Restiid-Feeding Semiini (Hemiptera: Miridae: Phylinae) From Western Australia: Description and Phylogenetic Analysis of the New Plant Bug Genus Restiophylus , n. gen

Abstract

The phyline fauna of Australia has only recently been shown to be highly diverse, both at the species and the genus levels. Here, a new genus and four new species of Australian Phylinae (Hemiptera: Miridae) are described. The species of Restiophylus , n. gen., occur on two genera of the rush-like Restionaceae, Hypolaena Brown 1810 and Leptocarpus Brown 1810, and on one genus of the closely related Anarthriaceae, Lyginia Brown 1810. Habitus images, illustrations of male genitalia, scanning micrographs, an identification key, and distribution maps for the new species are provided as well as digital images and distribution maps for the hosts. Consistent with the geographic distribution patterns of many other Australian Phylinae, the four new species are restricted to the Mediterranean-type biome of Western Australia. A cladistic analysis based on 55 morphological characters, four ingroup taxa, and 31 outgroup taxa is presented, providing evidence for the monophyly of this new genus and its placement in the tribe Semiini, and potentially as sister to the subtribe Exocarpocorina.

The collaborative Planetary Biodiversity Inventory for Plant Bugs (PBI) project led by R. T. Schuh and G. Cassis (2003–2011) has enhanced our understanding of the diversity, distributions, and host associations of plant bugs on a global scale ( Cassis and Schuh 2012 ). The project has placed special emphasis on Mediterranean-type biomes across the globe, and Australia, unsurprisingly given its plant and insect diversity, has played an important role. The project has focused on two subfamilies, the Orthotylinae and Phylinae ( http://research.amnh.org/pbi/ ) and among those, Phylinae in Australia have been treated in a series of publications. As a result, >100 new species in nine new genera of Phylinae from Australia have been described during the past decade ( Soto and Weirauch 2009 ; Weirauch 2006 , 2007 ; Menard and Schuh 2011 ; Schuh and Pedraza 2010 ; Schuh and Weirauch 2010 ; Weirauch and Schuh 2010 ; Schuh et al. 2014 ). However, a substantial portion of biodiversity is still in need of documentation, and revisionary taxonomic efforts on Australian Phylinae are ongoing.

Until recently, phylogenetic relationships within Phylinae were virtually unknown and this has negatively impacted our ability to classify new genera. Based on both morphological and molecular data and comprehensive taxon sampling, Menard et al. (2014) analyzed relationships within the subfamily, recognizing nine tribes and nine subtribes. The tribe Phylini that used to comprise more than half of all Phylinae ( Cassis and Schuh 2012 ) was recovered as polyphyletic and redefined. Two new tribes, Decomiini and Coatonocapsini, were erected, Semiini and Nasocorini resurrected as tribes, Auricillocorini synonymized with Hallodapini, and Pronotocrepini with Cremnorrhini. In a companion paper, Schuh and Menard (2013) presented a comprehensive generic classification of Phylinae and provided arguments and diagnoses for new and resurrected tribes. The tribe Semiini originally comprised only the genus Semium Reuter and was placed in the Orthotylinae ( Knight 1923 , Carvalho 1955 ) and transferred to Phylinae by Kelton (1959) . Schuh (1974) later transferred Semium to Phylini, synonymizing Semiini with Phylini. However, based on several morphological synapomorphies, such as the eyes being parallel to the anterior margin of the pronotum, the highly sclerotized ventral sack in females, and various characters of the male genitalia, Schuh and Menard (2013) resurrected the tribe Semiini. It now comprises the new subtribes Exocarpocorina that contains a large proportion of Australian Phylinae (e.g., Leptidolon Reuter, Melaleucoides Schuh and Weirauch, and Wallabicoris Schuh and Pedraza), and the subtribe Semiina that includes genera and species from all biogeographic regions. Semiina combines taxa with unique and relatively derived male genitalia with taxa that possess a very simple, tubular endosoma.

Restionaceae, or restios, are a family of flowering plants that comprises about 520 species in 58 genera ( Angiosperm Phylogeny Group III [APG III] 2009 ). Until recently, this family also contained what is now recognized as its sister group and a separate family, the Anarthriaceae, a clade of 10 species in 3 genera that are endemic to Western Australia. Together, these two families make up the restiid clade ( Briggs et al. 2014 ), a group of rush-like plants with small, wind-pollinated flowers and reduced leaves. Restionaceae show highest species diversity in South Africa, Australia, and New Zealand, but a few widespread species also occur in Southeast Asia and a single species in South America ( Linder et al. 2003 ). The Cape Floristic Region of South Africa alone contains 350 species of restios ( Kemp 2014 ). Maybe unsurprisingly, studies documenting associations between Restionaceae and specialist herbivorous insects are so far restricted to this region ( Kemp 2014 , Augustyn 2013 , Davies 1988 , Slater 1976 ). The most prominent among them is an endemic tribe of leafhoppers (Cicadellidae: Cephalelini) that exhibits species-level host specificity, and where some species seem to track the phenology of their primary hosts, allowing the use of the same plant by multiple cephaleline species at different times of the year ( Davies 1988 , Augustyn et al. 2013 ). In addition, tropichulid leafhoppers, planthoppers, chrysomelid beetles, and lentulid grasshoppers have been found associated with Restionaceae ( Kemp 2014 ), but their level of specialization on restios is unknown. Among Heteroptera, species of the South African blissid genus Capodemus Slater and Sweet have been reported feeding on the South African Restionaceae genus Elegia L. ( Slater 1976 ). However, not all members of Capodemus occur on Restionaceae; some have been reported on other grass-like families such as Cyperaceae and even on true grasses ( Slater 1976 ). Within Miridae, a search of the PBI locality database ( http://research.amnh.org/pbi/databases/locality_database.html ) shows that the mirine Nymannus typicus Distant, treated as belonging to Stenotus by Carvalho (1981) , has been recorded on South African Restionaceae.

Here, we present a study focusing on a clade of Phylinae in the tribe Semiini, subtribe Semiina, that was collected from Restionaceae and Anarthriaceae in Australia, thus expanding both known insect taxa and geographic range of restiid–insect interactions. We describe a new genus and four new species, and outline their distributions and hosts, and conduct a morphological cladistic analysis to place this new genus in phylogenetic context.

Materials and Methods

Specimens Examined

A total of 761 specimens were examined for this project. Unique specimen identifier (USI) labels were attached to the specimens. The USIs show a unique combination of an eight-digit number and the pre-fix AMNH_PBI or UCR_ENT and a collection acronym that usually (see below) indicates the depository of the specimen. The majority of specimens were given USI labels with the prefix “AMNH_PBI”, this prefix was omitted from the material examined section, and only the eight-digit number is shown; UCR_ENT USIs appear with prefix. Specimen data were captured using the PBI instance of the Arthropod Easy Capture (AEC) database https://research.amnh.org/pbi/locality/ . Specimen information, including maps showing the collecting locality, is available through the Heteroptera Species Pages http://research.amnh.org/pbi/ . A number of specimens, including holotypes, collected by R. T. Schuh at the American Museum of Natural History (AMNH) and G. Cassis, then at the Australian Museum (AM), were donated to the Western Australian Museum Perth (WAMP), or one of the PBI participating institutions (Canadian National Collection; University of California Riverside; University of New South Wales; United States National Museum; Zoological Institute, Russian Academy of Sciences, St. Petersburg). These specimens retain their original AMNH or AM collection depository on the USI label.

Abbreviations for institutional depositories

• AM—Australian Museum, Sydney

• AMNH—American Museum of Natural History, New York

• ANIC—Australian National Insect Collection, Canberra

• CNC—Canadian National Collection of Insects, Ottawa

• UCR—University of California, Riverside

• UNSW—University of New South Wales, Sydney

• USNM—United States National Museum of Natural History, Smithsonian Institution, Washington, DC

• WAMP—Western Australian Museum, Perth

• ZISP—Zoological Institute, Russian Academy of Sciences, St. Petersburg

Comments on Descriptions and Diagnoses

Species descriptions were generated from the character data matrix that was also used for the cladistic analysis (see Supp Appendix 1 [online only]). The matrix was coded in WinClada ver. 0.9.99.60 (Nixon, 2002), the descriptions for the four new species were written to text file (using commands “output and describe”), and the resulting raw-descriptions edited. The genus-level description of Restiophylus was generated from one of the species descriptions and modified to include all character states represented within the genus. Both genus- and species-level diagnoses are derived from the cladistic analysis based on this matrix.

Habitus Images, SEM Imaging, and Genitalic Illustrations

Habitus images of males and females were taken using a GT Vision imaging system (Hagerstown, MD). Four specimens (00128440, 00128478, 00214379, and 00215308) were dissected, placed on a stub with an adhesive carbon sticker (Ted Pella, Inc. Redding, CA), coated with gold-palladium (Cressington 108 auto sputter coater, Ted Pella, Inc. Reddin, CA), and observed using a Hitachi S-4700 electron microscope (Hitachi, Tokyo, Japan) at UCR’s imaging facility http://cfamm.ucr.edu/ . Male and female genitalia were dissected for 53 specimens using standard procedures for Miridae. Male genitalia (endosoma and parameres) were illustrated using a camera lucida on a Nikon Eclipse 80i compound microscope (Nikon, Tokyo, Japan). Habitus images for plants were obtained as part of the PBI Plant Bug project and are linked to the AEC database. Host distribution maps were created using the Atlas of Living Australia spatial portal on the Australia’s virtual herbarium ( Australia’s Virtual Herbarium [AVH] 2015 ) website (http:// http://avh.chah.org.au/ ); plant habitus images for Hypolaena exsulca and an image of Lyginia imberbis are also taken from this site.

Specimen Measurements

Measurements were made using a two-axis micrometer (Boeckeler Instruments Microcode II, Tucson, AZ) driven stage mounted onto a Lomo SF-100 MBC-10 stereoscrope (St. Petersburg, Russia) with micrometer output written directly onto a spreadsheet. Measurements in millimeters for all taxa are presented in Table 1 . Ranges for the total body length are also included in the descriptions.

Character Matrices for Cladistic Analyses

The purpose of the phylogenetic analysis is twofold: to test whether the new species together form a monophyletic group and to propose hypotheses on their relationships within Phylinae. The matrix (see Supp Appendix 1 [online only]) is based on matrix 1 used in Weirauch and Schuh (2010) , but modified by removing a number of terminal taxa and adding several morphological characters. The dataset comprised 35 taxa, including all species of Restiophylus and a sample of Phylinae from Australia, North and South America, and Africa. A species of Leucophoropterini was used to root the tree. The 55 characters selected for this dataset are derived from structural morphology (e.g., male and female genitalia), but also include a comprehensive selection of color characters.

Cladistic Analyses

The dataset was analyzed in TNT (Goloboff et al. 2008) using New Technology searches with default parameters and Ratchet, Drift, and Tree fusing. The six resulting trees were opened in WinClada to examine and document character optimizations. The homoplasy settings were chosen as “any extra step makes it homoplasious.” Support values were calculated in TNT using jackknifing with a 36% removal probability, 1,000 replications, and a traditional search and were mapped above the nodes of the most parsimonious trees. We are treating synapomorphies shown under unambiguous optimization as diagnostic characters ( Fig. 6 ). Habitus images in Fig. 6 other than those of Restiophylus were modified from Weirauch (2007) , Soto and Weirauch (2009) , Schuh and Pedraza (2010) , Weirauch and Schuh (2010) , Henry (2012) , and Russell and Weirauch (in prep); the image for Semium hirtum Reuter was taken from the PBI locality database, using the report mode, under queries. The numbers in parentheses in the diagnoses refer to characters and character states derived from the cladistic analysis.

Nomenclature

This paper and the nomenclatural acts it contains have been registered in Zoobank ( www.zoobank.com ), the official register of the International Commission on Zoological Nomenclature. The LSID (Life Science Identifier) number of the publication is: urn:lsid:zoobank.org:pub:DF8DD722-FF1E-45C7-A678-7A3BDFB57CE7

Taxonomy

Restiophylus Leon and Weirauch, new genus( Figs. 1–4 , 6 ; Tables 1–2 )

(urn:lsid:zoobank.org:act:CE20A160-0CB4-4E4F-9D56-829A3A404AE7)

Type species: Restiophylus leptocarpi , new species

Diagnosis

Recognized among Phylinae by the following characters ( Figs. 1–3 ): relatively large size (males 2.84–3.97 mm); elongate head (11-0); reddish-brown coloration (1-6), pale lateral margins (5-1) of the pronotum and pale coloration of the costal margin (6-1), with median cream-colored longitudinal line on pronotum in many species (2-1); scutellum with a white tip in many species (4-1); the simple J- or C-shaped endosoma (e.g., 19-1, 21-0); absence of a secondary gonopore sclerite (27-0); the presence of a single apical, either slender or flared, process of the primary endosomal strap (25-1); the female typically more vividly colored than the male (45-1); and the simple female internal genitalia (e.g., characters 46–54). This new genus is superficially similar in body shape and prognathous head structure to some undescribed Australian Cremnorrhina, but distinguished from all other Australian Phylinae based on its coloration, body size, as well as the very simple male and female genitalia.

Description

Male: Body moderately elongate, ovoid, relatively large, males ranging between 2.84–3.97 mm (see Table 1 ). COLORATION ( Fig. 1 ): General coloration reddish brown; pronotum and scutellum with median cream-colored longitudinal line and scutellum with white tip in most species or pronotum and scutellum uniformly reddish brown; sometimes pronotum with lateral cream-colored lines; lateral margin of pronotum pale; costal margin pale; embolium with pale mark of varying length along claval commissure or concolorous with remainder of embolium. SURFACE AND VESTITURE ( Figs. 1 and 2 ): Dorsum with black, cylindrical, suberect setae intermixed with subadpressed, slightly flattened pale setae in most species or with only black, cylindrical, suberect setae. STRUCTURE: Head ( Figs. 1 and 2 A): Elongate, projecting anteriorly; antennal fossa with ventral margin of fossa at ventral eye margin; synthlipsis large; eyes leaving gena broadly exposed in lateral view; details of scent gland evaporatory area pretarsus, and pygophore as in Fig. 2 B–D. GENITALIA: Pygophore: Simple, without row or tuft of setae on left side. Endosoma ( Fig. 3 ): Base short and curving, C- or J-shaped, with a single unified strap, U-shaped in cross section; body without torsion, primary strap ventral to secondary gonopore; primary strap short, ratio length apex strap/length secondary gonopore 1.00–1.50; apex nearly straight and with one tip; apical process of primary strap equal to or longer than 1.5 times length of apex; apical process slender or flared (leaf-shaped); secondary gonopore sclerite absent; secondary gonopore seen in semi-frontal view; fingerlike protuberance at distal margin of secondary gonopore absent; spine-like, elongate process arising near gonopore absent. Phallotheca : Smoothly curving on dorsal margin; posterior surface lacking transparent window. Left paramere ( Fig. 3 ): Body relatively short, just exceeding margin of pygophore; anterior process triangular or slender in lateral view; posterior process in dorsal view much longer than or of same length as anterior process; base of posterior process without conspicuous shoulder; base of anterior process sometimes with conspicuous shoulder; anterior rim of body with simple setae. Right paramere ( Fig. 3 ): Body elongate or moderately elongate; apex with short fingerlike process; posterior surface of apex smooth. Female: Similar to male but body shape slightly more ovoid; more vividly red than male. GENITALIA: Internal genitalic structures simple and largely membranous (and therefore not illustrated), posterior wall laterally with crescent-shaped interramal sclerites, but without a sclerotized transverse band and posteriolaterally without a distinct swelling covered with microtrichia; interramal lobes absent.

Etymology

This genus is named for the host-plant association of most of its members with Restionaceae and “phylus” to indicate that it is classified in the subfamily Phylinae. The gender is masculine.

Hosts

Recorded from species of two genera of Restionaceae and one genus of Anarthriaceae ( Table 2 ).

Distribution

The currently known distribution range of species in this genus is Western Australia.

Key to the Species of Restiophylus , n. gen. ( Figs. 1 and 3 )

• 1a. Vestiture on hemelytra comprising black, cylindrical and white, flattened setae ( Fig. 1 ; R. hypolaenae , Fig. 2 E-G)2

• 1b. Vestiture on hemelytra comprising only black, cylindrical setae ( Fig. 1 ; R. meeboldinae , Fig. 2 H)…………………… Restiophylus meeboldinae , n. sp.

• 2a. Pronotum with one median and paired lateral cream colored lines ( Fig. 1 ; R. lyginiae [arrow B])…………………… Restiophylus lyginiae , n. sp.

• 2b. Pronotum either uniformly reddish ( Fig. 1 ; R. leptocarpi ), or with one median cream-colored line ( Fig. 1 ; R. hypolaenae ), never with paired lateral cream-colored lines3

• 3a. Pronotum uniformly reddish, without cream-colored lines ( Fig. 1 ; R. leptocarpi ); process of primary strap of endosoma slender ( Fig. 3 ; R. leptocarpi )……………… Restiophylus leptocarpi , n. sp.

• 3b. Pronotum with one median, cream-colored line ( Fig. 1 ; R. hypolaenae [arrow A]); process of primary strap flared, almost leaf-shaped ( Fig. 3 ; R. hypolaenae )……… Restiophylus hypolaenae , n. sp.

Restiophylus hypolaenae Leon and Weirauch, new species ( Figs. 1–4 ; Tables 1–2 )

(urn:lsid:zoobank.org:act:779F484F-4AD6-4C56-8ADF-0692A4D73943)

HOLOTYPE: 1♂ AUSTRALIA, Western Australia, 4.2 km SE of Esperance, Lake Mullet Nature Reserve, -33.79691, 121.95427, 10 m (33 ft), 23-XI-99, WA99_L28, on Hypolaena humilis , R.T. Schuh, G. Cassis and R. Silveira (00128488) (WAMP) PARATYPES: 17♂ (00214374–00214391), 13♀ (00214424–00214436) (WAMP), 20♂ (00216310–00216319, 00128357–00128360, 00128483–00128489), 38♀ (00216320–00216335, 00128369–00128385, 00128490–00128494) (AMNH), AUSTRALIA, Western Australia, 4.2 km SE of Esperance, Lake Mullet Nature Reserve, 33.79691°S 121.95426°E, 10 m, 23-XI-99, on Hypolaena humilis , det. PERTH staff PERTH 05672376, R.T. Schuh, G. Cassis and R. silveira; 4♂ (UCR_ENT 00047204–00047207), 6♀ (UCR_ENT 00047208–00047213) (AMNH), AUSTRALIA, Western Australia, 39 km NE of King River, 34.78937°S 118.2759°E, 200 m, 06-XI-96, on Hypolaena exsulca , det. PERTH staff PERTH 05236606, Schuh and Cassis; 1♂ (00215229) (AM), AUSTRALIA, Rossiter Bay, Cape Le Grande National Park, 33.96726°S 122.2674°E, 3 m, 23-XI-99, R.T. Schuh, G. Cassis and R. Silveira.

Diagnosis

Recognized among species of Restiophylus by the single, cream-colored medial longitudinal line on the pronotum and scutellum (2-1) ( Fig. 1 ) and the flared, almost leaf-shaped apical process of the primary endosomal strap (25-1) ( Fig. 3 ).

Description

Male: As in generic description, total length 2.84–3.70 mm ( Fig. 1 ). COLORATION: As in generic description, with pronotum and scutellum with median cream-colored longitudinal line, but without lateral lines, and scutellum with white tip; embolium concolorous with remainder of hemelytron. SURFACE AND VESTITURE: ( Fig. 2 E): Dorsum with black, cylindrical, suberect setae intermixed with subadpressed, slightly flattened pale setae on hemelytra. STRUCTURE: Head ( Fig. 1 ): As in generic description. GENITALIA: Pygophore: As in generic description. Endosoma ( Fig. 3 ) : As in generic description, with apical process of primary strap longer than 1.5 times length of apex; apical process flared (leaf-shaped). Phallotheca: As in generic description. Left paramere ( Fig. 3 ) : As in generic description, with anterior process slender in lateral view; posterior process in dorsal view about same length as anterior process. Right paramere ( Fig. 3 ): as in generic description. Female: See generic description for structural details and Fig. 1 for habitus and coloration.

Etymology

A noun in genitive case and named for the association with plants in the genus Hypolaena Brown.

Hosts

Recorded from two species of Hypolaena : Hypolaena exsulca Brown and Hypolaena humilis Briggs and Johnson ( Fig. 5 A; Table 2 ).

Distribution

Currently known from three localities close to the southern coast of Western Australia ( Fig. 4 ). This narrow distribution range matches fairly closely the range observed in the host plant H. humilis ( Fig. 5 ).

Other Specimens Examined

AUSTRALIA: Western Australia, 28 juv. (00214394–00214405, 00214407–00214416, 00214418–00214423) (AM), 22 juv. (00216336–00216349, 00128361–00128368) (AMNH), 2♂ (0099377, 00214379), 1♀ (0099378), 4.2 km SE of Esperance, Lake Mullet Nature Reserve, 33.79691°S 121.95426°E, 10 m. 23-XI-99, on Hypolaena humilis det. PERTH staff PERTH 05672376, R.T. Schuh, G. Cassis and R. Silveira; 2♂ (00087328, 00087535), 1♀ (00087329) (AM), 3♂ (00135285–00135287), 16♀ (00135288–00135303) (AMNH), 39 km NE of King River, 34.78937°S 118.2759°E, 200 m, 06-XI-96, on Hypolaena exsulca , det. PERTH staff PERTH 05236606, Schuh and Cassis.

Restiophylus leptocarpi Leon and Weirauch, new species( Figs. 1–4 ; Tables 1–2 )

(urn:lsid:zoobank.org:act:AC6D0026-62B9-4867-8E2E-0F383FAED5B3)

HOLOTYPE. 1♂ (00128638), AUSTRALIA, Western Australia, 10.1 km W of Broke Inlet Road on Chesapeak Road, D'Entrecasteaux National Park, -34.85263, 116.39450, 20 m (66 ft), 2-XII-99, WA99_L59, on Leptocarpus tenax , R.T. Schuh, G. Cassis and R. Silveira. (WAMP) PARATYPES: 14♂ (00131182–00131195), 18♀ (00131197–00131214) (AMNH), 5♂ (00089816, 00089817, 00089828, 00089830, 00089831), 3♀ (00089813–00089815) (WAMP), AUSTRALIA, Western Australia, 3.5 km N of Mt. Chudalup, D'Entrecasteaux National Park, 34.73335°S 116.0889°E, 50 m, 15-XII-97, Schuh, Cassis, Brailovsky; 11♂ (00214319–00214329), 12♀ (00214343–00214354) (AM), AUSTRALIA, 7.5 km N of Mt. Chudalup, D'Entrecasteaux National Park, 34.73363°S 116.0861°E, 50 m, 16-XII-97, on Meeboldina scariosa , det. PERTH staff PERTH 05099773, Schuh, Cassis, Brailovsky; 26♂ (00214471–00214495, 00215230), 7♀ (00214534–00214539, 00215232) (AM), 12♂ (00128638–00128649), 14♀ (00128653–00128666) (AMNH), AUSTRALIA, 10.1 km W of Broke Inlet Road on Chesapeak Road, D'Entrecasteaux National Park, 34.85263°S 116.3945°E, 20 m, 2-XII-99, R.T. Schuh, G. Cassis and R. Silveira; 33♂ (00215307, 00215309–00215327, 00215278–00215288, 00214460, 00214461), 30♀ (00215328–00215330, 00215333–00215351, 00215299–00215306) (AM), 13♂ (00128606–00128618), 15♀ (00128623–00128637) (AMNH), AUSTRALIA, Chesapeak Road, 47.2 km W of Broke Inlet Road, 34.7681°S 116.1575°E, 50 m, 3-XII-99, on Leptocarpus tenax det. PERTH staff PERTH 05671515, R.T. Schuh, G. Cassis and R. Silveira.

Diagnosis

Recognized by the uniform reddish coloration of the pronotum and scutellum (2-0) ( Fig. 1 ) and the long (24-1) and slender (25-0) apical process of the primary endosomal strap ( Fig. 3 ).

Description

Male: As in generic description, length 3.35–3.50 mm ( Fig. 1 ). COLORATION: As in generic description, with pronotum and scutellum concolorous with remainder of thorax; embolium with pale mark along entire length of claval commissure. SURFACE AND VESTITURE ( Fig. 2 F): Dorsum with black, cylindrical, suberect setae intermixed with subadpressed, slightly flattened pale setae on hemelytra. STRUCTURE: Head ( Fig. 1 ): As in generic description. GENITALIA: Pygophore: As in generic description. Endosoma ( Fig. 3 ): As in generic description, with apical process of primary strap longer than 1.5 times length of apex and apical process slender. Phallotheca : As in generic description. Left paramere ( Fig. 3 ): As in generic description, with anterior process triangular in lateral view; posterior process in dorsal view much longer than anterior process. Right paramere ( Fig. 3 ): As in generic description. Female: See generic description for structural details and Fig. 1 for habitus and coloration.

Etymology

A noun in genitive case and named for the association with plants in the genus Leptocarpus Brown.

Hosts

Recorded from two species of Restionaceae: Leptocarpus tenax Brown and Meeboldina scariosa Brown ( Fig. 5 B; Table 2 ).

Distribution

Known only from the southwestern tip of Western Australia. The primary plant host, Leptocarpus tenax , is widely distributed throughout the southern parts of Australia ( Fig. 5 B), and ranges from Western Australia to South Australia Victoria, New South Wales, and Queensland. At this point, there is no indication that the plant bugs occur beyond Western Australia, but future sampling on Restionaceae in other parts of Australia will test this hypothesis.

Other Specimens Examined

AUSTRALIA: Western Australia: 1 juv. (00131196) (AMNH), 10 juv. (00089818–00089827) (AM), 3.5 km N of Mt. Chudalup, D'Entrecasteaux National Park, 34.73335°S 116.0889°E, 50 m, 15-XII-97, Schuh, Cassis, Brailovsky; 13 juv. (00214330–00214342) (AM), 7.5 km N of Mt. Chudalup, D'Entrecasteaux National Park, 34.73363°S 116.0861°E, 50 m, 16-XII-97, Schuh, Cassis, Brailovsky, on Meeboldina scariosa , det. PERTH staff PERTH 05099773; 1 juv. (00215231), 38 juv. (00214496–00214526) (AM), 1♂ (00214540), 3 juv. (00128650–00128652), (AMNH), 10.1 km W of Broke Inlet Road on Chesapeak Road, D'Entrecasteaux National Park, 34.85263°S 116.3945°E, 20 m, 2-XII-99, on Leptocarpus tenax , det. PERTH staff PERTH 05671272R.T. Schuh, G. Cassis and R.Silveira; 21 juv. (00214462–00214470, 00215289–00215298, 00215331, 00215332) (AM), 2♂ (00099388, 00215308) 1♀ 4 juv. (00128619–00128622) (AMNH), Chesapeak Road, 47.2 km W of Broke Inlet Road, 34.7681°S 116.1575°E, 50 m, 3-XII-99, on Leptocarpus tenax , det. PERTH staff PERTH 05671515, R.T. Schuh, G. Cassis and R. Silveira.

Restiophylus lyginiae Leon and Weirauch, new species( Figs. 1–4 ; Tables 1–2 )

(urn:lsid:zoobank.org:act:08E3B4EA-AC39-426B-9D50-3BC4CC30FC75)

HOLOTYPE. 1♂ (00216275), AUSTRALIA, Western Australia, Madfish Bay, William Bay National Park, -35.02013, 117.25420, 100 m (329 ft), 1-XII-99, WA99_L54, on Lyginia imberbis, R.T. Schuh, G. Cassis and R. Silveira (WAMP). PARATYPES: 66 ♂ (00128386–00128412, 00215361, 00128427–00128439, 00128441–00128443, 00216350, 00216272–00216274, 00216276–00216293), 41♀ (00128418–00128426, 00128451–00128466, 00216294–00216309) (WAMP), AUSTRALIA, Western Australia, Madfish Bay, William Bay National Park, 35.02013°S 117.2542°E, 100 m, 1-XII-99, on Lyginia imberbis , det. PERTH staff PERTH 05672198, R.T. Schuh, G. Cassis and R. Silveira; 12♂ (00215233–00215240, 00215352, 00215353, 00214355, 00214356), 17♀ (00215241–00215247, 00215356–00215358, 00214549, 00214368–00214373) (AM), AUSTRALIA, 1 km S of Murchison House HS, Kalbarri National Park, 27.65822°S 114.2394°E, 60 m, 23-X-2004, on Lyginia imberbis, det. PERTH staff PERTH6988601, Cassis, Wall, Weirauch, Symonds.

Diagnosis

Recognized by the medial longitudinal line on the pronotum and scutellum (2-1), white tip on the scutellum (4-1) and the lateral cream-colored lines on the pronotum (3-1) ( Fig. 1 ) and by the short (24-0) and slender (25-0) apical process of the primary endosomal strap ( Fig. 3 ).

Description

Male: As in generic description, total length 3.72–3.91 mm ( Fig. 1 ). COLORATION: As in generic description, with pronotum and scutellum with median cream-colored longitudinal line and with lateral cream-colored lines on pronotum; scutellum with white tip; embolium pale mark along claval commisure restricted to anterior 1/4. SURFACE AND VESTITURE ( Fig. 2 G): Dorsum with black, cylindrical, suberect setae intermixed with subadpressed, slightly flattened pale setae on hemelytra. STRUCTURE: Head ( Fig. 1 ): As in generic description. GENITALIA: Pygophore : As in generic description. Endosoma ( Fig. 3 ): As in generic description, with apical process of primary strap about equal length of apex and with apical process slender. Phallotheca : As in generic description. Left paramere ( Fig. 3 ): As in generic description, with anterior process slender in lateral view; posterior process in dorsal view slightly longer than anterior process. Right paramere ( Fig. 3 ): As in generic description. Female: See generic description for structural details and Fig. 1 for habitus and coloration

Etymology

A noun in genitive case and named for the association with plants in the genus Lyginia Brown.

Hosts

Recorded from two species of Lyginia (Anarthriaceae): L. imberbis Brown and L. barbata Brown ( Fig. 5 C; Table 2 ).

Distribution

Known from three collection events in the southwestern tip of Western Australia and the west coast south of Shark Bay.

Other Specimens Examined

AUSTRALIA: Western Australia: 11♂ (00131088–00131098), 1 juv. (00131099), 7♀ (00131100–00131106), 7.5 km N of Mt. Chadulaup, D’Entrecasteaux National Park, 34.73335°S 116.0889°E, 50 m, 15-XII-97, Schuh, Cassis, Brailovsky; 36 juv. (00128413–00128417, 00128444–00128450, 00216351–00216374), 1♂ (00128440) (AMNH). Madfish Bay, William Bay National Park, 35.02013°S 117.2542°E, 100 m, 1-XII-99, R.T. Schuh, G. Cassis and R. Silveira, Lyginia imberbis , det. PERTH staff PERTH 05672198; 43, juv. (00215248–00215277, 00215354, 00215355, 00214357–00214367) (AM), 1 km S of Murchison House HS, Kalbarri National Park, 27.65822°S 114.2394°E, 60 m, 23-X-2004, on Lyginia imberbis , det. PERTH staff PERTH6988601, Cassis, Wall, Weirauch, Symonds.

Restiophylus meeboldinae Leon and Weirauch, new species( Figs. 1 , 2 , and 4 ; Tables 1–2 )

(urn:lsid:zoobank.org:act:C6F5ED2B-6071-4D99-B136-80517CD759B9)

HOLOTYPE: 1♀ (00128468), AUSTRALIA, Western Australia, 13 Km E of Denmark on South Coast Highway, -34.98333, 117.50000, 80 m (262 ft), 1-XII-99, on Leptocarpus scariosus , R.T. Schuh, G. Cassis and R. Silveira (WAMP). PARATYPE: 1♀ (00214340) AUSTRALIA, Chesapeak Road, 47.2 km W of Broke Inlet Road, 34.7681 ° S 116.1575 ° E, 50 m, 03 Dec 1999, R.T. Schuh, G. Cassis and R. Silveira, 3-XII-99, on Leptocarpus tenax , det. PERTH staff PERTH 05671515, R.T. Schuh, G. Cassis and R. Silveira (WAMP).

Diagnosis

Female: Recognized among species of Restiophylus by the pale medial longitudinal line on the pronotum and scutellum (2-1) ( Fig. 1 ) and the lack of white silvery setae on the corium (8-0; 9-0) ( Fig. 2 H). Shares a host plant with R. leptocarpi ( Leptocarpus spp.), but clearly differentiated from that species by coloration and vestiture.

Description

Female: As generic description, with length 4.06–4.32 mm ( Fig. 1 ). COLORATION: As generic description, with pronotum and scutellum with median cream-colored longitudinal line; tip of scutellum white; embolium with pale mark along entire length of claval commissure. SURFACE AND VESTITURE ( Fig. 2 H): Dorsum with black, cylindrical, suberect setae on hemelytra. STRUCTURE: As in generic description. GENITALIA: See generic description.

Etymology

A noun in genitive case and named for the association with plants in the subgenus Meeboldina of the genus Leptocarpus Brown

Hosts

Recorded from two species of Leptocarpus : L. ( Meeboldina ) scariosus Brown and L. ( Leptocarpus ) tenax Brown ( Fig. 5 B; Table 2 ).

Distribution

Known from two collecting events in the South West region of Western Australia ( Fig. 4 ). Leptocarpus ( Meeboldina ) scariosus shows a small endemic range in that area that is closely matched by the plant bug species.

Other Specimens Examined

AUSTRALIA: Western Australia: 17♀ (0099381, 00128467–00128482), 13 Km E of Denmark on South Coast Highway, -34.98333, 117.50000, 80 m (262 ft), 1-XII-99, on Leptocarpus ( Meeboldina ) scariosus det. PERTH staff PERTH 05672198 R.T. Schuh, G. Cassis and R. Silveira.

Discussion

Only females of R. meeboldinae were collected. All specimens examined showed significant differences in coloration and vestiture when compared to other species of Restiophylus. We find these differences significant enough to treat R. meeboldinae as a separate species.

Discussion

Cladistic Analysis

The cladistic analysis resulted in six equally parsimonious trees (L = 320; CI = 36; RI = 58). All trees recovered a monophyletic Restiophylus with jackknife support of 60 ( Fig. 6 ) as well as a sister group relationship between Restiophylus and a clade comprising the New World taxa Semium hirtus Reuter and Tytthus amazonicus Carvalho, both members of the subtribe Semiina. Furthermore , Restiophylus  + ( Tytthus  +  Semium ) was recovered as sister to part of the subtribe Exocarpocorina that comprises several other Australian taxa (e.g., Jiwarli Soto and Weirauch, Exocarpocoris Weirauch). The trees differed in the placement of “Protemiris conospermi” (ms name), Leptidolon galbanus ( Eyles and Schuh 2003 ) and Jiwarli heliotropium Soto and Weirauch within Exocarpocorina as well as in the relationships within Restiophylus , specifically the position of R. meeboldinae. We chose the tree illustrated in Fig. 6 because it placed R. meeboldinae in a clade with R. hypolaenae and R. lyginiae with multiple characters supporting this grouping. Alternate tree hypotheses placed R. meeboldinae outside the R. lyginiae  +  R. hypolaenae clade, leaving its position unresolved within Restiophylus. Exocarpocorina is polyphyletic in these analyses, with Wallabicoris Schuh and Pedraza being recovered as sister group to Plagiognathus Fieber and the clade comprising a species of Larinocerus Froeschner, which is part of the Nasocorini, and Capecapsus Schuh and Coatonocapsus Schuh, members of the Cremnorrhini, as sister to the Xiphoides clade ( Weirauch and Schuh 2010 ). Several morphological characters are in support of the monophyly of Restiophylus , including the pale lateral margin of the pronotum (5-1) and the vivid coloration of females (44-1). Within Restiophylus , R. leptocarpi is recovered as the sister species to a clade comprising the remaining species of Restiophylus. The relationships within this clade are unresolved, but these three species are unified by coloration patterns of the pronotum (2-1) as well as the white-tipped scutellum (4-1) . Restiophylus lyginiae is defined by several autapomorphies, including the short apical process of the primary strap (24-0) and the presence of a “conspicuous shoulder” on the anterior process of the left paramere (38-2). The flaring of the process of the primary strap is unique to R. hypolaenae.Restiophylus meeboldinae differs in vestiture ( Fig. 2 G) and coloration from the remaining described species in this new genus, but examination of male genitalia will be crucial to further evaluate its relationships within the genus.

The analyses and re-classification of Phylinae by Menard et al. (2014) and Schuh and Menard (2013) allow for evaluation of the results of our small cladistic analysis that focuses on Restiophylus. Our analysis included a diverse range of Phylinae, with emphasis on Australian taxa, but also African and New World taxa, with 17 of the included taxa classified in the subtribe Exocarpocorina, within the tribe Semiini, and two taxa representing the subtribe Semiina. Species of the Exocarpocorina show the highest diversity in Australia and New Zealand and the clade is characterized by the asymmetrical sclerites of the female vestibulum, elaborations of the posterior wall of the female genitalia, and the horizontally expanded central portion of the left paramere ( Schuh and Menard 2013 ). Males of Exocarpocorina consistently show a broad, flat and T-shaped endosoma with a medial, well-developed secondary gonopore and lateral straps ( Schuh and Menard 2013 ). Semiina is composed of taxa that have been of problematic taxonomic placement and have much broader distributions than species of Exocarpocorina ( Menard et al. 2014 ). The group is characterized by the extremely simplified tubular endosoma ( Schuh and Menard 2013 ), a feature also observed in the nominal New World genus Semium Knight ( Kelton 1959 ) as well as some members of the genus Tytthus ( Henry 2012 ), and the simple posterior wall of the female genitalia ( Slater 1950 , Henry 2012 ). In our analysis, Restiophylus is recovered as sister to members of the subtribe Semiina; this relationship is supported by the pale coloration of the costal margin (6-1) as well as multiple characters of the male endosoma (19-1), (20-0), (21-0), and (29-0). The simplicity of both male and female genitalia in Restiophylus also suggests that this new genus is best placed in the subtribe Semiina.

Host Relationships

Host specificity of species of Restiophylus occurs at two levels: first, all specimens of this plant bug genus were collected from Australian restiids and we hypothesize that the last common ancestor of this plant bug genus was likely associated with plants in this group, and then diversified on restiids. Second, although there are currently 35 genera of restiids recorded from Australia (AVH taxon record [ http://avh.ala.org.au/#tab_simpleSearch ]) any given species of Restiophylus plant bugs seems to show an association with plant species in a given genus (or subgenus) of restiids (see Table 2 ). Due to small sample size (two or three collection events for each of the four species), it is premature to hypothesize that species of Restiophylus may show preferences for individual host plant species, even though the uneven numbers of specimens collected from different plant species may indicate this (e.g., R. hypolaene : 32 specimens collected from H . exsulca , but 165 specimens from H. humilis ).

Restiophylus species are currently the only arthropods that are documented to be closely associated with Australian restiids. Given the abundance of insects using African Restionaceae as host plants, this is somewhat surprising, and may indicate that the Australian fauna is at present poorly sampled. Recent systematic work on both Anarthriaceae and Australian Restionaceae (i.e., Briggs et al. 2014 , Briggs 2014 ) could provide an excellent foundation for future studies focusing on the host relationships of this group of plants and its arthropod herbivores.

Supplementary Data

Supplementary data are available at Annals of the Entomological Society of America online.

Acknowledgments

We thank Randall T. Schuh and Gerasimos Cassis (and their field teams) for their tremendous efforts in collecting Miridae and documenting host plants in past decades, making this project possible. A special thank you to the members of the Heteropteran Systematics (Weirauch) Lab: Aleksandr Knyshov, Eric Gordon, Michael Forthman, Filipe Michels Bianchi, Junxia Zhang, and Rochelle Hoey-Chamberlain for their comments on earlier versions of this manuscript. This project was made possible in part by the NSF (National Science Foundation) Planetary Biodiversity Inventory grant (PBI) DEB-0316495 awarded to Randall T. Schuh and Gerasimos Cassis; C.W. was a postdoctoral fellow on this grant.

References Cited