespiformis and other thrips species [46][47][48]. Heat and tetracycline treatments appeared to produce male F. vespiformis. Despite the fact that males produced motile sperm, which was forwarded via spermatheca, mating had no effect on the subsequent generation's sex ratios. This indicates that the sperm do not fertilize eggs [46]. Among the introduced thrips, parthenogenesis is common, possibly spreading more easily than sexual forms [49,50].

Ovipositing Behavior
Arakaki and Okajima [36] as well as Arakaki, Miyoshi, and Noda [46] studied the reproductive behavior of F. vespiformis. Viable eggs are produced via parthenogenesis with eggs laid singly into the stem, leaf vein or other soft plant tissue using their serrated ovipositor. Females can oviposit three eggs within an hour, producing 150 to 200 eggs in their lifetime. Moreover, females deposit a drop of yellowish protective secretion on the exposed tip of the eggs, which makes them difficult to locate.

Cocoon Spinning
Several species among Franklinothrips and Aeolothrips construct silken cocoons underneath the leaves or in the soil or leaf litter, for example, Aeolothrips kuwanaii, A. fasciatus, A. melaleucus, Orothrips kelloggi, Ankothrips yuccae, and A. gracilis [10,12,51]. Reyne [12] indicated that the cocoon production of F. vespiformis takes a full and larvae were ob-served sharply twisting and turning their abdomens, with the final cocoon as white and oval-shaped, measuring roughly 2.7 mm × 1.3 mm in size [12,36].

Ant-Mimicking Behavior
While some degree of myrmecomorphy is associated with most of the Franklinothrips, the extent of ant-like features and behavior is highly pronounced in adult female F. vespiformis [14]. A highly constricted first abdominal segment produces an ant-like waist [36]. Similar to ants, individuals can run quickly and palpate their antennae on the ground. These distinguishing characteristics have been proposed in order to help adults escape predation [52,53].

Natural Prey Range
Franklinothrips are generalist or opportunist feeders of thrips, but also attack a broad range of small arthropods and smaller conspecifics [10]. Among them, F. vespiformis is known to prey upon phytophagous insects and mites from several orders ( Table 3). Larvae and adults move quickly and seize the prey with their front legs, which are used to hold the prey while feeding [36].
Both larvae and adults are particularly predacious on other thrips, feeding on adults, larvae, and pupal stages. In Trinidad, F. vespiformis was observed feeding on the cacao thrips, Selenothrips rubrocinctus and Dinurothryps hookeri on ornamental flowers, and Caliothrips insularis on the Sudan grass [26]. In Mexico, F. vespiformis are the most prevalent among 16 predatory thrips, which were captured in an avocado orchard infested with several species of pest thrips. In Brazil, F. vespiformis was frequently found in association with Leucothrips furcatus, which appeared as the prey [31]. Additional economically important thripine targets for F. vespiformis include Thrips tabaci, T. palmi, and Frankliniella occidentalis [40].
In nature, F. vespiformis is usually found on low growing plants, shrubs, and bushes and has similar feeding habits to Aeolothrips melaleucus [51,54]. It is found in a variety of habitats, including roadsides [54], rainforests, orchards, and field crops [40]. Adult Franklinthrips feed on non-prey materials and can survive for extended periods of time on pollen and plant sap [43]. When reared under crowded conditions (10 individuals/Petri dish), adults and larval become cannibalistic [36].

Franklinothrips: As Augmentative Biological Control Agents
While predatory thrips are considered an important component of natural and agroecosystems, their use as commercial bio-control agents has gained relatively little attention. However, in Europe, F. vespiformis has been tested and marketed for use against thrips in greenhouses, nurseries, botanical gardens, and interiorscapes for many years [15,16,42]. In addition, F. orizabensis has been the focus of successful research with an augmentative release against several pest thrips in California avocado groves [17,43].

Release of F. vespiformis in Greenhouse Crops
Several studies have investigated the use of F. vespiformis to manage thrips in greenhouses. In southern France, F. vespiformis was first introduced in rose greenhouses for 2 years, with a predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) to suppress onion thrips T. tabaci and western flower thrips F. occidentalis [39]. Although widely used, N. cucumeris is less effective where temperatures are high. Therefore, F. vespiformis was used to supplement the control. In this case, F. vespiformis was generally effective at reducing Insects 2022, 13, 108 8 of 13 populations of thrips below economic thresholds, although it did not provide a long-term establishment, suggesting that repeated introductions would be needed. Follow-up tests showed that the combined use of F. vespiformis and N. cucumeris during periods of high thrips infestation gave better results when compared with N. cucumeris alone [38]. In another study in greenhouse cucumbers, the weekly release of one F. vespiformis adult per plant over 4 weeks after flowering, reduced the populations of thrips on leaves to low levels, although less control was observed on flowers [56]. In Japan, F. vespiformis was released in greenhouses to control T. palmi in eggplants and cucumbers [36,46]. Some evidence suggests that the releases were successful in ornamental plants. When F. vespiformis was used in Crown-of-Thorns (Euphorbia milii var. splendens), Frankliniella occidentalis larvae were drastically decreased compared to the control. Only one F. occidentalis larva/flower was found 7 weeks following the release of F. vespiformis, compared to 14 larvae/flower in the control plots [48]. Despite these limited studies, the prey range, choice, and requirements for the release of F. vespiformis in most greenhouse crops are yet unknown.

Commercial Availability
Since predatory thrips typically do not occur at high densities, they can be reared for augmentative use. In Europe, F. vespiformis is sold through at least two distributors for pest thrips, including Frankliniella occidentalis, Echinothrips americanus, Parthenothrips dracaenae, Scirtothrips spp, and Thrips palmi [58,59]. The product is sold as adult thrips in a tube, which can be stored for 2 days at 10-15 • C. The success of releases will vary, based on the release rate, environmental conditions, and economic threshold of the target pest [16,17].

Other Predatory Thrips and Prey Associations
Surveys have found predatory thrips on many natural and cultivated plants, which reflect the host range of their prey ( Table 4). Surveys of annual and perennial field crops, shrubs or trees, and roadside vegetation and weeds in three districts of northern Thailand revealed 10 species of predatory thrips in five genera of the Phlaeothripidae, i.e., Aleurodothrips fasciapennis, Androthrips flavipes, A. ramachandrai, Karnyothrips flavipes, two indeterminate Karnyothrips spp., Leptothrips sp., Podothrips lucasseni, and two indeterminate Podothrips spp. In this case, thrips hosts were present throughout the year. Preys of predatory thrips were identified on asteraceous weeds, including Bidens pilosa and Tridax procumbens, but also eriophyid mites were identified on Siam weed (Chromolaena odoratum). P. lucasseni was found on eriophyid mites on Sandoricum koetjape (santol) and Litchi chinensis (litchi). In addition, distinct distributions were found, i.e., Karnyothrips flavipes was usually correlated with green field crops, such as coffee, garlic (Allium sativum), and Spanish needle (B. pilosa). Kar nyothrips were observed feeding on unidentified crambid larvae (Lepidoptera: Crambidae) on Spondias pinnata (Lepidoptera: Crambidae) in another province. Podothrips spp. were observed in association with thrips on Argyreia capitiformis, aphids on Lepistemon bi nectariferum and Bidens pilosa, spider mites on Bambusa sp. (bamboo). Childers and Nakahara (2006) [60] found diverse predatory species of thrips in citrus groves in Florida, USA, associated with six weed species. The potential host diversity of predatory thrips on commercial crops highlighted by these surveys suggests that other species could be explored further as biological control agents.

Future Research Perspectives
Since its original description by Crawford [22], reports show that F. vespiformis is a widespread and important natural enemy of thrips and other small arthropods, as well as an interesting and unusual model organism for Batesian mimicry. From a pest management perspective, the advantages of F. vespiformis include the relatively wide range of attacked hosts and life-stages. The ability of this predator to attack thrips species, such as E. americanus, which are not easily controlled by most of the current commercial biological control agents, including predatory mites [66], is of particular benefit. However, the relatively slow intrinsic rate of increase, when compared with predatory mites [67], and its tendency for cannibalism [36] are hindrances, increasing the cost and complexity for mass production. Nevertheless, as the global market for predatory insects expands and moves towards the use of multiple biological control agents and bioactive molecules [68], we anticipate increased interest, production, and deployment of F. vespiformis (and likely F. orizabensis) in crops where the current biocontrol agents do not provide reliable (or need supplemental) control. Their ability to feed on eggs of thrips, which are hidden in plant tissues and cryptic prey, such as leafminers [36,69] is also encouraging. Moreover, given that F. vespiformis can be cold-stored for a relatively long time period [15] will benefit its distribution to end users.
Despite their potential, it remains unclear on which crops F. vespiformis can be most effectively employed. The research gaps identified while compiling this review include the determination of optimal pest/crops associations, and the potential intraguild interactions with other biocontrol agents. To that end, most of the effective application rates and timing need further assessment under both greenhouse and field conditions. The provision of thrips banker plant systems or other supplemental food, such as pollen also need further investigation [40]. Of note, F. vespiformis may feed on a commercial supply of decapsulated brine shrimp eggs, which are used to support other commercially produced beneficial insects and mites (SPA personal observations). Moreover, it is possible that the ant-like appearance of F. vespiformis may help in the protection from negative intraguild interactions, while its adaption to topical environments may make it less likely to be established outdoor in temperate regions.
In conclusion, F. vespiformis is both a charismatic and economically important species of thrips, which warrants further attention in both conservation and augmentative biological control research. Furthermore, additional ecological and applied pest management studies will determine the role of this predator as both an invasion risk in natural ecosystems and as a commercial success in agricultural pest control.

Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.