Procontarinia fructiculi Jiao, Wang, Bu & Kolesik, 2018

Jiao, Ke-Long, Mo, Jian-You & Kolesik, Peter, 2018, A new species of Procontarinia (Diptera: Cecidomyiidae) damaging fruit of mango, Mangifera indica (Anacardiaceae), in China, Zootaxa 4413 (2), pp. 368-376 : 369-375

Procontarinia fructiculi Jiao, Wang, Bu & Kolesik sp. nov.

( Figs 1–24 )

http://zoobank.org/urn:lsid:zoobank.org:act:BA17861F-94E3-464C-9D70-3FD444CA71B9

Material studied. Holotype male, China, Guangxi Autonomous Region, Baise City, Youjiang District , Yongle Town , Xibeile Village , wanjiutun (23.98°N, 106.61°E, altitude 200 m), collected 30.III.2016 as larva and reared in laboratory by De-wei wei, deposited in NKUM.

Paratypes. 11 males, 28 females, 7 pupae, 15 larvae, same data as holotype.

Other material. 2 males, 10 females, same data as holotype but 14.III.2017 ; 30 males, 50 females, same data as holotype but collected 21–22.III.2017 ; 10 males, 20 females, same data as holotype but collected 9.IV.2017 .

Diagnosis. The new species differs morphologically from the other 15 known Procontarinia spp. in the mesobasal lobes on the male terminalia being heavily sclerotized and setulose, and in the combination of the following characters: a 4-segmented maxillary palpus; a protrusible ovipositor; female cerci nearly completely fused except apically; an extensive field of asetose sensory pores on the narrow and pointed aedeagus; short and wide male cerci that are nearly entirely fused; bare internodes of male flagellomeres; and two lobes of the larval sternal spatula being divided by a shallow incision. Procontarinia frugivora , the only other known fruit-feeding congener, differs from the new species in the following characters: the mesobasal lobes on the male terminalia bear spines with no setulae; circumfilar loops on the proximal node of the male flagellomere reach the base of the distal node (reaching the mid-length in P. fructiculi ); female cerci are completely fused; and the lobes of sternal spatula in the larva are divided by a deep incision.

Description. Male ( Figs 1–6 ). Colour: head and thorax brown, abdomen yellow brown. wing length 1.1–1.2 mm, width 0.5–0.6 mm (n = 12).

Head. Eye bridge 6–7 facets long on vertex. Maxillary palpus 4-segmented, segments progressively longer (see Fig. 12 for female palpus). Occipital protuberance present, small ( Fig. 5 ). Antenna with 12 flagellomeres, first and second fused; pedicel subglobular, slightly smaller than scape; flagellomeres binodal, each node with one whorl of circumfila; 3rd flagellomere ( Fig. 2 ) with asetose internode 0.6–0.7 times length of basal node, neck 1.0– 1.1 times length of distal node; circumfilar loops on proximal node reaching mid-length of distal node, circumfilar loops on distal node reaching end of neck.

Thorax. wing ( Fig. 1 ) hyaline, sparsely covered with narrow scales, R1 joining C slightly proximad of wing mid-length; R5 joining C at the wing apex, Rs reduced to small bulge on R5, Cu forked. Legs densely covered with narrow scales and sparse setae; tarsal claws ( Fig. 6 ) toothed on all legs; empodium as long as claws; pulvilli minute.

Abdomen. First through sixth tergites rectangular with single posterior row of long setae, several lateral and central setae, covered with scattered scales, anterior pair of trichoid sensilla; seventh tergite as sixth but slightly narrower; eighth tergite as seventh but considerably reduced in size; second through seventh sternites rectangular, with irregular row of long setae, lateral and central setae slightly denser than the ones on the corresponding tergites, and anterior pair of closely set trichoid sensilla; seventh sternite slightly narrower than sixth; eighth sternite as seventh but considerably reduced in size. Terminalia ( Figs. 3, 4 ): gonocoxite elongate; mediobasal lobes round, strongly sclerotized, densely covered with setulae; gonostyle stout, tapering towards distal tooth, basal third covered with dense microtrichia, rest with sparse short setae; cerci short, wide, nearly entirely fused, with slightly concave distal margin, bearing few long apical setae; hypoproct narrow, nearly as long as cerci, slightly concave distally, bearing several short setae distally; aedeagus narrow, distinctly longer than gonocoxite, gradually tapering, pointed apically, with dense field of small asetose sensory pores at distal 1/3 dorsally and sparser and slightly larger pores at distal 1/4 ventrally.

Female ( Figs 7–12 ). wing length 1.2–1.8 mm, width 0.6–0.7 mm (n = 28).

Head. Occipital protuberance present, small ( Fig. 10 ). Flagellomeres ( Fig. 7 ) cylindrical, 3rd flagellomere with node slightly constricted at mid-length, neck 1/3 length of node; circumfila appressed, consisting of interconnected two horizontal and two longitudinal bands.

Abdomen. First through seventh tergites and second through seventh sternites as in male, except for denser setae and scales; eighth tergite and sternite unsclerotized, with single posterior row and few scattered setae. Ovipositor ( Fig. 11 ) protrusible, when protruded 0.55–0.65 times as long as rest of abdomen; venter of ninth segment covered with dense setae, dorsum of ninth segment without vestiture; cerci ( Figs 8, 9 ) separated at distal 1/ 5, covered with dense short setae, few long setae scattered dorsally and few several medium-long thick setae distally; hypoproct ( Figs 8, 11 ) 5 times shorter than cerci, wide and rounded apically in ventral view, with pair of posterior setae. Otherwise as in male.

Pupa ( Figs 15–18 ). Colour orange brown. Body length 1.0 mm (n = 4) in male ( Fig. 15 ), 1.4–1.5 mm (n = 3) in female ( Figs 16–18 ). Antennal base with tiny angular horn; cephalic setae short and thin. Prothoracic spiracle obtuse, long and stout, gradually narrowing to apex, somewhat curved distally, trachea ending at apex.

Larva ( Figs 13, 14 , 19, 20 , 23, 24 ). Colour yellow to light orange. Length 1.8–2.2 mm (n = 15), width 0.5–0.6 mm (n = 15). Antennae tapered, 1.6–1.8 times as long as wide at base. Sternal spatula ( Figs 13 , 19, 20 ) with two anterior teeth, teeth bulged at base, divided by shallow U-shaped indentation; lateral papillae adjacent to anterior part of spatula consisting of one triplet and one single, all asetose. Terminal segment blunt posteriorly, with 8 papillae: one pair large corniform, one pair small with barely visible setae placed between the large corniform pair and two small setose laterad of the large corniform papillae ( Fig. 14 ). Area between corniform papillae slightly pigmented.

Egg. Spindle form, translucent, 0.15–0.25 mm in length.

Etymology. The specific name, fructiculi , is a noun in genitive case that means “of smaller fruit” in Latin, referring to the early development stage of fruit’s infestation by the new species.

DNA. COI sequences obtained for one female and one larva of P. fructiculi , collected with the holotype, were identical (GenBank accession numbers MG637425 and MG637426 , sequence length 446 bp). The sequences were compared to available COI sequences of other congeners: P. frugivora (sequences PFM-13, -14, -17, -18, - 19 in Medina et al. 2017), P. mangicola (GenBank accession numbers AB438110 – AB438112 ), P. mangiferae ( JQ823184 – JQ823234 ), P. matteiana ( JQ823235 – JQ823237 ), P. pustulata ( FJ820163 – FJ820172 ), P. robusta ( JX 110976 – JX 110979 ) and an undescribed Procontarinia sp. causing “low doughnut” galls on mango leaves in East Timor (3 unpublished sequences, see Kolesik et al. (2009) and Kolesik et al. (2017) for details). The similarity of P. fructiculi to the other species was as follows (in brackets are the intra-specific similarities of the particular species): 91.4–91.7% to P. mangiferae (99.7–100%), 89.5–89.8% to P. matteiana (99.7–100%), 88.3% to P. mangicola (100%), 86.3% to P. frugivora (100%), 85.8–86.1% to Procontarinia sp. from East Timor (99.6– 99.8%), 85.2–85.8% to P. robusta (99.0–99.6%) and 84.5–84.7% to P. pustulata (99.6–100%). The significant differences between the intra-specific and the inter-specific similarities suggest that P. fructiculi is a distinct species

Biology ( Figs 21–24 ). Infestation symptoms. Typically, young mango fruit of 2–5 mm diameter is found infested by larvae of the new species, while fruit larger than 5 mm has not been found infested yet. Between one and 8 larvae feed inside the mesocarp, each living within a separate larval chamber ( Fig. 23 ). Prior to larvae leaving the fruit, the infestation cannot be recognized by visual examination of the fruit’s surface. Mature larvae create an escape tunnel 0.4–0.6 mm in diameter. Following the departure of larvae for pupation in the soil, the tissue surrounding the escape tunnel becomes necrotic and turns dark ( Figs 22, 24 ), the infested fruit keeps growing for some time, becomes deformed and falls prematurely to the ground.

Life cycle. The female lays eggs in the flower at the base of the ovary ( Fig. 21 ). Following eclosion from the egg, the larva feeds within the mesocarp of the developing fruit ( Fig. 23 ). The mature larva leaves the fruit through a hole on fruit’s surface ( Figs 22, 24 ) and enters the soil where it creates a cocoon prior to pupation for overwintering. The pupal stage lasted 8–10 days under laboratory conditions. Most adults die the next day. In 2016 in Baise, Guangxi Autonomous Region, China, adults emerged from mid March to early April. Baise has a monsoon-influenced, humid subtropical climate, with short, mild, and dry winters, and long, hot and humid summers.

Damage to crop. From 2015 to 2017, an outbreak of the new species was recorded in Baise. The prevalence of infested trees was high, often reaching 100% locally. An average fruit set reduction was estimated as 65% (locally up to 85%) resulting in a considerable economic loss in the affected areas (De-wei wei pers. comm.).

Geographical distribution. Currently, the new species is known to occur in the Baise city district, and around towns of Baiyu, Tianyang Country and Xiangzhou, Tiandong Country, both in the vicinity of Baise city (De-wei wei pers. comm.).

Remarks. Procontarinia fructiculi differs from the other 15 described Procontarinia spp. in morphology, COI sequence and infestation symptoms. while all Procontarinia spp. feed on mango, only P. fructiculi and P. frugivora feed on the fruit. In P. fructiculi the oviposition takes place during flowering, the larvae live inside the fruit till it grows to about 2–5 mm in diameter, then they leave for pupation in the soil while the infested fruit continues growing for a while and then falls prematurely to the ground. In P. frugivora , known from the Philippines only, the infestation occurs at a slightly later state of the fruit’s development. Following the larvae leaving for pupation in the soil, the fruit continues growing but falls to the ground before ripening (Gagné & Medina 2004; Medina et al. 2017). See Diagnosis for morphological comparison between P. fructiculi and P. frugivora . Additionally to the 21 previously described Cecidomyiidae spp. associated with mango (Gagné & Jaschhof 2017) and the new species, there are several undescribed species feeding on leaves and inflorescence (Talukdar 2007; Kolesik et al. 2017), and one species that was found forming blisters on fruit and caused considerable mango production losses in the Indian state of Karnataka in 2015 and 2016 (Kalleshwaraswamy et al. 2016). This Indian fruit-feeding gall midge has not yet been identified to species level and efforts are being made to rear a representative insect series to enable the identification (Kalleshwaraswamy pers. comm.).

Previously, two Procontarinia spp. were found feeding on mango plants in China: P. mangicola inducing lesions on leaves in Guangxi Autonomous Region and P. robusta inducing conical galls on leaves in Fujian Province. The two species differ from each other and from P. fructiculi in several morphological characters. Procontarinia mangicola (see Shi (1980) and Harris & Schreiner (1992) for morphology) has a short ovipositor, a robust and distally broadened aedeagus, non-sclerotized and setulose mediobasal lobes on the male terminalia, and a larval sternal spatula that is bilobed, with a deep incision between the lobes. Procontarinia robusta (see Li et al. (2003) and Cai et al. (2013) for morphology) has mostly three-segmented (sometimes four-segmented) palpi, a short ovipositor, undivided female cerci, a setulose internode of the male flagellomere, no mediobasal lobes on the male terminalia, and a larval sternal spatula that is trilobed, with a prominent central lobe and minute lateral lobes. Procontarinia fructiculi has four-segmented palpi, a long ovipositor, shallowly divided female cerci, a bare internode of the male flagellomere, a slender and conical aedeagus, sclerotized and setulose mediobasal lobes on the male terminalia, and a larval sternal spatula that is bilobed, with a shallow incision between the lobes.

Figures

FIGURES 1–6. Procontarinia fructiculi. Male. (1) wing, (2) 3rd flagellomere, (3) terminalia in dorSal view, (4) terminalia in ventral view, (5) occipital protuberance on head, (6) tarSal claw with empodium.

FIGURES 7–14. Procontarinia fructiculi. 7–12: female, 13–14: larva. (7) 3rd flagellomere, (8) end of ovipoSitor in ventral view Showing cerci and hypoproct, (9) cerci in dorSal view, (10) occipital protuberance on head, (11) poStabdomen in lateral view, (12) maxillary palpuS, (13) Sternal Spatula with adjacent papillae, (14) poSterior Segment in dorSal view.

FIGURES 15–20. Procontarinia fructiculi. 15: male pupa, 16–18: female pupa, 19–20: larva. (15) ventral view, (16) ventral view, (17) lateral view, (18) dorSal view, (19) whole body in ventral view, (20) anterior end in ventral view with head and Spatula.

FIGURES 21–24. InfeStation of mango by Procontarinia fructiculi. (21) female laying eggS in flower on baSe of ovary, (22) normal fruit (upper left corner) and infeSted fruit with larval eScape holeS (centre), (23) Split open fruit to Show meSocarp with larvae within larval chamberS, (24) larval eScape holeS and larva leaving infeSted fruit.