Research Article |
Corresponding author: Fedor V. Konstantinov ( fkonstantinov@gmail.com ) Academic editor: Alfred Wheeler
© 2018 Fedor V. Konstantinov, Nikolay Simov.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Konstantinov FV, Simov N (2018) Review of the subgenus Plumiger of Myrmecophyes, with description of a new species (Heteroptera, Miridae, Halticini). ZooKeys 796: 215-239. https://doi.org/10.3897/zookeys.796.21877
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The Caucasian subgenus Plumiger Horváth, 1927 of the halticine genus Myrmecophyes Fieber, 1870 is revised. A key, updated diagnoses, and data on distribution are given for the subgenus and its four species, including M. tomi sp. n. (Georgia and Dagestan), and the previously unknown male of M. armeniacus Drapolyuk, 1989. Illustrations of the male and female genitalia, photographs of the dorsal habitus, and SEM micrographs of selected structures are provided for all species of the subgenus.
Alpine meadows, Caucasus, diagnosis, female genitalia, key to species, male genitalia, systematics
Myrmecophyes Fieber, 1870 is a distinctive and strikingly myrmecomorphic halticine genus comprising 30 currently recognized species (
Recent collecting by the authors from the Armenian Highlands produced a substantial number of Myrmecophyes spp., including long series of Myrmecophyes (Plumiger) armeniacus Drapolyuk, 1989, originally described from two females. Subsequent examination of holdings from the Zoological Institute, Russian Academy of Sciences (
The present paper provides the description of a new species, a key to males and females, a revised diagnosis, and a redescription of the subgenus. A diagnosis, description, measurements, distributional information, a dorsal habitus photograph, and illustrations of male and female genitalia are given for each species of the subgenus.
We are delighted to dedicate this paper to our eminent colleague Dr. Thomas J. Henry on the occasion of his 70th birthday. During a long and distinguished career at the USDA, c/o Smithsonian National Museum of Natural History, Tom Henry has made singular contributions to our knowledge of the Heteroptera worldwide. Despite his many duties, Tom always manages to find time to help his colleagues in their studies and to provide an energetic and supportive environment to all researchers working with the USNM Heteroptera collection.
Slightly more than 600 specimens were examined for this study. All specimens are retained in the Zoological Institute, St. Petersburg, Russia (
Unless otherwise stated, all measurements are in millimeters. Measurements shown in Table
Measurements (mm). Abbreviations: Clyp-Wing – distance between apex of clypeus and apex of wing pad in dorsal view, Head Length – distance between apex of clypeus and the highest point of vertex, AntSeg1 – AntSeg2 – length of antennal segments I and II, InterOcDi – width of vertex between inner margins of eyes in dorsal view.
Species | Length | Width | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Body | Clyp-Wing | Head | Pronotum | Tibia3 | AntSeg1 | AntSeg2 | Head | InterOcDi | Pronotum | ||
Myrmecophyes armeniacus | |||||||||||
♂♂ (n = 5) | Mean | 3.46 | 2.07 | 0.55 | 0.65 | 3.27 | 0.48 | 0.67 | 1.15 | 0.56 | 0.85 |
SD | 0.11 | 0.07 | 0.03 | 0.02 | 0.11 | 0.02 | 0.03 | 0.02 | 0.02 | 0.03 | |
Range | 0.25 | 0.16 | 0.09 | 0.04 | 0.28 | 0.04 | 0.07 | 0.04 | 0.04 | 0.07 | |
Min | 3.40 | 2.02 | 0.50 | 0.64 | 3.08 | 0.46 | 0.64 | 1.13 | 0.53 | 0.81 | |
Max | 3.65 | 2.18 | 0.58 | 0.67 | 3.36 | 0.50 | 0.71 | 1.17 | 0.57 | 0.88 | |
♀♀ (n = 5) | Mean | 3.99 | 2.17 | 0.52 | 0.65 | 3.02 | 0.51 | 1.00 | 1.20 | 0.60 | 0.89 |
SD | 0.11 | 0.11 | 0.05 | 0.02 | 0.11 | 0.02 | 0.02 | 0.04 | 0.03 | 0.03 | |
Range | 0.25 | 0.28 | 0.11 | 0.04 | 0.28 | 0.05 | 0.04 | 0.07 | 0.07 | 0.07 | |
Min | 3.86 | 2.05 | 0.46 | 0.64 | 2.90 | 0.48 | 0.99 | 1.17 | 0.57 | 0.85 | |
Max | 4.11 | 2.34 | 0.57 | 0.67 | 3.19 | 0.53 | 1.03 | 1.24 | 0.64 | 0.92 | |
Myrmecophyes heterocerus | |||||||||||
♂♂ (n = 5) | Mean | 2.97 | 1.71 | 0.48 | 0.52 | 1.88 | 0.42 | 0.53 | 0.99 | 0.46 | 0.71 |
SD | 0.16 | 0.12 | 0.06 | 0.02 | 1.07 | 0.00 | 0.03 | 0.02 | 0.01 | 0.03 | |
Range | 0.42 | 0.32 | 0.14 | 0.04 | 2.58 | 0.00 | 0.07 | 0.05 | 0.04 | 0.07 | |
Min | 2.76 | 1.52 | 0.42 | 0.50 | 0.00 | 0.42 | 0.50 | 0.97 | 0.44 | 0.67 | |
Max | 3.19 | 1.84 | 0.57 | 0.53 | 2.58 | 0.42 | 0.57 | 1.03 | 0.48 | 0.74 | |
♀♀ (n =5) | Mean | 3.37 | 1.90 | 0.53 | 0.57 | 2.39 | 0.48 | 0.88 | 1.11 | 0.56 | 0.84 |
SD | 0.38 | 0.10 | 0.07 | 0.03 | 0.10 | 0.03 | 0.05 | 0.04 | 0.03 | 0.03 | |
Range | 0.92 | 0.21 | 0.18 | 0.07 | 0.25 | 0.07 | 0.11 | 0.09 | 0.05 | 0.07 | |
Min | 2.90 | 1.81 | 0.46 | 0.53 | 2.30 | 0.46 | 0.81 | 1.08 | 0.53 | 0.81 | |
Max | 3.82 | 2.02 | 0.64 | 0.60 | 2.55 | 0.53 | 0.92 | 1.17 | 0.58 | 0.88 | |
Myrmecophyes nasutus | |||||||||||
♂♂ (n = 2) | Min | 3.60 | 2.05 | 0.46 | 0.60 | 3.36 | 0.85 | 1.56 | 1.24 | 0.64 | 0.85 |
Max | 3.75 | 2.30 | 0.57 | 0.64 | 3.54 | 0.85 | 1.59 | 1.26 | 0.65 | 0.88 | |
♀♀ (n =5) | Mean | 4.30 | 2.19 | 0.59 | 0.67 | 3.25 | 0.64 | 1.48 | 1.30 | 0.68 | 0.99 |
SD | 0.11 | 0.05 | 0.03 | 0.01 | 0.08 | 0.02 | 0.07 | 0.03 | 0.03 | 0.03 | |
Range | 0.28 | 0.11 | 0.07 | 0.02 | 0.21 | 0.04 | 0.18 | 0.09 | 0.07 | 0.07 | |
Min | 4.18 | 2.12 | 0.57 | 0.65 | 3.12 | 0.64 | 1.42 | 1.26 | 0.64 | 0.96 | |
Max | 4.46 | 2.23 | 0.64 | 0.67 | 3.33 | 0.67 | 1.59 | 1.35 | 0.71 | 1.03 | |
Myrmecophyes tomi sp. n. | |||||||||||
♂♂ (n = 1) | 3.40 | 1.88 | 0.46 | 0.64 | 3.19 | 0.57 | 0.99 | 1.13 | 0.57 | 0.85 | |
♀♀ (n =5) | Mean | 3.33 | 1.84 | 0.52 | 0.57 | 2.48 | 0.46 | 0.86 | 1.10 | 0.56 | 0.81 |
SD | 0.16 | 0.10 | 0.05 | 0.03 | 0.20 | 0.04 | 0.04 | 0.04 | 0.02 | 0.04 | |
Range | 0.42 | 0.25 | 0.11 | 0.07 | 0.46 | 0.07 | 0.11 | 0.11 | 0.05 | 0.11 | |
Min | 3.12 | 1.70 | 0.46 | 0.53 | 2.30 | 0.42 | 0.81 | 1.03 | 0.53 | 0.74 | |
Max | 3.54 | 1.95 | 0.57 | 0.60 | 2.76 | 0.50 | 0.92 | 1.13 | 0.58 | 0.85 |
Observations, measurements, and digital dorsal color images were made with a Nikon SMZ 1500 stereomicroscope equipped with Nikon D700 digital SLR camera. Images of the genitalic structures were taken with a Leica DM2500 microscope equipped with Leica DFC 450 digital camera. Partially focused images of each specimen or structure were stacked using the Helicon Focus 6.2.2 software. The terminology used for genitalia follows
Plumiger Horváth, 1927: 189 (new subgenus). Type species by monotypy: Myrmecophyes heterocerus Horváth, 1927.
Antenna sexually dimorphic (Figs
All species of the subgenus Myrmecophyes differ from Plumiger in having filiform (rather than sexually dimorphic) antennae and two or three variously shaped and typically large sclerites of the endosoma (
Male. Total body length 2.8–3.8, brachypterous and distinctly antlike. Coloration (Figs
Female. Similar to male in coloration, surface, and main structural details, but differing in structure and vestiture of antennal segments, abdomen strongly expanded at middle, and body proportions (Figs
The subgenus is endemic to the Caucasus Mountains including Greater and Lesser Caucasus, and Armenian Highlands (Figure
The striking sexual dimorphism in Plumiger species and one of the main diagnostic features of the subgenus, is exhibited by the enlarged antennal segments I and II and their peculiar vestiture (Figs
We swept specimens of Plumiger in large numbers between 1950 and 2450 m a.s.l. in different grasslands and steppe habitats, viz. Ponto–Caucasian hay meadows, grass meadow-steppes, feather-grass steppes, and acid subalpine grasslands (Figs
Almost nothing is known about the phenology of Plumiger species. Based on the presence of eggs in females, the ratio of males to females, and available collection dates, we speculate that M. armeniacus and M. heterocerus have one and two generations, respectively. More interesting are our observations of diurnal activity of Armenian Myrmecophyes. Despite maximal efforts in suitable habitats, we had little success in collecting at noon. The insects became active and started to move up the culm and leaves of grasses approximately two and a half hours before sunset (just after 18:00 in June). During the day, the bugs were close to the surface, hidden among lower parts of the grasses. This corresponds with our previous observations on other brachypterous halticines, viz. Myrmecophyes s. str., Scirtetellus, and Dimorphocoris spp. in the high mountains of the Balkans and Central Asia.
1 | Clypeus distinctly bulging, rectangular in lateral view (Figs |
3 |
- | Clypeus not bulging, slightly convex in apical half (Figs |
2 |
2 | Larger, body length 3.4–3.7. Head and abdomen matt. Left paramere with rounded outgrowth at base of apical process (Figs |
armeniacus |
- | Smaller, body length 2.8–3.2. Head and abdomen smooth and shiny. Left paramere without outgrowth at base of apical process (Figure |
heterocerus |
3 | Antennal segments longer, segment I 1.3–1.4 × as long as pronotum, segment II 1.2–1.3 × as long as head width and 1.8–1.9 × as long as width of pronotum at middle. Left paramere with two subapical recurved denticles (Figs |
nasutus |
- | Antennal segments shorter, segment I 0.9 × as long as pronotum, segment II 0.9 × as long as head width and 1.2 × as long as width of pronotum at middle. Left paramere with single subapical recurved denticle (Figs |
tomi |
1 | Larger, body length 3.9–4.5. Head and abdomen matt (Figs |
2 |
- | Smaller, body length 2.8–3.2. Head and abdomen smooth and shiny (Figs |
3 |
2 | Body length 3.9–4.1. Sclerotized rings of dorsal labiate plate broadly oval (Figs |
armeniacus |
- | Body length 4.2–4.5. Sclerotized rings of dorsal labiate plate subtriangular, long and narrow, with apices distinctly attenuated (Figs |
nasutus |
3 | Sclerotized rings of dorsal labiate plate subtriangular, long and narrow, with apices distinctly attenuated (Figs |
heterocerus |
- | Sclerotized rings of dorsal labiate plate broadly oval (Figs |
tomi |
Myrmecophyes (Plumiger) armeniacus Dapolyuk, 1989: 125; figs 51, 55.
Holotype: TURKEY: Kars: Kars, 40.58333°N, 43.06666°E, 04 Jun 1915, Olsufiev, 1♀ (AMNH_PBI 00261681) (
ARMENIA: Gegharkunik: N coast of Sevan Lake, Artanish – Shorzha Rd, 40.50109°N, 45.3282°E, 1962 m, 14 Jun 2017, F. Konstantinov & N. Simov, (Poaceae), 15♂ (AMNH_PBI 00343264-AMNH_PBI 00343277, AMNH_PBI 00343331), 70♀ (AMNH_PBI 00343249-AMNH_PBI 00343263, AMNH_PBI 00343232-AMNH_PBI 00343248, AMNH_PBI 00343196-AMNH_PBI 00343231, AMNH_PBI 00343330, AMNH_PBI 00343376) (
Size large, clypeus straight, not bulging apically in either sex (Figs
Males of M. armeniacus are most similar to M. heterocerus in structure of the head and male genitalia, but the latter species can be distinguished by the smaller size, shiny head and abdomen, and structure of the left paramere with the apical process narrowing before the T-shaped blade and equipped with a prominent outgrowth at base (compare Figs
Male. Total length 3.4–3.7. Coloration: (Figure
Female. Body large, total length 3.9–4.1. Coloration: As in male, but antennal segment I and femora ranging from uniformly rust brown to totally black (Figure
The current distribution of M. armeniacus spans a distance of less than 200 km from northeastern Turkey in the west to northwestern Armenia in the east (Figure
Myrmecophyes heterocerus Horváth, 1927: 189
Myrmecophyes (Plumiger) heterocerus Drapolyuk, 1989: 135, figs 46–50, 54 (figs, habitus, male and female genitalia)
ARMENIA: Gegharkunik: 7 km S from Nshkhark, 39.95378°N, 45.23438°E, 2418 m, 13 Jun 2017, F. Konstantinov & N. Simov, (Poaceae), 56♀ (AMNH_PBI 00343163-AMNH_PBI 00343195, AMNH_PBI 00343338, AMNH_PBI 00343339, AMNH_PBI 00343156-AMNH_PBI 00343162, AMNH_PBI 00343149-AMNH_PBI 00343155, AMNH_PBI 00343142-AMNH_PBI 00343148), 70♂ (AMNH_PBI 00343378, AMNH_PBI 00343337, AMNH_PBI 00343329, AMNH_PBI 00343071-AMNH_PBI 00343074, AMNH_PBI 00343069, AMNH_PBI 00343067, AMNH_PBI 00343080-AMNH_PBI 00343136, AMNH_PBI 00343138-AMNH_PBI 00343141), 2 larvae (AMNH_PBI 00343075, AMNH_PBI 00343137) (
Distinguished from M. armeniacus by the smaller size, shiny abdomen (Figs
Male. Total length 2.8–3.2. Coloration: As in M. armeniacus. Surface and vestiture: Pronotum and scutellum matt, head and abdomen smooth, distinctly shiny (Figure
Female. Similar to male but body larger on average, total length 2.9–3.8. Coloration: As in male, but with pale brown to dirty yellow antennal segment I (Figure
Myrmecophyes heterocerus appears to be the most wide-ranging species of the subgenus, occurring along the Greater Caucasus range from North Ossetia in the west across Georgia to southeastern Dagestan in the east, and along the Greater Caucasus range to central Armenia and western Azerbaijan in the south (Figure
Myrmecophyes (Plumiger) nasutus Drapolyuk, 1989: 125; figs 40–45, 52, 53.
Holotype: GEORGIA: Racha-Lechkhumi and Kvemo Svaneti: Korel’dash, 42.9183°N, 43.144°E, 26 Jul 1957, Akramovskaya, 1♂ (AMNH_PBI 00261441) (
Distinguished from other Plumiger spp. by the larger size (Figs
Male. Total length 3.8–3.9. Coloration (Figure
Female. Body larger on average, total length 4.2–4.5. Coloration: Similar to male, but antennal segment I ranging from dirty orange to entirely black, coxae usually entirely or at least apically dirty orange, femora from entirely dirty orange to black, with apices dirty orange (Figs
Known from several localities in northern Georgia along the southern slopes of the Greater Caucasus Mountain range (Figure
Georgia, Kakheti, Sakhkhova Mts. Range, 42.36666°N, 45.61666°E
Holotype: GEORGIA: Kakheti: Sakhkhova Mts. Range, Tushetia, 42.36666°N, 45.61666°E, 28 Aug 1959, I. Zaytseva, 1♂ (AMNH_PBI 00261443) (
Distinguished from congeners by the small size (Figs
Myrmecophyes tomi is separated from the morphologically similar M. nasutus by the shiny head and abdomen, the smaller body size, the shorter first two antennal segments in the male, the single subapical, recurved denticle of the left paramere, and the broad sclerotized rings. The last-named character would allow females of M. tomi to be distinguished from those of M. heterocerus, which otherwise are similar in body size and proportions, and in having a shiny abdomen.
Description. Male. Total body length 3.4. Coloration: Dorsum and venter uniformly black, with contrasting yellowish-white stripe along apical margin of wing pad; antennal segment I chestnut brown, remaining segments dark brown; coxae and femora dirty yellow, tibiae and tarsi dark brown (Figure
Female. Larger than male on average, total body length 3.1–3.5, with antenna unmodified and abdomen broadly oval, strongly expanded at middle. Coloration: Similar to male, but antennal segment I dirty orange, coxae and femora black, with apices dirty orange (Figure
The species is named for Thomas J. Henry in recognition of his unparalleled contributions to heteropterology.
Known from northeastern Georgia in the Transcaucasia to southwestern Dagestan in the North Caucasus (Figure
The new species is described from the specimens originally included in the paratype series of M. nasutus by
Dorsal habitus of Myrmecophyes (Plumiger) species. 5, 8 Myrmecophyes armeniacus Drapolyuk, 1989 5 male 8 female 6, 9 Myrmecophyes heterocerus Horváth, 1927 6 male 9 female 7, 10 Myrmecophyes tomi sp. n. 7 male 10 female 11–13 Myrmecophyes nasutus Drapolyuk, 1989 11 male 12 pale female 13 dark female.
Scanning electron micrographs. 14, 15 Head and thorax in lateral view 14 Myrmecophyes armeniacus Drapolyuk, 1989, female 15 Myrmecophyes heterocerus Horváth, 1927, male 16, 17 Metathoracic scent gland evaporative area and spiracle 16 M. armeniacus 17 M. heterocerus 18 Head of M. heterocerus male in lateral view 19 Antennal segment I of M. heterocerus male.
Male genitalia: 30–32, 34–35 Left paramere in lateral (30, 34) and dorsal (31, 32, 35) views 30–32 Myrmecophyes armeniacus Drapolyuk, 1989 34, 35 Myrmecophyes heterocerus Horváth, 1927 33, 36 Right paramere in dorsal view 33 M. armeniacus 36 M. heterocerus 37–40 Aedeagus in lateral view (38, 40) and with phallotheca detached from phallobase and partially expanded endosoma (37, 39) 37, 38 M. armeniacus 39, 40 M. heterocerus. Abbreviations: outgr – rounded outgrowth at base of apical process of the left paramere.
Male genitalia: 41–42, 44–45 Left paramere in dorsal (41, 44) and lateral (42, 45) views 41, 42 Myrmecophyes nasutus Drapolyuk, 1989 44, 45 Myrmecophyes tomi sp. n. 43, 46 Right paramere in dorsal view 43 M. nasutus 46 M. tomi sp. n. 47–50 Aedeagus in lateral view (48, 50) and with phallotheca detached from phallobase and partially expanded endosoma (47, 49) 47, 48 M. nasutus, 49, 50 M. tomi sp. n. Abbreviations: dent –recurved denticle(s) of the left paramere, lob – slightly sclerotized lobes of endosoma.
Female genitalia: 55–58 Posterior wall of bursa copulatrix 55 Myrmecophyes armeniacus Drapolyuk, 1989 56 Myrmecophyes heterocerus Horváth, 1927 57 Myrmecophyes nasutus Drapolyuk, 1989 58 Myrmecophyes tomi sp. n. 59–62 Sclerotized rings of dorsal labiate plate 59 M. armeniacus 60 M. heterocerus 61 Myrmecophyes nasutus 62 M. tomi sp. n. 63 Vulva of M. heterocerus.
Funding for this study was provided by the Russian Foundation for Basic Research, project 16–04–01682. The Heteroptera collection of the Zoological Institute, Russian Academy of Sciences, is financially supported by the state research project АААА-А17-117030310210-3. We appreciate the assistance of Alexey Mirolyubov and Svetlana Janson (microscopy and microanalysis facility center, SPSU) for technical support in the operation of the SEM. Michael D. Schwartz (CNC) and Alfred G. Wheeler Jr. (Clemson University) provided valuable comments on an earlier version of the manuscript.
Figure | Species | Sex | USI number |
---|---|---|---|
5 | Myrmecophyes armeniacus | male | AMNH_PBI 00343298 |
6 | Myrmecophyes heterocerus | male | AMNH_PBI 00343084 |
7 | Myrmecophyes tomi | male | AMNH_PBI 00261443 |
8 | Myrmecophyes armeniacus | female | AMNH_PBI 00343318 |
9 | Myrmecophyes heterocerus | female | AMNH_PBI 00343142 |
10 | Myrmecophyes tomi | female | AMNH_PBI 00261684 |
11 | Myrmecophyes nasutus | male | AMNH_PBI 00261441 |
12 | Myrmecophyes nasutus | female | AMNH_PBI 00261674 |
13 | Myrmecophyes nasutus | female | AMNH_PBI 00261640 |
14, 16, 22, 23, 25 | Myrmecophyes armeniacus | female | AMNH_PBI 00343376 |
15, 17–21, 24 | Myrmecophyes heterocerus | male | AMNH_PBI 00343378 |
26 | Myrmecophyes armeniacus | male | AMNH_PBI 00343291 |
27 | Myrmecophyes nasutus | male | AMNH_PBI 00261441 |
28 | Myrmecophyes heterocerus | male | AMNH_PBI 00343083 |
29 | Myrmecophyes tomi | male | AMNH_PBI 00261443 |
30–31 | Myrmecophyes armeniacus | male | AMNH_PBI 00343331 |
32–33 | Myrmecophyes armeniacus | male | AMNH_PBI 00343334 |
34 | Myrmecophyes heterocerus | male | AMNH_PBI 00343092 |
35–36 | Myrmecophyes heterocerus | male | AMNH_PBI 00343129 |
37–38 | Myrmecophyes armeniacus | male | AMNH_PBI 00343268 |
39 | Myrmecophyes heterocerus | male | AMNH_PBI 00343329 |
40 | Myrmecophyes heterocerus | male | AMNH_PBI 00343092 |
41–43 | Myrmecophyes nasutus | male | AMNH_PBI 00261441 |
44–46 | Myrmecophyes tomi | male | AMNH_PBI 00261443 |
47–48 | Myrmecophyes nasutus | male | AMNH_PBI 00261441 |
49–50 | Myrmecophyes tomi | male | AMNH_PBI 00261443 |
51 | Myrmecophyes armeniacus | female | AMNH_PBI 00343333 |
52 | Myrmecophyes tomi | female | AMNH_PBI 00261684 |
53 | Myrmecophyes heterocerus | female | AMNH_PBI 00261637 |
54 | Myrmecophyes nasutus | female | AMNH_PBI 00261646 |
55 | Myrmecophyes armeniacus | female | AMNH_PBI 00343333 |
56 | Myrmecophyes heterocerus | female | AMNH_PBI 00343339 |
57 | Myrmecophyes nasutus | female | AMNH_PBI 00261646 |
58 | Myrmecophyes tomi | female | AMNH_PBI 00261444 |
59 | Myrmecophyes armeniacus | female | AMNH_PBI 00343333 |
60 | Myrmecophyes heterocerus | female | AMNH_PBI 00261637 |
61 | Myrmecophyes nasutus | female | AMNH_PBI 00261646 |
62 | Myrmecophyes tomi | female | AMNH_PBI 00261684 |
63 | Myrmecophyes heterocerus | female | AMNH_PBI 00261637 |