Franklinothrips vespiformis: History
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Subjects: Agriculture, Dairy & Animal Science
Contributor:
Mubasher Hussain

Species of Franklinothrips (Thysanoptera: Aeolothripidae) are predatory on various other insects. These fast moving, ant-mimicking predatory thrips are widely distributed in the tropics. F. vespiformis has gained attention for its potential as a biocontrol agent for a diverse range of greenhouse pests, and it has already been commercially cultured in Europe for certain use.

  • ant-mimic
  • demography
  • habitat
  • Franklinothrips
  • prey specificity
  • predatory thrips

1. 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 pest control [7]. In USA, mite-predatory species Scolothrips sexmaculatus (Thripidae) and Leptothrips mali (Phlaeothripidae) are considered important biological control agents in almonds and apple orchards, respectively [8][9]. However, most of the predatory thrips species are confined within the Aeolothripidae.
Species of Franklinothrips (Thysanoptera: Aeolothripidae) are predatory on various other insects. These fast moving, ant-mimicking predatory thrips are widely distributed in the tropics, with 17 species described [1][10][11]. In addition, they are unusual among thrips due to the fact that most of them are habitually parthenogenetic and spin a silken cocoon [12]. Moreover, cocoon spinning is observed among the Aeolothripidae [13]. Among Franklinothrips, F. vespiformis is the most widespread and was noted considerably earlier as distinctive from most of the other Aeolothrips [14]. F. vespiformis has gained attention for its potential as a biocontrol agent for a diverse range of greenhouse pests, and it has already been commercially cultured in Europe for certain use [15][16]. F. orizabensis, a similar species, has also been documented as a biocontrol agent for thrips management in avocado plantations in California, USA [17].

2. Distribution

2.1. F. vespiformis

The native range is presumed to be Central America [10], although this species has been recorded subsequently in North and South America, Southeast Asia, Africa, Oceania, and Europe. F. vespiformis is distributed in different locations with references, as shown in Table 1, and distributed in wild and artificially released populations around the globe, as shown in Figure 1.
Insects 13 00108 g001 550
Figure 1. Known global distribution of Franklinothrips vespiformis. Red spots indicate locations with wild populations; green spots indicate artificial releases.
Table 1. The distribution of Franklinothrips vespiformis.

Region

Country (Location)

Reference(s)

North America

USA (Colorado)

[18]
 

USA (Arizona, California, Florida, Texas)

[10][19][20][21]
 

Mexico

[22][23][24][25]

Caribbean

Jamaica, Dominican Republic, Barbados

[24][25]
 

Puerto Rico

[25]
 

Trinidad and Tobago

[26][27]
 

St. Vincent Island, West Indies

[24][25]

Central America

Costa Rica, El Salvador, Nicaragua

[14][22][24]
 

Honduras

[28]
 

Panama

[14]

South America

Brazil

[29][30][31]
 

Paraguay

[24]
 

Peru (Miraflores)

[14]
 

Surinam

[12][25]

Asia

China (Taiwan)

[32]
 

China (Guangdong Yunnan, Guangxi)

[11]
 

India (Karnataka, Maharashtra, Kerala, Tamil Nadu)

[33][34]
 

Indonesia (Java)

[35]
 

Japan (Okinawa)

[36][37]
 

Thailand

[7][25]

Oceania

Australia (Queensland)

[10]
 

New Caledonia

[10]
 

Hawaii

[24]

Europe

France

[38][39][40]
 

Germany

[41]
 

Portugal

[24]
 

UK

[15][16][42]
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].

2.2. Other Franklinothrips Species

Compared with the pantropical F. vespiformis, the reported distribution of 16 other Franklinothrips spp. are relatively more localized. The current known distribution includes F. atlas Hood and F. megalops Trybom (mainly in Africa), F. basseti Mound and Marullo as well as F. variegatus Girault (Australia), F. brunneicornis Mound and Reynaud (New Caledonia), and F. fulgidus Hood and F. lineatus Hood (Brazil) [1]. Five additional species are noted from Asia, i.e., F. rarosae Reyes (Philippines), F. strasseni Mound and Reynaud (Nepal), F. suzukii Okajima (Taiwan), F. tani Mirab-Balou, Shi and Chen (China), and F. uttarakhandiensis Vijay Veer (India) [1]. Moreover, three additional species are recorded from Central America, i.e., F. tenuicornis Hood (Panama), as well as F. orizabensis Johansen and F. caballeroi Johansen (Mexico and Costa Rica). Furthermore, in USA, F. orizabensis, which closely resembles F. vespiformis, has been reported from Arizona, California, Colorado, Florida, and Texas [17][43].

3. 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].
Insects 13 00108 g002 550
Figure 2. Different stages of Franklinothrips vespiformis. (a) Egg; (b–d) Larva: (b) Newly emerged larva; (c) first instar larva; (d) second instar larva; (e–g) pupal stages: (e) pupa into cocoon; (f) Pupal stage 1; (g) pupal stage 2; (h) adult.

3.1. 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).

3.2. 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.

3.3. 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).

3.4. 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.
Insects 13 00108 g003 550
Figure 3. Sexual dimorphism in adult Franklinothrips vespiformis. (a) Female; (b) Male.

3.5. 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.

4. Life History

4.1. 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.
Table 2. Developmental parameters (days) of Franklinothrips vespiformis reared at different temperatures.

Development Parameter

Temperature (°C)

Reference(s)

21 °C

25 °C

27 °C

Life Stage (Days (±SE))

[15][16]

Eggs

16.06 ± 0.8

10.39 ± 0.1

9.7 ± 0.0

Larva 1

4.04 ± 0.12

2.03 ± 0.0

1.9 ± 0.0

Larva 2

3.9 ± 0.1

2.1 ± 0.0

1.1 ± 0.0

Prepupal and Pupal

12.5 ± 0.1

7.4 ± 0.1

5.3 ± 0.0

Unmated Males

24.3 ± 1.6

16.4 ± 1.3

9.0 ± 0.7

Mated Males

15.6 ± 1.9

12.8 ± 1.6

8.0 ± 0.6

Reproductive parameter (±SE)

Unmated Females

      

Pre-oviposition period (days)

1.6 ± 0.2

0.9 ± 0.2

2.4 ± 1.0

Mean total progeny

67.9 ± 21.4

71.2 ± 12.9

8.5 ± 3.8

Mean daily progeny

2.3 ± 0.2

4.1 ± 0.3

1.0 ± 0.1

Mean lifetime oviposition rate

154 ± 22.4

314 ± 44.1

105 ± 17.9

Mean daily oviposition rate

7.1 ± 0.4

18.1 ± 13.6

12.9 ± 1.3

Mated Females

      

Pre-oviposition period (days)

1.5 ± 0.2

0.9 ± 0.1

0.8 ± 0.2

Mean total progeny

35.2 ± 6.6

44.4 ± 11.8

8.4 ± 2.8

Mean daily progeny

1.8 ± 0.1

3.1 ± 0.2

0.9 ± 0.2

Mean lifetime oviposition rate

128 ± 25.5

220 ± 47.9

101 ± 14.7

Mean daily oviposition rate

6.5 ± 0.5

15.9 ± 1.1

12.8 ± 1.1

Population growth parameters (±SE)

Net reproductive rate (R0)

18.5 ± 0.18

33.3 ± 0.28

4.5 ± 0.07

Generation time (Tc)

49.1 ± 0.12

27.9 ± 0.05

24.2 ± 0.06

Intrinsic rate of increase (rm)

0.06 ± 0.0002

0.13 ± 0.0003

0.06 ± 0.0007

Finite rate of increase (λ)

1.06 ± 0.0002

1.14 ± 0.0004

1.07 ± 0.0007

Survival time in days (Td)

11.12 ± 0.03

5.16 ± 0.01

11.05 ± 0.12

4.2. 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].

4.3. 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.

4.4. 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 observed 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].

4.5. 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].

This entry is adapted from the peer-reviewed paper 10.3390/insects13020108

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