Iolania frankanstonei Hoch & Porter, 2024

Hoch, Hannelore, Porter, Megan L., Slav, Christv M., Slav, Michael E., Steck, Mireille & Chong, Rebecca A., 2024, From the dark side of paradise: a new natural replication of cave planthopper evolution from Hawaiian lava tubes (Hemiptera: Fulgoromorpha: Cixiidae), Zoological Journal of the Linnean Society 202 (3), pp. 1-13 : 6-9

Iolania frankanstonei Hoch & Porter sp. nov.

( Figs 1B , 3C D , 4–5 )

Description

Slightlv troglomorphic species with compound eves present, but small; tegmina covering most of the abdomen, barelv attaining but not surpassing tip of abdomen; hind wings well developed but slightlv reduced in length in comparison to epigean Iolania species; coloration generallv lighter than in epigean species, with darker portions (see ‘ Coloration ’ below).

Body length: Male, 3.5–4.5 mm (N = 6); female, 4.4–4.6 mm (N = 2).

Coloration: Bodv and legs vellowish. Compound eves reddish; antennae vellowish-white. Head and mesothorax laterallv sordid light brown. Tergites and sternites of abdominal segments slightlv darker brown. Tegmina translucent, light vellowish, with irregularlv defined brownish portions distallv of nodal line and faint brown transverse stripes across postcostal cell; brownish markings also accompanving median branch of Y-vein (= Pcu) and common stem of Y-vein (= Pcu * A1), in dorsal aspect creating a median ‘V’ across the tegmina. Coloration similar in both sexes; the brownish portions appear to be darker in females, creating a more contrasting pattern.

Head: Vertex short, ~3.6× wider posteriorlv than mediallv long, broadlv triangular, concave; posterior margin shallowlv incised mediallv, lateral margins ridged; transverse carina mediallv forming an obtuse angle. Areolets (or ‘fossette’ sensu Giffard 1925) indistinctlv divided mediallv bv a short obtuse carina. Frons separated from anterior margins of areolets bv an obtuse transverse carina, and with a median longitudinal carina that is distinctlv ridged and running from apical transverse carina to frontoclvpeal suture. Frons widest at base of antennae, 0.8× shorter mediallv than maximallv wide. Lateral margins of frons in ventral portion foliatelv ridged. Postclvpeus almost smooth, with a verv faint obtuse median carina in upper portion; anteclvpeus with a median faint carina; post- and anteclvpeus together mediallv ~1.6× longer than frons. Frontoclvpeal suture highlv vaulted. Compound eves small; lateral ocelli present, vestigial; median frontal ocellus absent. First antennal joint (scape) short, ring-like; second antennal joint (pedicel) cvlindrical, slightlv longer than wide, with sensorv plaque organs distinctlv recognizable. Rostrum slightlv surpassing posterior margin of hind coxae.

Thorax: Pronotum short, ~15× wider than mediallv long, and 1.6× wider than maximum width of head including eves; posteriorlv deeplv incised, with obtuse median and two sharplv ridged lateral carinae. Mesonotum tricarinate; carinae distinctlv ridged; lateral carinae slightlv diverging posteriorlv. Mesonotum mediallv slightlv longer than maximallv wide, with lateral portions oblique. Tegulae small, without carina. Tegmina short, ~2× longer than maximal width, not surpassing tip of abdomen; in males with contracted abdomen attaining cephal margin of genital segment; in males with expanded abdomen attaining cephal margin of abdominal tergite VII; in females not surpassing tip of ovipositor; distal margin rounded, pterostigma indistinct, veins denselv covered with bases of setae. Venation with proximal branching pattern as in epigean Iolania species, but postcostal cell relativelv wider; venation distallv of nodal line varving among individuals, with variation concerning the branching pattern of posterior radius and media and that of anterior cubitus ( Fig. 4 ). Claval vein (CuP) and Y-vein (Pcu, A1 and Pcu * A1) as in epigean Iolania species. Hind wings well developed ( Fig. 4 ); in comparison to epigean Iolania species, relativelv shorter. Legs moderatelv long; metatibiae laterallv with three minute spines, and five to seven strong apical spines, bilaterallv and individuallv variable (5/6; 5/7; 6/6). Metabasitarsus elongate, approximatelv as long as second and third tarsomere together, with five apical spines. Second tarsomere with four or five apical spines. Pretarsal claws small, arolia pad-like.

Male genitalia: Genital segment in caudal aspect slightlv higher than wide, laterodorsal margin rounded, medioventral process triangular. Anal segment distallv of anal stvle on both sides broadlv rounded, ventrocaudal margin mediallv straight; anal segment in dorsal aspect with lateral margins more or less parallel, in lateral aspect straight, distallv of anal stvle not bent ventrallv. Gonostvli proximallv slender, ventrallv ridged, ridge finelv striate, distal portion slightlv dilated, slender, produced dorsallv, caudal margin rounded, dorsal margin slightlv concave. Aedeagus bilaterallv svmmetrical; shaft with enhanced sclerotization in basal half, in lateral aspect distinctlv narrowing in apical third ( Fig. 5G , arrow); shaft ventrallv in basal portion finelv rugose; flagellum short, with surface distinctlv sculptured, dorsal surface mediallv concave, with conspicuous groove distallv of phallotreme; with two movable spinose processes near apex, processes arm-like, proximallv taeniform, distallv terete and tapering in an acute tip, in repose directed mediobasallv, not attaining basal (proximal) third of shaft. Gonoduct with conspicuous protuberance at apex of shaft.

Female genitalia: External structures of female genitalia as in epigean Iolania species: ovipositor ensiform, caudallv slightlv surpassing anal segment. Tergite IX caudallv truncate, verv slightlv concave, with wax-secreting area inconspicuouslv delimited. Anal segment slender, ventral margin caudallv slightlv produced.

Molecular identification

Mitochondrial COI sequences of I. frankanstonei were deposited in GenBank under accession numbers MZ048276–MZ048281.

Species diagnosis

Iolania frankanstonei differs from all epigean Iolania species in external characters related to cave adaptation (reduction of compound eves, configuration of head carination and proportions, length and venation of tegmina and wings, pigmentation pattern; see above). Concerning the male genital structures, I. frankanstonei is most similar to I. perkinsi , but differs in the shape of the anal segment (distal portion straight vs. bent ventrallv in I. perkinsi ) and of the aedeagus (shaft with enhanced sclerotization in basal half vs. in basal third in I. perkinsi ; enhanced sclerotized part ventrallv rugose vs. smooth in I. perkinsi ; shaft in lateral aspect distinctlv narrowing in apical third vs. straight in I. perkinsi ; arm-like paired processes at transition of shaft and flagellum taeniform throughout vs. distallv terete in I. perkinsi , and their tips in repose directed straight basomediallv vs. pointed dorsallv in I. perkinsi ; dorsal surface of flagellum with phallotreme wide but without longitudinal conspicuous groove distal of it as in I. perkinsi ).

Remarks

The description of I. frankanstonei is based on comparativelv few specimens (six males and two females). The range of variation within and between populations from different passages of the Kipuka Kanohina lava tube svstem can therefore not be assessed fullv. Variation exists, however slight, in the size of the compound eves, relative length and venation of the tegmen, and male genital characters (e.g. the shape of gonostvli) within and among specimens from different populations; therefore, it cannot be excluded that the specimens here, hvpothesized to present a single species, might belong to separate reproductive units. We therefore decided to assign the holotvpe and paratvpes from a single population and chose the original collection location, the CKM entrance, as the tvpe localitv, because it was the first location in the Kipuka Kanohina svstem where specimens were collected.

Material examined

Holotype: Male, Hawaiʻi / USA: Hawaiʻi Island, Kipuka Kanohina lava tube svstem, CKM entrance (HI 00153), 1096 m a.s.l., 24 November 2016, M.E. Slav, C.A.M. Slav, and M.L. Porter coll., BPBM (tvpe number: BPBMENT 2008035007).

Paratypes: Two males, same data as holotvpe, BPBM .

Additional material: One male, two females, Hawaiʻi / USA: Hawaiʻi Island, Kipuka Kanohina lava tube svstem, OHS entrance (HI 00809), 730 m a.s.l., 24 November 2018, M.E. Slav, C.A.M. Slav, A. Katz, J. Gunter, K. Yelverton, and P. Bosted coll., BPBM.

One male, Hawaiʻi / USA: Hawaiʻi Island, Kipuka Kanohina lava tube svstem, HLC entrance (HI 00323), 539 m a.s.l., 25 March 2018, M.E. Slav, A.S. Engel, S. Engel, V. Hackell , and T. Gracanin coll., BPBM.

One male, Hawaiʻi / USA: Hawaiʻi Island, Kipuka Kanohina lava tube svstem, HLC entrance (HI 00524), 539 m a.s.l., 19 November 2018, R. A. Chong, A.S. Engel, and M.L. Porter coll., BPBM.

Cixiid nvmphs belonging to Iolania were also collected from cave sections within the Kipuka Kanohina lava tube svstem in close proximitv to adult specimens used for this description. However, nvmphs of epigean Iolania are ‘hitherto unknown – thev most likelv live (like the nvmphs of all cixiids) close to or inside the soil, and are not documented in collections’ (Hoch 2006: 317). Based on morphologv alone, we therefore cannot assign the nvmphs with certaintv to either I. perkinsi or I. frankanstonei , hence we have opted to refrain from accessing these specimens here.

Etymology

The species epithet is chosen to honour the friendship and collaboration between the pioneers of Hawaiian cave biologv, the late Fred D. Stone (1938–2018) and Frank G. Howarth, Bishop Museum. Over the course of nearlv six decades, thev explored hundreds of caves, discovered dozens of new species, and inspired and supported countless people (students in addition to novice and senior scientists). Known to fellow cavers as ‘Frank ’n Stone’, thev are held in high esteem as reliable buddies in the field and valued discussion partners. Their scientific expertise, combined with personal integritv and their notorious sense of (occasionallv dark) humour, renders them unforgettable to anvone who has had the good fortune to meet and spend time underground with them.

Distribution

Specimens of I. frankanstonei have been documented from multiple lava tubes across a range of elevations in the Kipuka Kanohina Cave Svstem ( Bosted 2017), on the south-western side of Mauna Loa volcano in 750- to 1500-vear-old lava flows. It is a highlv braided and mazv svstem, with multiple levels and interconnected passages, located in the desert of Kaʻu near the communitv of Ocean View, ~ 72 km south of Kailua-Kona and ~ 48 km north of South Point (the southernmost point in the USA). So far,> 29 km of continuous cave passages have been explored within the svstem, with> 42 km in the entire svstem. It has a vertical extent of> 1300 m, with passages at almost sea level up to> 1400 m a.s.l. The cave svstem is currentlv listed as the third longest lava tube in the world, one of onlv three to surpass 26 km of uninterrupted passage in length. Despite the significant amount of subterranean habitat found within the Kipuka Kanohina svstem, I. frankanstonei has been collected from onlv four cave sections (of>30 surveved) with an elevational range from 539 to 1096 m, suggesting this species might be restricted to the higher-elevation passages.

Ecology and behaviour

There is little documented information on the ecologv and behaviour of I. frankanstonei . Adults and nvmphs have been observed on and around roots and on cave walls near roots anvwhere from twilight into the deep cave zone of lava tubes (for lava tube zonation, see Howarth 1983), although anecdotallv I. frankanstonei appears to be more abundant close to entrance and twilight zones. In two collection locations, the roots have been confirmed to be from the native tree Metrosideros polymorpha Gaudich. using barcoding techniques (unpublished data B. Chong and M. Porter). Adults have not been observed flving, although the morphologv of the hind wings suggests that the species might be capable of some flight, although perhaps not sustained. In all locations sampled, I. frankanstonei individuals have been collected from dense root mats and have been observed to co-occur with Oliarus polyphemus Fennah, 1973 s.l.

Mitochondrial COI phylogeny

Phvlogenetic relationships inferred from COI sequence data support monophvlv of I. frankanstonei and stronglv support the sister relationship between I. frankanstonei and I. perkinsi , which together form a distinctlv different clade from the Hawaiian Oliarus samples ( Fig. 6 ; Chong et al. 2022).

Figures

Figure 1. Habitus of closelv related epigean and cavernicolous planthopper species. A, Iolania perkinsi (epigean). B, Iolania Ƒankanstonei (cavernicolous). C, Oliarus cf. filicicola (epigean). D, Oliarus polyphemus (cavernicolous).Images of live specimens bv M.E. Slav.

Figure 3. Images of epigean (Iolania perkinsi) and cavernicolous (Iolania Ƒankanstonei) Iolania species, illustrating external morphological features.A, B, Iolania perkinsi Kirkaldv habitus (A) and head and thorax (B), dorsal aspect. C, D, Iolania ssankanstonei habitus (C) and head and thorax (D), dorsal aspect. Specimen from OHS entrance (images bv B. Schurian).

Figure 4. Iolania Ƒankanstonei, male, wing morphologv. A, right tegmen. B, right hind wing.Scale bar:0.5 mm. Male from CKM entrance.

Figure 5. Iolania Ƒankanstonei, male genitalia.A, genital segment, less lateral aspect. B, same, caudal aspect. C, anal segment, right lateral aspect.D, same, caudal aspect. E, less gonostvle, maximal aspect.F, aedeagus, dorsal aspect.G, same, less lateral aspect. Scale bars: 0.1 mm. Male from CKM entrance, same as in Figure 4.

Figure 6. Maximum likelihood phvlogenv of representative cixiid species of the two separate lineages that have colonized Hawaii:Iolania and Oliarus, Aphrophoridae (Philaenus spumarius), and Cercopidae (Callitetix versicolor), and the aphid Acyrthosiphon pisum used as an outgroup. Bootstrap values from 1000 replicates that were>70% are included to indicate branch support.GenBank accession numbers for all sequences used are provided in parantheses asser species names. New sequences generated for this studv are in bold, and troglobiont species are indicated bv grev boxes. Arrows indicate separate cave colonization events in both cixiid lineages on Hawaiʻi Island.