Hallodapus Fieber, 1858

Yasunaga, Tomohide, Tamada, Yui, Hinami, Haruka, Miyazaki, Ayana, Duwal, Ram Keshari & Nagashima, Tetsuya, 2019, Taxonomic review for the Asian taxa of plant bug tribe Hallodapini, with emphasis on stridulatory mechanism (Hemiptera: Heteroptera: Miridae), Acta Entomologica Musei Nationalis Pragae (Acta. Ent. Mus. Natl. Pragae) 59 (1), pp. 71-99 : 82

Hallodapus Fieber, 1858

Diagnosis. Body rather small, elongate, slender but female predominantly brachypterous ( Figs 19–24 ); dorsum weakly shining, impunctate, with sparsely distributed, pale, simple, upright setae; general coloration basically brown, with pale or white maculae on corium and/or clavus, lacking greenish tinge; more or less prognathous head; eye small, contiguous to flattened pronotum collar; stridulatory device involving dorsobasal surface of metafemur and embolial edge present both in macropterous and brachypterous forms; scent efferent system small; parempodia setiform ( Figs 91 , 129 ); pygophore usually smooth, rarely with a pygophoral spine (in H. spinosus sp. nov. and H. susurratus sp. nov.); left paramere developed ( Figs 85 , 130 ); endosoma slender, elongate or sometimes very long, with well-marked secondary gonopore ( Figs 94 , 107 , 178–180 ); ovipositors short, with developed apices; posterior wall simple; sclerotized ring small but clearly rimmed ( Figs 201–209 ).

Distribution. Known widely from the Old World (Palearctic Region to southern Africa, northeast to Japan, Korea and Russian Far East, and Oriental Region southeast across Wallacea to New Guinea and northern Australia); most speciose in the Ethiopian and Oriental Regions (SCHUH 2013).

Discussion. This is the most speciose genus in the tribe Hallodapini , including about 50 valid species from the Old World. Majority of them are thermophilic, known predominantly from tropical and subtropical climate zones. All Hallodapus species we have examined ( Table 1 ) are equipped with the distinct stridulatory device (e.g., Figs 41–53 , 77–78, 81–84 ). Our recent attempt successfully detected stridulation in two Japanese species, H. centrimaculatus (approx. 2,100 Hz) and H. ravenar (800 Hz), in laboratory observation ( Fig. 32 ).As exhibiting significant interspecific variation, extent and shape of MFP can be regarded as the effective key character for species identification (as in Figs 40–53 ). The stridulatory mechanism is equally possessed by both male and female adults (cf. Figs 40–46, 48–49 ) but absent in immature forms ( Fig. 50 ).

In addition to stridulation, we observed and videoed remarkable intraspecific conflict occasionally occurring between males of each Hallodapus centrimaculatus and H. ravenar in laboratory condition. Thus far as we recognized, no previous work has ever reported such fighting behavior for the Miridae . We have not yet clarified when and why they fight, and further continuing investigation is required to elucidate the meaning of their conflict. Some of our sample movies are available from the the websites mentioned in Online supplimentary data (p. 98).

All Hallodapus congeners are presumed to be epigeic, inhabiting ground densely covered with weeds and/or shrubs (cf. Figs 1−2 ). YASUNAGA (2001) considered that (at least Japanese) species of Hallodapus are predaceous. During our laboratory observation, four Japanese species, H. centrimaculatus , H. kyushuensis , H. linnavuori , and H. ravenar , did not attack or prey on live tiny arthropods but prefer to feed on the cadavers of various insects and spiders (sometimes much larger than these hallodapines) as well as birds’ droppings. This evidence could imply that Hallodapus species are scavengers instead of predators. The eggs and oviposition were for the first time confirmed for H. centrimaculatus and H. ravenar ( Figs 7–8 , 108–109 ); the female adults of both species were found to oviposit near the roots of weeds ( Fig. 6 ).

Figures

Figs 19–24. Habitus images of Asian Hallodapus species. 19 – H. spinosus sp. nov., ♁ (Nakhon Ratchasima, Thailand); 20 – H. brunneus (Poppius, 1915), ♁ (Ishigaki Island, Japan). 21–24 – Hallodapus species collected by engine vacuum netting method in Nagasaki, Japan: 21 – H. centrimaculatus (Poppius, 1909); 22 – H. linnavuorii Miyamoto, 1965; 23 – H. kyushuensis Miyamoto, 1965; 24 – H. ravenar (Kirkaldy, 1902).

Figs 86–100. Scanning electron micrographs for Japanese Hallodapus species (Nagasaki). 86–94 – Hallodapus centrimaculatus (Poppius, 1909): 86 – brachypterous ♀, dorsal habitus; 87 – ditto, ventral habitus; 88 – thorax, left lateral view; 89 – ♀ FWS; 90 – ♀ MFP; 91 – ♁ pretarsus (hind leg); 92 – ♁ head and thorax, right lateral view; 93 – ♁ stridulatory device (right); 94 – pygophore, right lateral view. 95–97 – H. kyushuensis Miyamoto, 1965, ♁: 95 – left lateral habitus; 96 – FWS; 97 – MFP. 98–100 – H. linnavuorii (Miyamoto, 1965), brachypterous ♀: 98 – stridulatory device (left); 99 – FWS; 100 – MFP.

Figs 116–130. Scanning electron micrographs for new Hallodapus species. 116–118 – H. jingfui sp. nov., ♁ (Taiwan): 116 – dorsal habitus; 117 – FWS; 118 – MFP. 119–124 – H. spinosus sp. nov., ♁ (Thailand): 119 – dorsal habitus; 120 – left lateral habitus; 121 – scent efferent system; 122 – FWS; 123 – MFP; 124 – pygophore with exposed endosoma. 125–130 – H. susurratus sp. nov., ♁ (Thailand): 125 – dorsal habitus of anterior body; 126 – FWS; 127 – MFP; 128 – thoracic pleura; 129 – pretarsus (hind leg); 130 – pygophore.

Figs 71–85. Scanning electron micrographs for Asian hallodapines.71–72 – Cleotomiris yamadakazi Yasunaga, 2012, paratype♁ (Thailand): 71 – thorax, left lateral view; 72 – smooth dorsal surface of metafemur.73 – Cleotomiroides tobii Yasunaga, 2012, paratype♁ (Thailand), head and thorax, left lateral view. 74–76 – C. ishikawachui sp. nov., holotype♁: 74 – head and thorax, left lateral view; 75 – basal part of metafemur; 76 – pretarsus (hind leg). 77–82 – Hallodapus albofasciatus (Motschulsky, 1863) (Thailand): 77 –♁ FWS; 78 –♁ MFP; 79 – metatarsus; 80 – brachypterous♀, habitus; 81 –♀ FWS; 82 – ♀ MFP. 83–85 – H. sibiricus Poppius, 1912,♁ (Russian Primorsky): 83 – FWS; 84 –MFP; 85 – metatarsus; 86 – apical part of pygophore, caudal view.

Figs 101–115. Scanning electron micrographs for Hallodapus species. 101–109 – H. ravenar (Kirkaldy, 1902) (Nagasaki, Japan): 101 – brachypterous ♀, ventral habitus; 102 – ♀ FWS; 103 – ♀ MFP; 104 – rudimental hindwing of brachypterous ♀; 105 – mesofemoral trichobothria; 106 – metafemoral trichobothrium; 107 –♁ apex of pygophore with exposed endosoma, ventral view; 108 – egg; 109 – operculum. 110–111 – H. brunneus (Poppius, 1915): 110 – ♀ FWS; 111 – ♁ MFP. 112–113 – H. fasciatus (Poppius, 1909), ♁: 112 – FWS; 113 – MFP. 114–115 – H. sp., ♀ (Tianjin, China): 114 – dorsal habitus; 115 – stridulatory device (left).

Figs 174–180. Male genitalia of Hallodapus species. 174–176 – H. jingfui sp. nov., holotype: 174 – pygophore with phallotheca, ventral view; 175 – left paramere; 176 – endosoma. 177–178 – H. brunneus (Poppius, 1915) (Ishigaki Island, Japan): 177 – phallotheca; 178 – endosoma. 179 – H. linnavuorii (Miyamoto, 1965) (Nagasaki, Japan), endosoma; 180 – H. kyushuensis (Miyamoto, 1965) (Okinawa, Japan), endosoma. Scale bars 0.2 mm.

Figs 201–217. Female genitalia and wing structures (216–218) of Asian hallodapines. 201–202 – Hallodapus brunneus (Poppius, 1915) (Yonakuni Island, Japan): 201 – bursa copulatrix with gonapophysis I, ventral view; 202 – gonapophysis II. 203 – H. centrimaculatus (Poppius, 1909) (Nagasaki), bursa copulatrix with gonapophysis I. 204–205 – H. kyushuensis (Miyamoto, 1965) (Okinawa Island): 204 – bursa copulatrix with gonapophysis I; 205 – gonapophysis II. 206–208 – H. linnavuorii (Miyamoto, 1965) (Nagasaki): 206 – bursa copulatrix; 207 – apex of gonapophysis I; 208 – gonapophysis II. 209 – H. ravenar (Kirkaldy, 1902) (Nagasaki), bursa copulatrix with gonapophysis I. 210–211 – Alloeomimella muiri (Schuh, 1984) (Nakhon Nayok, Thailand):210 – bursa copulatrix; 211 – gonapophysis II. 212–213 – Acrorrhinium kranion Yasunaga,Yamada &Artchawakom,2013 (Nakhon Ratchasima, Thailand): 212 – gonapophysis I; 213 – gonapophysis II; 214–215 – Cleotomiroides tobii Yasunaga, 2012 (Nakhon Ratchasima): 214 – gonapophysis I; 215 – gonapophysis II. 216 – forewing of Hallodapus kyushuensis (Nagasaki). 217 – dorsal habitus of H. linnavuorii (Nagasaki).

Figs 40–55. Stridulatory device (MFP, except for FWS on 55) of Asian hallodapines observed by a compound microscope. 40–41 – Hallodapus brunneus (Poppius, 1915); 42–43 – H. centrimaculatus (Poppius, 1909); 44 – H. fasciatus (Poppius, 1909) (Nakhon Nayok, Thailand); 45–46 – H. kyushuensis Miyamoto, 1965; 47 – H. spinosus sp. nov.; 48–50 – H. ravenar (Kirkaldy, 1902); 51 – H. linnavuorii Miyamoto, 1965; 52 – H. jingfui sp. nov.; 53 – H. sibiricus Poppius, 1912 (S. Primorsky, Russia); 54 – Alloeomimella muiri (Schuh, 1984); 55 – Wygomiris paveli sp. nov.

Fig. 32. Sound patterns emitted by two Japanese Hallodapus species (detected with courtship behavior).

Figs 1–8. Habitats of epigeic hallodapine plant bugs (1–2), sampling method (3–5), and oviposition (6) and eggs of Japanese Hallodapus species (laboratory observation) (7–8). 1 – typical habitat of Hallodapus centrimaculatus (Poppius, 1909), H. kyushuensis Miyamoto, 1965 and H. linnavuorii Miyamoto, 1965 in Nagasaki, Japan; 2 – habitat of Alloeomimella muiri (Schuh, 1984), Hallodapus albofasciatus (Motschulsky, 1863), H. ravenar (Kirkaldy, 1902) and H. spinosus sp. nov. in Nakhon Nayok, Thailand; 3–5 – engine vacuum netting method for sampling ground-inhabiting heteropterans; 6 – brachypterous female of H. centrimaculatus ovipositing into weed (Artemisia sp.) stem near root; 7 – eggs (opercula) of H. centrimaculatus; 8 – egg of H. ravenar (same egg as in Figs 108–109).