Revision of the staphylinoid and ground-dwelling genus Carvalhoma Slater & Gross ( Insecta : Heteroptera : Miridae : Cylapinae ) of Australia

The Australian endemic staphylinoid plant bug genus Carvalhoma Slater & Gross, 1977 is revised. The genus is redescribed and its systematic position within Cylapinae is discussed. Carvalhoma malcolmae Slater & Gross, 1977 and C. taplini Slater & Gross, 1977 are redescribed. Three species, C. ovatum sp. nov., C. parvum sp. nov., and C. weiri sp. nov., are described as new to science. A key to species, digital habitus images, SEM images, drawings of male and female genitalia and distribution map are provided.


R e s e a r c h a r t i c l e
urn:lsid:zoobank.org:pub:D7072C87-B839-4B55-A0A9-4785E04ACAA3 In contrast, the subfamily Cylapinae has received relatively little attention.This subfamily has a worldwide distribution, but collecting of its representatives is hampered by their cryptic habits, as they usually live under the bark, in litter, or on fungi (Gorczyca 2001).Currently the cylapine fauna of Australia includes 17 genera and 35 species (Cassis & Gross 1995;Gorczyca 2001;Cassis et al. 2003;Moulds & Cassis 2006;Wolski & Gorczyca 2014), although we estimate that the number of cylapine species represented in the collections is close to 100.Among Australian cylapines only the genera Peritropis Uhler, 1891 and Xenocylapidius Gorczyca, 1997 from the tribe Fulviini and Australian species from the tribe Vanniini have been revised recently (Cassis et al. 2003;Moulds & Cassis 2006;Wolski & Gorczyca 2014).
The aims of this work are to revise the Australian endemic genus Carvalhoma Slater & Gross, 1977, including a redescription and diagnosis of the genus, to discuss its systematic placement within Cylapinae, to redescribe the two previously described species, and to describe three new species.

Specimens
Twenty eight specimens were examined in this study.A unique specimen identifier with a UNSW_ENT prefix, unless otherwise stated, was attached to each specimen.Collection event data were digitised in the Plant Bug Planetary Biodiversity Inventory Database (http://research.amnh.org/pbi/databases/locality_database.html),which can also be accessed on the Discover Life website (http://www.discoverlife.org/) and the Heteroptera Species Page (http://research.amnh.org/pbi/heteropteraspeciespage/).
The specimens used for the descriptions of species are preserved in the following institutions: AM = Australian Museum (Sydney, Australia) ANIC = Australian National Insect Collection (Canberra, Australia) QM = Queensland Museum (Brisbane, Australia) NTM = Northern Territory Museum and Art Gallery (Australia) CAS = California Academy of Science (San Francisco, USA)

Dissections and terminology
Terminology mostly follows Schuh & Slater (1995) and Cassis & Schuh (2012).Specimens were dissected following Kerzhner & Konstantinov (1999).The terminology for male genitalia follows Kerzhner & Konstantinov (1999) and Konstantinov (2003), and the notion of the aedeagal endosoma is also consistent with the definition of Cassis (2008).The terminology for female genitalia follows Davis (1955).A single male and female were dissected for each of Carvalhoma malcolmae and C. weiri sp.nov.; two males and three females were dissected for C. parvum sp.nov.We decided not to dissect C. taplini as it is known only from two females, representing holotype and paratype, and we found it is European Journal of Taxonomy 253: 1-27 (2016) impossible to remove the abdomen of either of them without damaging the specimen.All parameres and genital capsules are illustrated in the dorsal view.

Images
Scanning electron micrographs of uncoated specimens were taken using a Hitachi TM-3000 desktop scanning electron microscope.Dorsal habitus digital images were made using the Visionary Digital Imaging system (www.visionarydigital.com) with a Canon EOS 40D camera.Multiple images were taken of a male and a female for each species where possible and concatenated using Helicon Focus software (www.heliconsoft.com).

Measurements
Measurements were taken for core mirid characters and are given in Table 1.They were taken using a Leica graticule and 10× eye pieces, attached to a Leica MZ16 stereo microscope.All measurements are given in millimetres, unless otherwise stated.

Diagnosis
Distinguished by staphylinoid hemelytron, reaching abdominal segments V-VI, veins obsolete, with distinct punctation or rugopunctate; hypognathous head with shallow midline depression, eyes embedded into head, not pedunculate (Figs

Description Male
Colouration.Body often mostly dark brown to black, rarely mostly pale brown (Fig. 1).

Diagnosis
Recognised by the following characters: large size, 2.25 in male and 2.3-2.8 in female; elongate body; pronotum ca 1.1× as long as wide in male and ca 1.2-1.3× in female (Fig. 1); head, pronotum and hemelytra shiny, male mostly dark brown to black (Fig. 1); lateral margins of pronotum mostly smooth, with a few rugosities, without dense setae (Fig. 2C); frons produced anteriad of eyes for more than half of eye diameter in dorsal view (Figs 1B, 2B); head ca 2.1× as wide as long in male and 1.7-2.2× in female; antennal segment I relatively long, ca 2.0× as long as vertex width in male and ca 1.8-2.2× in female.
SurfaCe and veStiture.Head and pronotum more or less smooth and shiny, except for shagreened collar; lateral margin of pronotum only with a few wrinkles, without dense setae; pleura with setae only in metepisternum anteriorly; hemelytron shiny, with distinct punctures.Dorsum and abdomen clothed with long erect pale simple setae.
StruCture and meaSurementS.Body ca 4.9× longer than pronotal width; head ca 2.1× wider than long, frons protruding anteriad at distance of more than half of eye diameter dorsally (Figs 1, 2B); vertex ca 1.2× wider than eye diameter; head ca 1.1× wider than high; antennal segment I twice length of vertex, antennal segment II longer than either segments I or III, ca 4.6× longer than vertex width, ca 2.3× longer than segment I; segment III slightly longer than segment I, segment IV slightly shorter than antennal segment III; labial segments I and II subequal in length, segment III slightly shorter than segment II, and segment IV slightly shorter than segment III (Fig. 2H); pronotum ca 1.1× wider than long, ca 0.8× width of head; metepimeron with distinct ridge (Fig. 2K); hind femur ca 3× longer than head height; tarsal segment I almost twice as long as segment II, segment II slightly shorter than segment III (Fig. 2).genitalia (Fig. 7A-E).Right paramere without ridge dorsally; outer margin of right paramere straight, apices of parameres straight, not hook-shaped; left paramere with ridge dorsally, its basal swelling rounded; theca mostly membranous, sclerotised apically; endosoma with single sclerite, placed ventrally on right side.Female body lengtH.2.3-2.8.
Colouration (Fig. 1).Similar to male, but usually somewhat darker; antennal segment IV brown to dark brown; labial segment I reddish or reddish brown, sometimes segment II reddish brown, segments III and IV rarely pale brown; labium yellow to pale brown, darkened apically, segment I sometimes reddish or with reddish tinge; coxae dark brown to black, yellow apically.
SurfaCe and veStiture.As in male.

Distribution
Eastern regions of NSW and Victoria (Fig. 11).

Remarks
Antennal segment IV is broken in males, and only partly present in examined females.

Differential diagnosis
Carvalhoma malcolmae was described from a single female specimen (Slater & Gross 1977) and the holotype is preserved in the Museum of Victoria.The specimen is damaged and photos of it are available at http://collections.museumvictoria.com.au/specimens/1018994.The non-type specimens we examined seem to be conspecific with the holotype and fit the original description.The only difference is a pair of strap-like sclerites on the dorsal labiate plate of the bursa copulatrix, as reported by Slater & Gross (1977), and we failed to find those structure in C. malcolmae and other congeners.However, the illustration of the bursa by Slater & Gross (1977) is not sufficiently detailed, and we refrain from drawing any further conclusions.The male genitalia of non-type material are very similar to those illustrated by Schuh & Schwartz (1984).Although they did not mention the sclerotised area in the description of the endosoma (= vesica in Schuh & Schwartz 1984), it was depicted on their fig.7.
Carvalhoma malcolmae is most similar to C. parvum sp.nov.externally, with both species having an elongate body and a dark brown to black dorsum (Fig. 1).Carvalhoma parvum sp.nov.differs in being smaller in size, with the body length 1.5-1.6 in male and 1.9-2.2 in female, the distinctly rugulose and densely setose lateral margins of the pronotum (Fig. 4C), the densely setose pleura (Fig. 4D), and the short antennal segment I, ca 1.4-1.8×as long as vertex width in male and ca 1.3-1.4× in female.
Carvalhoma malcolmae also shares many characters in structure with C. weiri sp.nov., but the latter species differs in the colouration of the male, being mostly whitish yellow to pale brown (Fig. 1), the head is more transverse, ca 2.7-2.9× as wide as long in male and ca 2.3× in female (Fig. 6C).

Etymology
The species is named for the oval body of males, whereas males of other species have an elongate body; from the Latin "ovatus", meaning "oval".Colouration (Fig. 1).Mostly dark brown to black, hind tibia apically and tarsi pale brown.

European Journal of Taxonomy
SurfaCe and veStiture.Body mostly matte and shagreened; pronotum laterally not wrinkled (Fig. 3A); pronotum laterally and pleura almost entirely clothed with short setae (Fig. 3G); dorsum clothed with very short setae only, few dark suberect setae present on head and pronotum (Fig. 3B, E, H); appendages and abdomen clothed with suberect or adpressed dark setae shorter than width of antennal segment II (Fig. 3D, F, I).StruCture and meaSurementS.Body ca 3.5× longer than pronotum width; frons only slightly protruding anteriad of eyes in dorsal view (Figs 1, 3B); head ca 2.4× wider than long, vertex ca 1.3× wider than eye diameter; in anterior view head ca 1.1× wider than high; antennal segment I ca 1.5× longer than vertex width, segment II ca 3.7× longer than vertex width, and ca 2.5× longer than segment I; labial segments I and II subequal in length, segments III and IV each shorter than segment II, subequal in length to each other; pronotum ca 1.6× wider than long, ca 0.9× wider than head, with single oval depression medially; metepimeron with shallow but distinct ridge (Fig. 3G).genitalia (Fig. 8).Right paramere with ridge dorsally, hook-shaped apically, its outer margin concave (Fig. 8D); left paramere with angulate basal swelling and hook-shaped apex, without dorsal ridge (Fig. 8E).Theca mostly sclerotised, endosoma with large sclerite, placed ventrally, smaller sclerite placed dorsally, and sclerotised area placed dorsally near base of endosoma in repose; membrane near base of endosoma thick, with small tubercles (Fig. 8A-B).

Female
Unknown.

Distribution
Known only from the type locality, Darlington, southwestern part of Western Australia (Fig. 11).

Remarks
Carvalhoma ovatum sp.nov. is distinguished by its oval male and shagreened hemelytron with shallow punctures, and it is not similar to congenerics.

Diagnosis
Recognised by the following combination of characters: head, pronotum, hemelytron and antennal segment I shiny and dark brown to black (Fig. 1); body small, 1.5-1.6 in male and 1.9-2.2 in female; head elongate, ca 3.7-4.0×as long as pronotum width in male and 4.1-4.5× in female; pronotum laterally covered with dense wrinkles and setae at sides (Fig. 2C); antennal segment I short, ca 1.4-1.8×as long as vertex width in male and ca 1.3-1.4× in female.

Etymology
The specific epithet refers to the size of the males, which are smaller than its congeners; from the Latin "parvus", meaning "small, minute, short".

Distribution
Known from the southeastern part of Queensland and northeastern New South Wales (Fig. 11).Colouration (Fig. 1).Mostly brown to dark brown, sometimes with reddish tinge, clypeus pale brown, labial segment I reddish brown to reddish, segments II-IV whitish yellow to yellow, segment IV brown apically; antennal segment II yellow, often reddish apically; fore-and middle coxae whitish yellow, often darkened basally; hind coxa the same colour as fore-and middle coxae or dark brown; femora reddish or dark brown, often whitish yellow basally, tibia whitish yellow, often darkened basally, tarsi whitish yellow to yellow.
Colouration (Fig. 1).Similar to male, but usually somewhat darker, colour of labial segments III-IV, coxae and tarsi varying from yellow to brown, tibiae whitish yellow to pale brown, often brown at extreme apex.

SurfaCe and veStiture. As in male.
StruCture and meaSurementS.Body ca 4.1-4.5×longer than pronotum width; head ca 1.9-2.2× wider than long, vertex ca 1.0-1.3×wider than eye diameter; head ca 1.1-1.3×wider than high; antennal segment I ca 1.3-1.4×longer than vertex width, segment II ca 3.1-3.7×longer than vertex width, and ca 2.2-2.5×longer than segment I, segment IV slightly longer than segment III; pronotum ca 1.2-1.3×wider than long, ca 0.8-0.9×wider than head; hind femur twice longer than head height.

Diagnosis
Separated from all other species in the genus by the following characters: head and pronotum matte and shagreened, hemelytron shiny, with distinct punctures (Fig. 1G); body large and ovate, total length of female 2.1-2.3,ca 3.6-3.8×longer than pronotum; antennal segment I ca 1.2-1.4×as long as vertex width; pronotum laterally with dense wrinkles and setae (Fig. 5G).
Colouration (Fig. 1G).Dark brown, mostly with reddish tinge, head anteriorly pale brown to yellow, antenna, labial segments I-III, fore-and middle coxa, tibiae and tarsi yellow, hind coxa brown or yellow, ventral side of abdomen pale brown or brown.
StruCture and meaSurementS.Body ca 3.6-3.8×longer than pronotum width; frons protruding anteriad at distance subequal to at least half of eye diameter in dorsal view (Figs 1, 5B), ca 2.0× as wide as long, vertex ca 1.1-1.4×as wide as eye diameter; head ca 1.2-1.4×as wide as high (Fig. 5C); antennal segment I ca 1.2-1.4×longer than vertex width, segment II ca 2.9-3.2×longer than vertex width, and ca 2.2-2.3×longer than segment I; segment III subequal to segment I, segment IV slightly shorter than segment III; labial segments I and II subequal in length, segments III and IV each shorter than segment II, subequal in length to each other (Fig. 5D); pronotum ca 1.4-1.5×wider than long, ca 0.9× wider NAMYATOVA A.A. & CASSIS G., Revision of the genus Carvalhoma of Australia than head, with single oval depression medially; metepisternum with very shallow ridge (Fig. 5G); hind femur ca 1.5× longer than head height; tarsal segment I almost twice as long as segment II, segment II slightly shorter than segment III (Fig. 5E).

Distribution
Known from a single locality in northeastern South Australia (Fig. 11).

Differential diagnosis
Due to its surface and oval body shape (see diagnosis) Carvalhoma taplini is not very similar to the congenerics.

Diagnosis
Recognized by the following combination of characters: head, pronotum and hemelytron shiny, hemelytron with distinct punctures; body in male mostly pale brown, antennal segment I in both sexes whitish yellow to pale brown (Fig. 1); lateral side of pronotum smooth, almost without wrinkles and setae; antennal segment I long, ca 1.9-2.1×as long as width of vertex in male and ca 1.2× in female.European Journal of Taxonomy 253: 1-27 (2016) Colouration (Fig. 1).Head brown or reddish brown, clypeus, maxillary and mandibular plates yellow, pronotum and scutellum brown or reddish brown; pleura brown, with yellow metathoracic scent gland evaporative area; hemelytron yellow, brown basally and with brown punctures; antenna, labium, legs and abdomen yellow, forefemur sometimes with reddish tinge, abdomen with pale brown or brown markings.SurfaCe and veStiture.Head shiny, pronotum shiny with collar shagreened, scutellum shagreened (Fig. 1); pronotum smooth laterally, without wrinkles or short setae; pleura with short setae only on anterior part of metapleuron (Fig. 6J); setae on dorsum, appendages and abdomen almost absent.
Colouration (Fig. 1).Darker than in male.Head dark brown, with clypeus and mandibular plate pale brown, antennal segment I and labium yellow; pronotum and scutellum dark brown; pleura dark brown; coxae pale brown to brown, paler apically; femora pale brown, tibia and tarsi yellow; abdomen brown.SurfaCe and veStiture.Similar to male, but setae on dorsum and legs distinct.
StruCture and meaSurementS.Body ca 5.0-5.1×longer than pronotum width; head ca 2.3× wider than long, vertex ca 0.9× wider than eye diameter; head ca 1.2× wider than high; antennal segment I ca 2.1× longer than vertex width, segment II ca 4.9× longer than vertex width, and ca 2.3× longer than segment I; pronotum ca 1.1× wider than long, ca 0.8× wider than head; hind femur ca 2.5× longer than head height.

Distribution
Known only from the Australian Capital Territory (Fig. 11).

Remarks
Antennal segments III and IV are broken in the males of the type material, and segments II-IV are broken in the female.In contrast to other Carvalhoma species, specimens of C. weiri sp.nov.are relatively pale, and genitalia also very soft and pale, which can indicate that the specimens are teneral.

Differential diagnosis
Carvalhoma weiri sp.nov. is most similar to C. malcolmae in the relatively large size, elongate body, surface and vestiture (Fig. 1).However, C. malcolmae differs in the mostly dark brown to black male (Fig. 1), the frons distinctly protruding anteriad of the eyes (Figs 1, 2B), in dorsal view ca 2.1× as wide as long in male and 1.7-2.2× in female.Slater & Gross (1977) described Carvalhoma, placing it in the nominotypical tribe of the subfamily Phylinae.Schuh & Schwartz (1984) transferred the genus to the subfamily Cylapinae.We agree with the latter decision.The representatives of Cylapinae are very diverse morphologically, but all of them have a similar structure of the tarsus and pretarsus, with thin tarsi, no pulvilli, setiform parempodia and slender claws often toothed apically (Gorczyca 2000;Cassis & Schuh 2012).The structure of the unguitractor in Carvalhoma is very similar to that found in other Cylapinae, except for the Vanniini, as described in Namyatova et al. (2016) (compare Figs 2L and4I with fig. 21E in Namyatova et al. 2016), with three rows of lamellae on the unguitractor placed close to each other and with the medial row of lamellae being characteristically acute.The position of the lamellate rows of the unguitractor in Carvalhoma is unique, with the three rows of lamellae separated in comparison to being contiguous as in other cylapines (fig.21E in Namyatova et al. 2016).All examined species of Cylapinae, except for Vannini, in Namyatova et al. (2016) also have asymmetrical parempodia with the outer parempodia in NAMYATOVA A.A. & CASSIS G., Revision of the genus Carvalhoma of Australia dorsal view strongly reduced.Although the SEM image is not particularly clear, Carvalhoma shares the same type of parempodia asymmetry (Fig. 4I).

Discussion
The tribal placement of Carvalhoma within Cylapinae is uncertain.Among Cylapinae tribes, this genus is not similar to Bothriomirini, as its members are stout bugs with the head and pronotum punctate and the pronotum without a collar (Wolski & Gorczyca 2012).It also does not fit to the diagnosis of Rhinomirini, as this tribe has a horizontal head (Gorczyca 2000).Although there are brachypterous species within Vanniini, this tribe differs from Carvalhoma in having flattened spatulate parempodia and impunctate hemelytra (Cassis et al. 2003).Gorczyca (2000Gorczyca ( , 2006) ) and Schuh (2003Schuh ( -2013) ) treated the genus within the tribe Fulviini.In contrast, Cassis & Gross (1995) in their catalogue of the Australian heteropteran fauna placed Carvalhoma within Cylapini.
When using Gorczyca's taxonomic key (Gorczyca 2000), Carvalhoma cannot be assigned to Fulviini or Cylapini with any confidence.According to this key the main difference between those two tribes is the structure of antennae.They are either longer than the body, with antennal segment IV being the longest in Cylapini, or the antennae are shorter than the body, with antennal segment II being longest in Fulviini.In Carvalhoma, antennal segment IV is the longest segment, but the antennae are as long as or slightly longer than the body Although Fulviini is likely a convenience group, most of its genera are characterised by a more or less prognathous head, whereas Carvalhoma has a strongly hypognathous head, which is elongate and dorsoventrally oriented, and with a swollen frons; this is more similar to the head of Cylapini (Gorczyca 2000).Carvalhoma is not very similar to most of the New World genera of Cylapini, as they usually have the antennae longer than the body and prominent eyes.However, some New World and Old World genera placed in the Cylapini by Gorczyca (2000Gorczyca ( , 2006) ) have eyes which are not prominent and/or antennae shorter than the body; these include Corcovadocola Carvalho, 1948) Cylapoides Carvalho, 1952, Phyllocylapus Poppius, 1913, and Cylapomoprha Yasunaga, 2000. Murphy & Polhemus (2012) also placed Mangalocoris Murphy & Polhemus, 2012, known from Singapore and Thailand, in the Cylapini; this genus has antennae distinctly longer than the body and fits the diagnosis of the tribe provided by Gorczyca (2000), and it is externally similar to Carvalhoma.Based on this, we support the placement of Carvalhoma in the tribe Cylapini (Cassis & Gross 1995), but acknowledge that an explicit phylogenetic analysis is required to determine its relationships with other genera of Cylapinae.
With respect to the proximity of relationship of Carvalhoma to Mangalocoris, both taxa have shortened wings, enlarged forefemora and a similar ratio of labial segments.Although Murphy & Polhemus (2012) did not give a detailed description of the external efferent system of the metathoracic glands of Mangalocoris, their illustration indicates that it is elongate and similar to that of Carvalhoma.Mangalocoris is separated from Carvalhoma by having very short wings, covering only the anterior part of the second abdominal tergite, and two-segmented tarsi.
Other species of Cylapinae with a hypognathous head and shortened wings include the Brazilian genus Corcovadocola Carvalho, 1948 and the Australian genus Schizopteromiris Schuh, 1986. Based on Carvalho's (1948) original description, Corcovadocola is separated from Carvalhoma by the following characters: males macropterous, forewings in female reaching abdominal segment IX, and the pronotum 3× wider than long.Schizopteromiris and Carvalhoma possess the similar hypognathous head, with a protruding frons and a similar ratio of labial segments, but can be separated by the former having a distinctly convex hemelytron, covering almost the entire abdomen, and the broad external efferent system of the metathoracic glands (Schuh 1986).
European Journal of Taxonomy 253: 1-27 (2016) In this paper, the genus Carvalhoma is revised and three new species, C. ovatum sp.nov., C. parvum sp.nov.and C. weiri sp.nov., are described.There might be more species of this genus inhabiting Australia, but not yet collected, due to the difficulties in finding representatives of this group.
As a result of this work the number of known species in Australia increased from five to eight for Cylapini and from 35 to 38 for Cylapinae, with some genera and many species awaiting description.

. 1 .
Fig. 1.Habitus of Carvalhoma species.Scale bar = 1 mm.When two specimens of the same species are shown, the male is on the left and the female on the right.C. ovatum sp.nov.shows the male holotype.C. taplini Slater & Gross, 1977 shows the female holotype.

Fig. 8 .
Fig. 8. Genitalia of C. ovatum sp.nov. A. Aedeagus, left lateral view.B. Aedeagus, ventral view.C. Genital capsule.D. Right paramere.E. Left paramere.Scale bars = 0.1 mm (the large scale bar is for A-B and D-E, the small scale bar is for C).

Fig. 9 .
Fig. 9. Genitalia of C. parvum sp.nov. A. Aedeagus, left lateral view.B. Aedeagus, ventral view.C. Genital capsule.D. Right paramere.E. Left paramere.F. Dorsal labiate plate of bursa copulatrix.G. Posterior wall of bursa copulatrix.Scale bars = 0.1 mm (the large scale bar is for A-B and D-E, the small scale bar is for C and F-G).

Fig. 10 .
Fig. 10.Genitalia of C. weiri sp.nov. A. Aedeagus, left lateral view.B. Aedeagus, ventral view.C. Genital capsule.D. Right paramere.E. Left paramere.F. Dorsal labiate plate of bursa copulatrix.G. Posterior wall of bursa copulatrix.Scale bars = 0.1 mm (the large scale bar is for A-B and D-E, the small scale bar is for C and F-G).

Table 1 .
Measurements.Abbreviations: Cunclyp = the length between apex of clavus and the base of clypeus; AntSeg = the antennal segment; InterOcDi = the vertex width.