Completely predatory development is described in a braconid wasp

The presents study indicates that Bracon predatorius generally oviposits during early stages of gall development (Fig. 1d) on galls induced by Aceria doctersi mostly on tender leaves (Fig 1a–c) and rarely on petioles and stems¹³. The number of B. predatorius larvae in parasitized galls ranged from 1–27 (n=93). Eighty-five percent of the examined galls (n=109) were parasitized by B. predatorius. Different development stages of larvae (Fig. 1f,g) and pupae (Fig. 1i) of B. predatorius were found together in some large galls (n=31) (Fig. 1i), which suggests multiple oviposition at different stages of gall development. Dissection of leaf galls two hours after oviposition by B. predatorius always revealed only a single egg (n=8). No live A. doctersi individuals were found close to the parasitoid wasp pupae (Fig. 1h). Aceria doctersi galls parasitised by B. predatorius have also been found in Kodakara (Thrissur district, Kerala) about 100 km away from the type locality in Kozhikode.

The larval stages of B. predatorius feed on both juvenile and adults of A. doctersi (Fig 2d–f, Supplementary Video 1) which usually remain close to the erineal hairs on which they feed¹⁶; no egg predation occurs. Young larvae of B. predatorius wriggle through in between erineal hairs (Supplementary Video 1). They use their sickle-shaped mandibles (Fig 3b–e) to hunt mites (Supplementary Video 1). Continuous outward and inward movement of mandibles of B. predatorius larvae occurs along with the wriggling movement (Supplementary Video 1). The final instar larvae of B. predatorius are the most active and they feed voraciously at the rate of 5–7 A. doctersi individuals/min (n=8) (Supplementary Video 1).

Unattacked galls were significantly smaller than those containing B. predatorius (means 217 and 595 respectively; p<0.0001) (Fig. 2a) as were galls containing only a single Bracon juvenile (p<0.0001). However, galls without Bracon larvae contained significantly more mites than either all attacked galls (means 503 and 194 respectively; p<0.0001) (Fig. 2b) or those attacked by only one Bracon larvae (p<0.0001). Considering only attacked galls with numbers of Bracon and gall volume as explanatory variables and including an interaction term, we found that the number of mites was highly significantly negatively correlated (p<0.0001) with the number of Bracon present (Fig. 2c) but gall volume and the interaction terms were both insignificant (p=0.94 and p=0.58 respectively).

Bracon predatorius females oviposit singly within leaf galls of size 1.5–2.4 mm during morning (0800–0900 h) and evening hours (1700–1800 h) (Fig. 1d). The searching behaviour of the female B. predatorius is completed in 1–3 minutes (n=8). The oviposition is completed in 4–6 minutes (n=8). Adult females of B. predatorius oviposit through the adaxial side of the gall-bearing leaves. The egg is deposited in spaces between two adjacent erineal hairs. The B. predatorius egg is yellow with rounded edges (Fig. 1e) and is almost as long as the mite, A. doctersi. The first instar larva of B. predatorius is transluscent and wriggles inside spaces that occur in the galls due to puckering and crinkling of the leaf tissue that includes the erineal hairs. These erinea serve as the source of nutrition for populations of A. doctersi. The final instar larva of B. predatorius is 1.8–2.1 mm long, dull-white with yellowish head capsule and 13 body segments (Figs 1f,g, 2d–f). The body of the larva of B. predatorius bears dorsal protuberances and is densely setose (Figs. 1f,g, 2d–f, 3e). The larvae of B. predatorius pupate in the space occupied by the final instar larva (Fig 1h,i), and pupae are oriented in sagittal as well as transverse planes (Fig. 1i). Adults of B. predatorius exit by cutting a hole with their mandibles along the dorsal side of the gall.

The wasp larvae possess highly derived cephalic structures: massive, elongate and overlapping mandibles that lack a comb of serrations, and otherwise strongly sclerotised epistoma and well-developed antennae and palps. The cephalic structures of the final instar larva (Fig 3a–e) differ markedly from those of typical ectoparasitic braconines¹⁷. The epistoma is robust, though weakened medio-dorsally possibly allowing some flexibility, ∩-shaped (Fig. 3a). Both pairs of mandibular processes are large and robust (Fig. 3a). The mandibles are large, heavily sclerotised, with small swollen base and long blades, completely overlapping and without serrated combs (Fig 3a–e). The hypostoma is greatly reduced and the short arms converging ventrally (Fig. 3a). Stipital sclerites are strongly curved, L-shaped (Fig. 3a). The cardo is apparently lacking, or if present, indistinct and weakly sclerotised (Fig. 3d). Antennae, and both maxillary and labial palps are relatively large (Fig. 3a).

Systematic entomology

Hymenoptera Linnaeus, 1758

Apocrita Gerstaecker, 1867

Ichneumonoidea Latreille, 1802

Braconidae Nees 1811

Bracon Fabricius 1804

Bracon predatorius Ranjith & Quicke sp. nov. Figures 4 and 5

Diagnosis

Body yellow (Fig. 4a). Antenna with 17 flagellomeres. Mandible twisted, two teeth visible in anterior view (Fig. 4b). Face medially smooth, shiny, rest aciculate, sparsely setose (Fig. 4b). Malar groove absent (Fig 4b,d). Frons shiny with distinct midlongitudinal groove (Fig. 4c). Head smooth, evenly rounded posteriorly in dorsal view (Fig. 4c). Median and lateral lobes of mesoscutum largely glabrous, setose posteriorly (Fig. 4f); notauli only indicated anteriorly. Scutellar sulcus narrow, divided by eight carinae. Propodeum smooth with an incomplete midlongitudinal carina, sparsely setose laterally (Fig. 5a). Length of fore wing veins 3RSb: 3RSa: r-rs = 15: 5: 3 (Fig. 5e). Length of fore wing veins 2RS: 3RSa: rs-m = 5: 5: 3. Tarsal claws with pointed basal lobe. Metasoma largely smooth and shiny with seven exposed, sparsely setose, tergites (Fig 5c,d). Median area of first tergite largely smooth and shiny, dorso-lateral carina strong and lamelliform, dorsal carina strong with angulate projection subbasally (Fig. 5b). Second metasomal suture sinuate, strongly crenulate (Fig. 5c); Tergite 4–7 rugose, sparsely setose. Tergite 2–6 with distinct antero-lateral area. Ovipositor slender, darkened apically, with an indistinct dorsal nodus and ventral serrations (Fig. 5f).

Material examined

Holotype female, “INDIA: Kerala, Malappuram, Calicut University Botanical Garden, 4.iii.2020, emerged from leaf galls of Cinnamomum verum induced by Aceria doctersi, ex. A.P. Ranjith” (ZSIK-ZSI/WGRC/IR.INV-14852). Paratypes, Two female paratypes and one male paratype with same data as holotype (ZSIK) 20 females and 19 males with same data of holotype (Department of Zoology, University of Calicut (DZUC)).

Description

Holotype, female.

Length of body 2.1 mm, of fore wing 1.7 mm, and of ovipositor 0.6 mm.

Head

Antenna with 19 flagellomeres. Terminal flagellomere strongly acute. Median flagellomeres normal in dorsal view. First flagellomere 1.2 times length of second and third flagellomeres respectively, first flagellomere 3.6 times as long as wide. Mandible twisted, two teeth visible in anterior view (Fig. 4b). Inter-tentorial distance: tentorio-ocular distance = 1.5:1. Inter-tentorial distance: height of clypeus = 3:1. Face medially smooth, shiny rest aciculate, sparsely setose (Fig. 4b). Height of eye: shortest distance between eyes: width of head = 1:1.1:2.3. Oculo-antennal groove absent. Malar groove absent. Malar space 0.95 times basal width of mandible. Frons shiny with distinct midlongitudinal groove (Fig. 4c). Stemmaticum triangular forming equilateral triangle. Head evenly rounded posteriorly in dorsal view (Fig. 4c). Length of eye 1.5 times as long as temple in dorsal view. Shortest distance between posterior ocelli: transverse diameter of posterior ocellus: shortest distance between posterior ocellus and eye = 4:4:11.

Mesosoma

Mesosoma 1.3 times longer than maximum height, largely smooth, shiny (Fig. 4e). Medial lobe and lateral lobes of mesoscutum glabrous, setose posteriorly (Fig. 4f). Pronotum smooth (Fig. 4d). Notauli only indicated anteriorly (Fig. 4f). Scutellar sulcus narrow, divided by eight carinae. Scutellum smooth (Fig. 4f). Median area of metanotum large, smooth, with distinct midlongitudinal and lateral carina anteriorly and stub like longitudinal carina submedially (Fig. 5a). Propodeum smooth with an incomplete midlongitudinal carina, sparsely setose laterally (Fig. 5a).

Wings

Fore wing, Vein 2-M 1.8 times 3RSa. Vein 1-M straight. Vein (RS+M)a straight (Fig. 5e). Vein rs-m without bulla. Vein 1RS forming an angle of 55° with vein C+SC+R. Vein m-cu 0.6 times 1-M. Vein 1cu-a interstitial. Hind wing vein R1 1.5 times length of 1r-m. Apex of vein C+SC+R with one hamulus. Base of hind wing without medium sized glabrous area distal to vein cu-a on posterior half of cell.

Legs

Claws with pointed basal lobe. Fore tibia with transverse apical row of thickened bristles. Lengths of hind femur:tibia:basitarsus = 32:46:32.

Metasoma

Metasoma largely smooth and shiny with six exposed, sparsely setose, tergites (Fig 5b–d). First metasomal tergite 0.86 times as long as wide (Fig. 5b). Second tergite rugose on basal 0.3, rest smooth, 3.1 times wider than medially long, without triangular mid basal area, with a pair of sub lateral depressed area (Fig. 5c). Second metasomal suture sinuate medially, strongly crenulate; third tergite rugose, 4.0 times wider than medially long, without sublateral grooves and with antero-lateral areas defined. Tergite 4–7 rugose, sparsely setose. Tergite 2–6 with distinct antero-lateral area (Fig. 5c). Hypopygium acute apically reaching end of metasomal tergites (Fig. 5d). Ovipositor sheaths 1.2 times longer than hind tibia. Ovipositor slender, darkened sub apically, dorsal valve with an indistinct nodus and serrations ventrally (Fig. 5f).

Colour

Body yellow (Fig. 4a) except eye grey, stemmaticum silvery, antenna, tip of mandible, anterior 0.5 of pterostigma, wing veins, telotarsus, metasomal suture 2–4, ovipositor sheath light brown to dark brown.

Male

Similar to female.

Etymology

The specific epithet refers to its unusual feeding behaviour.

Remarks

Determination of a new species within the cosmopolitan genus Bracon was challenging, indeed there are undoubtedly thousands of undescribed Bracon species worldwide. The keys published for the Indian and Chinese species of Bracon^18,19 were unhelpful. The species comes close to B. keralense Sheeba & Narendran in having propodeum with midlongitudinal carina not extending to middle of propodeum. Apart from the differences mentioned in the comparative affinities it differs from B. keralense in having following characters; length of eye 1.5 times as long as temple in dorsal view (vs length of eye 2.30 times as long as temple in B. keralense), intertentorial distance 1.5 times tentorioocular distance (vs as long as in B. keralense), first metasomal tergite with depressed medial area (vs with elevated medial area in B. keralense). The highly derived larval cephalic structures, which are presumed adaptations to its predatory lifestyle, also differ from the mandibles of all other braconine larvae which have been described to date.

Comparative affinities

The cosmopolitan genus Bracon⁷ includes 17 subgenera and more than 800 described species²⁰. For historical reasons, its subgeneric classification is largely based on the Palaearctic fauna and is unreliable especially for extralimital taxa^21,22,23. Bracon predatorius sp. nov. comes close to the subgenus Orthobracon Fahringer although with some distinct differences in the sculpture of propodeum and metasoma, and therefore we provisionally include it under Orthobracon. Of the described Indian fauna, B. predatorius comes close to B. keralense reared from the leaf galls on Cinnamomum malabatrum (Burm.f.) J.Presl (Lauraceae) induced by an unnamed Cecidomyiidae²⁴, but B. predatorius differs in having the face without medial longitudinal ridge, notauli indistinct posteriorly, scutellar sulcus divided by eight carinae, metanotum with midlongitudinal carina anteriorly, second metasomal tergite without smooth, parallel sided medio-basal area, ovipositor without dorsal nodus and ventral serrations.

Source: Ecology - nature.com