Contarinia caryafloralis Jiao, Bu & Kolesik, 2018

Jiao, Ke-Long, Wang, Hao, Huang, Jun-Hao, Han, Pei-Jin, Zhang, Long-Wa, Jiao, Xue, Wu, Zhi-Hui, Zhang, Jing, Wang, Yuan-Hong, Bu, Wen-Jun & Kolesik, Peter, 2018, A new species of Contarinia (Diptera: Cecidomyiidae) damaging inflorescence of Carya cathayensis (Juglandaceae) in China, Zootaxa 4442 (1), pp. 187-193 : 188-192

Contarinia caryafloralis Jiao, Bu & Kolesik sp. nov.

( Figs 1–16 ) http://zoobank.org/ urn:lsid:zoobank.org:act:F95FE170-973E-40D6-B395-8C762ECFB3AB

Material studied. Holotype: male, China, Zhejiang Province, Hangzhou, Lin’an District , Banqiao Town , Mengwuli Village (30.189166°N, 119.758867°E), collected 28.IV.2016 as larva and reared in laboratory by Xue Jiao, deposited in NKUM.

Paratypes. 5 males, 2 females, same data as holotype ; 7 males, 6 females, 9 larvae, same data as holotype but collected 19.IV.2016 ; 2 males, same data as holotype but collected 7.V.2015 .

Other material. 2 males, 7 females, China, Anhui Province, Xuancheng, Ningguo , Jialu Town (30.330593°N, 118.730039°E), collected 2–8.IV.2016 as larvae and reared in laboratory by Zhi-Hui Wu, deposited in NKUM.

Diagnosis. Most Contarinia species are monophagous ( Gagné & Jaschhof 2017), some feed on a few hosts from one respective plant family, and only the cosmopolitan pest C. maculipennis Felt is known to feed on hosts from several families ( Uechi et al. 2011). The new species differs from C. maculipennis in morphology and in the COI sequence (see DNA). In C. caryafloralis the female cerci are nearly three times as long as wide in ventral view, the aedeagus is constricted below apex and bulbous apically, and the male cerci are rounded while in C. maculipennis the female cercus is approximately five times as long as wide in ventral view, the aedeagus is evenly tapered and pointed apically, and the male cerci are triangular ( Gagné 1995). The new species can be distinguished from two North American species of Contarinia on Carya ( Gagné 2008) , the leaf-galling C. bulliformis Gagné and C. cucumata Gagné (both known from the larval stage only), by the shape of the anterior teeth on the larval spatula that are rounded in C. caryafloralis and acute in C. bulliformis and C. cucumata .

Description. Male ( Figs 1, 2, 4–7 ). Colour of abdomen yellow. Wing length 1.3–1.6 mm (n=15), 2.2–2.4 times longer than wide.

Head. Eye bridge 6–7 facets long, occipital protuberance small, in shape of truncated cone, length half of width at middle. Palpus 4-segmented, segments progressively longer ( Fig. 1 ). Antenna: scape and pedicel as wide as long, scape slightly larger than pedicel; flagellomeres binodal, 12 in number, first and second fused, circumfilar loops slightly uneven in length, longest loops of anterior whorl reaching distal edge of posterior node, longest loops of posterior whorl distinctly over-reaching end of neck ( Fig. 2 ).

Thorax. Wing ( Fig. 4 ) hyaline, setose, sparsely covered by narrow scales, R1 joining C slightly proximad of wing mid-length, R5 slightly arched backward distally, joining C at wing apex, Cu forked, Rs absent. Legs densely covered by narrow scales and sparse setae; tarsal claws ( Fig. 5 ) untoothed on all legs, empodia 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 by scattered scales, with anterior pair of trichoid sensilla, seventh tergite as for sixth but slightly narrower; eighth tergite as for seventh but considerably smaller; second through seventh sternites rectangular, with irregular but mostly one posterior row of long setae, more lateral and several central setae than on corresponding tergites, with anterior pair of closely set trichoid sensilla; seventh sternite as for sixth but slightly narrower; eighth sternite as for seventh but considerably smaller. Terminalia ( Figs 6, 7 ): gonocoxite elongate; mediobasal lobes low, broad; gonostylus slightly widened and setulose at basal 1/3, carinate at distal 2/3, sparsely setose, bearing strong comb-like tooth distally; aedeagus slender, tapering distally, constricted subapically, rounded apically; cerci mostly 3/4-length aedeagus (the length of cerci is variable in the mounted specimens, in some they are just slightly shorter than aedeagus), round, separated by deep U-shaped incision, with few long apical setae; hypoproct nearly as long as aedeagus, lobes narrow, divided by U-shaped incision slightly shorter than total length, bearing several short apical setae.

Female ( Figs 3 , 8–10 ). Wing length 1.5–1.8 mm (n=8), 2.2–2.4 times longer than wide.

Head. Flagellomeres cylindrical, slightly narrowed distally, first and second fused, first 1.2–1.3 times length of second, circumfila consisting of two transverse and two longitudinal bands ( Fig. 3 ).

Abdomen. First through seventh tergites and second through seventh sternites as in male, except for denser setae and scales, seventh sternite with irregular but mostly two posterior rows of long setae; eighth tergite slightly longer than seventh, with single posterior row of long setae, many central and lateral setae; eighth sternum unsclerotized. Terminalia: ovipositor long, retractable ( Fig. 8 ); cerci closely appressed, separated at distal half, about three times longer than wide at base in dorso-ventral view, evenly narrow in lateral view, slightly striate, bearing two pairs of unequally large setae basally and two pairs of equally large setae subapically, three to four pairs of small setae scattered in between and two pairs of small setae apically; hypoproct with two setae apically ( Figs 9, 10 ). Otherwise as in male.

Pupa. Colour: head and thorax yellowish brown and abdomen grayish yellow when containing full-grown adult, pale brown when empty. Length 1.6–1.8 mm long, 0.5–0.6 mm wide ( Hu et al. 2007).

Larva ( Figs 11, 12 , 14, 16 ). Colour light yellow. Length 1.2–1.6 mm long (n=9), 0.4–0.6 mm wide. Antennae tapered, 2.5–2.8 times as long as wide at base. Sternal spatula ( Fig. 11 ) with two anterior teeth, apices rounded, divided by deep V-shaped incision, lateral papillae adjacent to anterior part of spatula consisting of two groups, each made of two smaller asetose and one larger setose papillae. Ventral and sternal papillae asetose. Spiracles of eighth abdominal segment on posteriorly directed lobes. Terminal segment on either side with four terminal papillae: one stublike, remaining setose ( Fig. 12 ).

Etymology. The composite adjective “ caryafloralis ” means “of hickory flower” in Latin.

DNA. COI sequences obtained for two females and two larvae of Contarinia caryafloralis , collected with the holotype, were identical (GenBank accession numbers MH039840 – MH039843 , sequence length 636 bp). The similarity of C. caryafloralis to other described Contarinia spp. with available COI sequence was lower than 91%. The similarity to the only known polyphagous congener, the cosmopolitan pest C. maculipennis Felt (intraspecific similarity 98–100%), was 86–88%. This high level of genetic difference shows that C. caryafloralis is a species distinct from all Cecidomyiidae with published COI sequence.

Biology ( Figs 13–16 ). Infestation symptoms. The new species feeds on male and female inflorescences of Carya cathayensis . Infested female flower becomes swollen and malformed ( Figs 13–14 ), and does not produce seeds. Infested male infloresence has a shortened and curved rachis, the flowers are swollen and malformed ( Figs 15–16 ), and do not produce viable pollen. Following the departure of larvae, the inflorescences become necrotic and die ( Figs 13, 15 ).

Life cycle. Adults emerge from the soil beneath the host plant in late March and early April. The females lay eggs in the female flower buds and at the rachis of the male inflorescence. Following eclosion from the eggs, the larvae feed within the female flower buds ( Fig. 14 ) and among young anthers ( Fig. 16 ). The larval stage lasts two weeks ( Wu et al. 2004). Mature larvae leave the plant by jumping to the ground or fall to the ground within abscised inflorescence between late April and mid May. The larvae overwinter in the soil within a cocoon and pupate on the soil surface in March the following year. In Zhejiang and Anhui provinces, the species has one generation per year ( Hu et al. 2007; Ji & Guo 2011; Jun-Hao Huang & Long-Wa Zhang pers. comm.).

Geographical distribution and damage to crop. Currently, the new species is known to occur only in Zhejiang and Anhui provinces of China. It can cause substantial damage in orchards, with the proportion of infested flowers reaching 90% in male and 40% in female flowers in the outberak hot spots ( Wu et al. 2004; Hu et al. 2007; Ji & Guo 2011; Jun-Hao Huang & Long-Wa Zhang pers. comm.). In recent years the implementation of chemical and physical control measures reduced overall average fruit loss to 5%–8% in Anhui and 20% in Zhejiang provinces ( Hu et al. 2007; Ji & Guo 2011.).

Remarks. The plant genus Carya Nuttal contains 11–13 North-American ( Stone 1997) and 4 Asian species, with one of the North-American species, Carya illinoiensis (Wangenheim) K. Koch (pecan), grown commercially in several provinces of China ( Lu et al. 1999). The new gall midge is the first species of Cecidomyiidae known to feed on an Asian Carya sp. and the only one that feeds on the inflorescence of this plant genus. Sixty-three Cecidomyiidae species occur on the North-American Carya spp., belonging to six genera: two to Caryadiplosis Gagné , 56 to Caryomyia Felt , two to Contarinia , and one each to Gliaspilota Gagné , Harmandia Kieffer and Parallelodiplosis Rübsaamen ( Gagné 2008; Gagné & Jaschhof 2017). The majority of the North-American species induce galls on leaves, some on leaves and nut husk, one is an inquiline ( Gagné 2008). The two North-American Contarinia spp., both known from the larval stage only and thus in need of confirmation of their generic placement, are Contarinia bulliformis Gagné and Contarinia cucumata Gagné. Contarinia bulliformis causes a smooth, bubble-like swelling of the leaf mid-vein or petiole of Carya illinoiensis . Contarinia cucumata Gagné causes a hairy, cucumber-like gall on the leaf blade of Carya ovata (Miller) K. Koch , C. tomentosa (Poiret) Nuttal , C. pallida (Ashe) Engler & Graebner , C. cordiformis (Wangenheim) K. Koch , C. glabra (Miller) Sweet and Carya sp. ( Gagné 2008). The new species differs from C. bulliformis and C. cucumata in the shape of the larval spatula, see Diagnosis.

Figures

FIGURES 1–5. Contarinia caryafloralis. 1, 2, 4, 5: male; 3: female. (1) palpus, (2) 3rd flagellomere, (3) 3rd flagellomere, (4) wing, (5) front tarsal claw with empodium and pulvillus.

FIGURES 6–12. Contarinia caryafloralis sp. nov. 6, 7: male; 8–10: female; 11, 12: larva. (6) terminalia in dorsal view, (7) terminalia in ventral view, (8) postabdomen in lateral view, (9) end of ovipositor in ventral view showing cerci and hypoproct, (10) end of ovipositor in dorsolateral view showing cerci and partly hypoproct, (11) sternal spatula with adjacent papillae, (12) last two abdominal segments of larva in dorsal view.

FIGURES 13–16. Infestation of Chinese Hickory by Contarinia caryafloralis sp. nov. (13) damaged female inflorescence, (14) mature larvae feeding within female flower (infested flower was cut open to reveal larvae), (15) damaged male inflorescences, (16) young larvae feeding on male flowers.