Philippine Journal of Science 149 (3): 571-579, September 2020 ISSN 0031 - 7683 Date Received: 15 Apr 2020

Morphology and Morphometrics of Diotarus verrucifer (Stål, 1877), a Pygmy Grasshopper Endemic to Mindanao

Alma B. Mohagan1,2, Romeo R. Patano Jr.1,2*, Emmanuel P. Leaño1,2, Merced G. Melencion1,2, Fulgent P. Coritico1,2, and Victor B. Amoroso1,2

1Center for Biodiversity Research and Extension in Mindanao 2Department of Biology, College of Arts and Sciences Central Mindanao University, Musuan, Maramag, Bukidnon 8710 Philippines

Diotarus Stål, 1887 (: Cladonotinae) is a genus of pygmy grasshoppers with four species, all of which are inhabiting the Philippines with one species known also from Sulawesi. Diotarus verrucifer Stål, 1877 was originally described from Semper’s collection and from an unknown location from the Philippines. The species has been reported once since the description by Gůnther in 1938. In this study, we report species diagnostic characteristics and describe its natural habitat. The brief morphological description and, more importantly, the updated distribution map are firsts for this species. The species is similar to Diotarus galeatus and is still not clear if they represent separate species. We present detailed measurements of our specimens in order to make comparison in the future possible.

Keywords: Diotarus verrucifer, groundhopper, Marilog District, measurements, Mt. Agad-agad, pronotum, tectiform

INTRODUCTION the head (Tumbrinck 2014). Those species have crested, tectiform pronotum with truncated apex, giving the The genus Diotarus Stål, 1877 belongs to the family a leaf-like pattern. This is only one of the genera Tetrigidae and subfamily Cladonotinae. Members of this with leaf-like mimicry (Skejo et al. 2019). The holotype family are characterized mainly by having filiform or originated from the Semper’s collection, and most of thicker antennae, and the medial ocellus is situated below the grasshoppers’ material lack detailed locality data the lower margin of the eyes. The dorsal margin of the (Stål 1877; Bolívar 1887; Tumbrinck and Skejo 2017; anterior and middle femora has a well-developed carina, Muhammad et al. 2018). with the facial carina of the frontal costa considerably widened in which they enclose a widened scutellum Based on Semper’s collections as shown by Tumbrinck (wider than the scapus) (Tumbrinck 2014). However, (2014), except for D. verrucifer, some specimens of the subfamily seems not to be monophyletic (Tumbrinck species from the genus Diotarus were collected in Luzon – 2014; Skejo et al. 2019). The genus includes four species, specifically from Norzagaray, Bulacan and Mount Bulusan three of which are endemic in the country while Diotarus in Sorsogon (D. galeatus) – while other species were pupus is also known from Sulawesi. The genus Diotarus collected in Camarines Sur (D. pupus) and Los Baños, is unique through its pronotum by having semicircular to Laguna (D. ikonnikovi). truncated apex and elevated anterior margin in relation to New distribution records and habitat of D. verrucifer are *Corresponding Author: [email protected] described in this paper. We aim to provide its morphological

571 Philippine Journal of Science Mohagan et al.: Morphology and Morphometrics of Vol. 149 No. 3, September 2020 Diotarus verrucifer description, as we have observed a lack of actual images in – number of outer spine on hind tibia; 1stTL – first tarsal its natural environment online or in literature. The specific segment (basal) length; 3rdTL – third tarsal segment localities on which this species can be found were also (apical) length (without claws); SGPL – subgenital illustrated. We provide habitat description with supporting plate length; SGPW – subgenital plate width; OVDL – images. This study provides new pygmy grasshoppers ovipositor dorsal valve length; OVDW – ovipositor dorsal records from the area in which we recently recorded valve width (maximum, including denticle); OVVL – Spartolus pugionatus (Mohagan et al. 2020). ovipositor ventral valve length; and OVVW – ovipositor ventral valve width (maximum, including denticle). All measurements are shown in millimeters. All of the MATERIALS AND METHODS collected specimens examined in the study were mounted and then deposited to the Central Mindanao University, University Museum, Zoological Section, Tetrigidae Entry Protocol and Permits Collection. Necessary permits such as an approved gratuitous permit (GP) from the Department of Environment and Natural Studied area. The study was conducted in Mt. Agad-agad, Resources, in compliance with the Philippine Republic Sitio Langinlanon, Barangay Pugaan, Iligan City, Lanao Act No. 9147 for the collection of the specimens, and del Norte and Marilog District, Davao City Philippines – the Institutional Animal Care and Use Committee permit as shown in Figure 1 and are listed in Table 1. Other than for animal handling were obtained prior to the conduct these localities, there are no other georeferenced localities of the research project. for this species. We give approximate coordinates for Davao and Zamboanga, the localities for which Günther reported this species. Table 1 shows all the known Photography and Measurements (published) localities together with their accompanying Documentation of the specimens was conducted using a references, as well as new localities present in this study. Canon™ digital single-lens reflex camera with the use of a stereomicroscope. Small body parts such as the antennae were measured using an ocular micrometer. The studies of Skejo and Berner (2017), Tan and Artchawakom (2015), RESULTS AND DISCUSSION Tumbrinck and Skejo (2017), and Muhammad et al. (2018) were used as guides for the measurements. The following measurements were taken: Family Tetrigidae Rambur, 1838 Subfamily Cladonotinae Bolívar, 1887 BL – body length (length from vertex of head to apical Genus Diotarus Stål, 1877 margin of subgenital plate); PL – pronotum length (from the anterior margin (FM included if present) to the tip); Species included: Diotarus galeatus Bolívar, 1887, PW – pronotum lobe width (in its widest part); PH – endemic to Luzon (Angat and Norzagaray); Diotarus pronotum height (from the lowest part of the lateral lobes ikonnikovi Bey-Bienko, 1935, also endemic to Luzon to the highest part of dorsum); FFL – fore femur length; (Los Baños); Diotarus pupus Bolívar, 1887, known from FFW – fore femur width (in the middle); MFL – mid the Philippines and with records from Sulawesi that need femur length; MFW – mid femur width (in the middle); to be checked. HFL – hind femur length (from the base to the tip of the Species verrucifer Stål, 1877 by original monotypy. knee); HFW – hind femur width (in its widest parts); VW – vertex width; EW – compound eye width (in Type locality: Philippines, no specified type locality in frontal view between the eyes, or in dorsal view between Semper’s collection. the place of the supraocular lobes); SW – scutellum (or Distribution: Philippines. Mindanao: Lanao del Norte: frontal ridge) width (between the facial carinae); and IAH Iligan City (new locality record); Davao Region: Marilog – infrascapular area height (in its highest part). District (new locality record) The following measurements were also made: Material examined in this study. Philippines, Mindanao MAL – middle segment of antenna length (7th or 8th Island, Lanao del Norte, Iligan City, 08°27’31.30”N, segment); MAW – middle segment of antenna width (7th 125°35’43.20”E; 325 masl, 24-ii-2020, 1 male and 2 or 8th segment); 1stAW – first antennal segment width females, coll. A.B. Mohagan, R.R. Patano, F.P. Coritico, (in the middle of the segment) or the scapus width; HTL and V.B. Amoroso [repository (CMU-UM)]; 1 male and – hind tibia length (from knee to base of apical spine); 5 females, same locality: Davao del Sur: Davao City, n(HTIS) – number of inner spine on hind tibia; n(HTOS) Marilog District, Marilog Forest Reserve, 07°27’13.74”N,

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Figure 1. Map of the Philippines (A) and Mindanao (B) showing the distribution of Diotarus verrucifer Stal, 1877. The study was conducted from months of February 2018 to February 2020. Localities are shown in Figure 1 and in Table 1.

Table 1. Localities in from which Diotarus verrucifer is known, together with information on coordinates, elevation, date of research, and reference for each. Locality Coordinates Elevation Date Reference Unknown region, Philippines Unknown Unknown 1887 Stål 1877 Mindanao: Davao* 07°11’26.55”N, Unknown 1938 Günther 1938 125°27’19.23”E Mindanao: Zamboanga* 06°55’17.19”N, Unknown 1938 Günther 1938 122°04’44.45”E Mt. Agad-agad, Sitio Langinlanon, Barangay 08°27’31.30”N, 216–420 masl February 2020 Present study Pugaan, Iligan City, Lanao del Norte 125°35’43.20”E Lawi-lawi Forest Reserve, Sitio Maharlika and 07°27’13.74”N, 1220–1240 masl February 2018 – July Present study Sitio Calinan, Barangay Baganihan 125°15’1.12”E 2019 Mt. Malambo, Barangay Datu Salumay 07°29’87”N, 1,151–1,178 February 2018 – July Present study 125°15’22.23”E masl 2019 Lola Mommy’s Rainforest, Sitio Epol, Barangay 07°27’19.73”N, 1,197–1,345 February 2018 – July Present study Baganihan 125°14’33.37”E masl 2019 Mt. Ulahingan, Sitio Tagumpay, Barangay Datu 07°28’29.89”N, 1,280–1,320 February 2018 – July Present study Salumay 125°16’36.77”E masl 2019 *Günther’s records were identified with uncertainty, but they likely belong to D. verrucifer, as D. galeatus seems to endemic to Luzon Island.

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125°15’1.12”E, 1,171 masl, 18-ii-2020, coll. A.B. morphology is very similar, if not the same between the Mohagan, R.R. Patano Jr., E.P. Leaňo, M.G. Melencion, two. D. verrucifer has a somewhat stouter pronotum, and and V.B. Amoroso [repository (CMU-UM)]. the general outline is a bit different. D. galeatus has more uneven pronotum, and the coloration is different – for Diagnosis. The species can be easily distinguished from example, the carina is striped. the other three species of the genus Diotarus by the shape of the pronotum (Figure 2). Diotarus ikonnikovi and Diotarus pupus both have smooth pronotum, Updated Description of Diotarus verrucifer Based on while Diotarus galeatus and D. verrucifer have warty. Mindanao Specimens D. verrucifer is the most similar to D. galeatus from (nine specimens altogether: two males, seven females) Luzon Island. The two species probably had the same Head. Head situated at the bottom of the anterior apex ancestor and represent geographical varieties of it. Head of the tectiform pronotum in the lateral view. Vertex,

Figure 2. Diotarus verrucifer Stål, 1877 female: (A) dorsal view, (B) lateral view, and (C) ventral view. Scale bar: 10 mm.

574 Philippine Journal of Science Mohagan et al.: Morphology and Morphometrics of Vol. 149 No. 3, September 2020 Diotarus verrucifer seen from above, has a blunt or clearly rounded process Antennae. Antennae are filiform and thicker. Antennal produced before the eyes. Facial carinae of the frontal grooves are situated just next to the lower margins of costa are considerably widened and are enclosing the compound eye. Antennae have 15 segments in males a broadened scutellum (broader than the scapus). and 16 in females: 1st scape, 2nd pedicel, and 3rd and 4th Supraocular lobes are absent (dorsal view). Vertex is basal segment (which is almost of the same size with the almost twice as wide as a compound eye (dorsal view). first segment) are present; 5th–9th central segments are Lateral ocelli are situated in the lower third of the much longer and thicker than the 1st segment; 10th–12th compound eyes height. Frontal costa are not strongly apical segments are almost of the same size with the projected in lateral view. Scutellum is wide, which is central segments in which the last segment (14th, or 15th almost 1 mm (Table 2). Scape is considerably narrower in females) is reduced and pointed in shape (Figure 3). than scutellum. Compound eyes are also touching the anterior margin of pronotum, while the occipital area is Pronotum. Dorsum of pronotum is granulated and rough; narrow (Figure 3). it exhibits variable coloration from black to pale yellow; it is always with strong median carina. It ranges 14.0–14.6

Table 2. Measurements (in mm) and counts of Diotarus verrucifer Stål, 1877. All the measurements are in millimeters. Body Females Males Average Average parameters female male BL 15.3 15.8 14.8 14.6 15.4 14.8 15.3 14.1 13.7 15.14 13.9 PL 14.6 14.5 14.3 14.2 14.4 14.2 14 13 12.6 14.31 12.8 PW 6.1 6 5.8 5.6 6.1 5.8 6 5.5 5.2 5.91 5.35 PH 6.1 6 5.7 5.5 5.6 5.6 5.55 5.1 4.6 5.72 4.85 HFL 7.4 7 7.2 7.2 7.1 7 7.2 7 6.6 7.16 6.8 HFW 3.7 3.7 3.65 3.5 3.45 3.55 3.5 3.2 3 3.58 3.1 VW 2.5 2.6 2.5 2.4 2.4 2.5 2.5 2.1 2.2 2.49 2.15 EW 1.2 1.2 1.1 1.1 1.2 1.2 1.15 1.1 1.1 1.16 1.1 SW 1 1 0.9 1.1 1 1 1.1 0.9 0.8 1.01 0.85 IAH 2.5 2.5 2.4 2.5 2.45 2.5 2.4 2.1 2 2.46 2.05 MAL 0.28 0.3 0.29 0.28 0.29 0.29 2.29 0.21 0.18 0.57 0.195 MAW 0.11 0.14 0.13 0.11 0.11 0.14 0.15 0.09 0.09 0.13 0.09 1ST AW 0.09 0.1 0.09 0.09 0.09 0.09 0.1 0.08 0.07 0.09 0.08 FFL 4.6 4.6 4.6 4.5 4.5 4.6 4.5 4.2 4.1 4.56 4.15 FFW 1.1 1.2 1.1 1.1 1.1 1.2 1.1 1.1 0.7 1.13 0.9 MFL 4.5 4.6 4.4 4.4 4.4 4.5 4.45 4.2 3.2 4.46 3.7 MFW 1.4 1.45 1.3 1.4 1.3 1.4 1.2 1.2 1 1.35 1.1 HTL 7.4 7.4 7.2 7.2 7.3 7.45 7.3 6.6 4.8 7.32 5.7 n(THIS)R 5 5 5 5 5 5 5 5 5 5.00 5 n(THIS)L 5 5 5 5 5 5 5 5 5 5.00 5 n(THOS)R 0 0 0 0 0 0 0 0 0 0 0 n(THOS)L 0 0 0 0 0 0 0 0 0 0 0 1ST TL 1.5 1.6 1.5 1.45 1.4 1.55 1.4 1.2 1.1 1.49 1.15 3rd TL 1.1 1.15 1.1 1.1 1 1.1 1 0.9 0.8 1.08 0.85 SGPL 0 0 0 0 0 0 0 1 0.9 0.00 0.95 SGPW 0 0 0 0 0 0 0 0.9 0.8 0.00 0.85 OVDL 2 2.1 2 1.9 2 1.9 2 0 0 1.99 0 OVDW 0.7 0.8 0.8 0.8 0.75 0.75 0.8 0 0 0.77 0 OVVL 1.8 1.8 1.8 1.9 1.8 1.8 1.8 0 0 1.81 0 OVVW 0.6 0.7 0.7 0.6 0.6 0.65 0.7 0 0 0.65 0

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Figure 3. Diotarus verrucifer morphology: (A) antenna, (B) head in dorsal view, (C) head in frontal view, and (D) head and paranota in lateral view. Scale bars: 2.4 mm. mm in length and 5.6–6.1 mm in width for females (Table Legs. Dorsal margin of the anterior and middle femora 2). Pronotum is elevated in the anterior part, humpy, and has an evident carina. Legs are variable in color, from with one or more short, upper multi-peaked ridges on black to pale yellow. Dorsal margin of fore femora has the median carina, or irregular elevations. Median carina three strong undulations, both on the dorsal and ventral descends towards the pronotal apex – the process is on margins. Dorsal and ventral margins of mid femora a lower level than the anterior part. Pronotum covers are straight or bearing weak undulations. All the tibiae almost the entire abdomen but sometimes not the tip of bear spines in the distal parts (Figure 5). Hind femora the abdominal apex and not surpassing the hind femora. are about twice as long as wide. External outer area Anterior margin is projected forwards. Median carina is has transverse dark-colored ridges. Genicular teeth and continuous and more elevated in the anterior part than in antigenicular teeth are small and blunt. Hind tibiae are the posterior. Extralateral carinae are strong, composed of variable in color, from black to yellow. Fore, mid and tubercles. Interhumeral carinae are absent. Humeroapical hind tarsi are black to yellow in color. Middle segments carinae fuses with external lateral carinae obtuse, forming are much longer compared to 1st and 3rd segments of the a right angle. Humeral angles are absent. Paranota has no fore, mid, and hind tarsi (Table 2). Pulvilli of the hind spine-like projections along its length (Figure 4). tarsi rounded to slightly right-angled, but not sharp or angulate (Figure 5). Wings. Wings are absent, as it is a flightless species. Local name. There are no known local names reported Abdomen. The abdomen is colored black to yellow with on this species according to the local people in Marilog a spine-like subgenital plate (in females). The width of District, Davao City and Pugaan, Iligan City, Lanao del each of the 8 abdominal segment segments is about 0.85 Norte, Philippines. With that, we propose English name mm (Figure 4). “Mindanao helmed pygmy grasshopper”. “Helmed”

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Figure 4. Pronotum and abdominal morphology of Diotarus verrucifer Stål, 1877 female: (A) dorsal view and (B) lateral view. Scale bar: 10 mm.

Figure 5. Leg morphology of Diotarus verrucifer Stål, 1877: foreleg (A – outside, and B – inside), middle leg (C – outside, and D – inside), and hind leg (E – outside, and F – inside). Scale bar: 7 mm.

577 Philippine Journal of Science Mohagan et al.: Morphology and Morphometrics of Vol. 149 No. 3, September 2020 Diotarus verrucifer refers to their anterior margin of pronotum that looks and Caballero 2016) and Spartolus pugionatus Stål, 1877 like a helmet, while “Mindanao” refers to the island the while two individuals were just observed in forest patch of species is inhabiting. Mt. Agad-agad. Marilog District is mostly composed of a montane forest with an elevation of 1,151–1,345 m, while Habitat and ecology. D. verrucifer was observed perching Mt. Agad-agad is can be considered as an agroforest as it in ferns and shrubs in the forest patches Marilog District, is composed of forest patches (Figure 7). Altogether, nine Davao City, together with Arulenus miae Skejo et individuals (two males and seven females) were examined Caballero, 2016 or the Mia’s pygmy devil and Spartolus in the present study, but much more were observed in the pugionatus Stål, 1877 or the Mindanao yellow striped field (approximately more than 40). giraffehopper (Figure 6). In Mt. Agad-agad, Pugaan, Iligan City, Lanao del Norte Philippines, they are mostly observed Variability. Variability of Diotarus verrucifer can be in leaf litters. Both areas are considered secondary forests noted on four morphological characters mostly observed and some are agroforest areas, with remnants of loggings in the pronotum – (1) purely black to pale yellow in color and other anthropogenic disturbances such as agricultural throughout the body; (2) having tectiform pronotum in activities. The species was observed mostly in dense which its anterior part is extending above the head with forest patches in Marilog District, which means it prefers a truncated apex, or more flat pronotum; (3) pronotum untouched rainforest habitats, just as Arulenus miae (Skejo with a leaf-like pattern in the middle down to the apex,

Figure 6. Diotarus verrucifer Stål, 1877 (A and B) in its natural habitat perching on shrubs and ferns.

Figure 7. Habitat of Diotarus verrucifer Stål, 1877: (A) view on Mt. Agad-agad (216–420 masl) and (C) view on Mt. Malambo (1,151–1,345 masl); habitat of the species in agroforest of (B) Mt. Agad-agad and (D) montane forest in Marilog District.

578 Philippine Journal of Science Mohagan et al.: Morphology and Morphometrics of Vol. 149 No. 3, September 2020 Diotarus verrucifer which is formed by three rows or ridges in the pronotal MUHAMMAD AA, TAN MK, ABDULLAH NA, AZI- process; and (4) having various undulations on fore and RUN MS, BHASKAR D, SKEJO J. 2018. An anno- mid femora with a rough like textures. tated catalogue of the pygmy grasshoppers of the tribe Scelimenini Bolívar, 1887 (: Tetrigidae) with two new Scelimena species from the Malay Pen- insula and Sumatra. Zootaxa 4485(1): 1–75. ACKNOWLEDGMENTS SKEJO J, BERNER P. 2017. No More Dust and Exo- This study would not be possible without the help of skeletons—in Vivo Photographic Records Provide the Commission on Higher Education, as the funding New Data on Eufalconius pendleburyi Günther, 1938 agency of our research in Marilog District, as part of (Orthoptera: Tetrigidae) from the Titiwangsa Mts. An- DARE TO (Discovery-Applied Research and Extension nales Zoologici 67(4): 665–673. for Trans/Interdisciplinary Opportunities) program SKEJO J, CABALLERO JHS. 2016. A hidden Pygmy entitled “Saving Terrestrial Biodiversity: Inventory, Devil from the Philippines: Arulenus miae sp. nov.—a Assessment, Conservation and Capability Building in new species serendipitously discovered in an amateur Marilog Forest Reserve, Southern Mindanao, Philippines” Facebook post (Tetrigidae: Discotettiginae). Zootaxa and to the National Research Council of the Philippines 4067(3): 383–393. for also funding our research in Mt. Agad-agad entitled “Biodiversity, Inventory, Assessment and Conservation SKEJO J, GUPTA SK, CHANDRA K, PANHWAR for Ecotourism Development in Mt. Agad-agad, Lanao del WA, FRANJEVIĊ D. 2019. Oriental macropterous Norte”; to the MAMATRIPCEDI (Matigsalug-Manobo leaf-mimic pygmy grasshoppers-genera Oxyphyllum Tribal People Council of Elders Davao Inc.) of Marilog and Paraphyllum (Orthoptera: Tetrigidae) and their District; to the local researchers and also to stakeholders taxonomic assignment. Zootaxa 4590(5): 549. for collaboration; to the Department of Environment and STÅL C. 1877. Orthoptera nova ex Insulis Philippinis Natural Resources for the issuance of the GP; and to the descripsit. Öfversigt af Kongliga Vetenskaps-Akade- College of Veterinary Medicine of Central Mindanao miens Förhandlinger 34(10): 33–58. University, Musuan, Bukidnon for the issuance of IACUC permit. The research was also not possible without the TAN MK, ARTCHAWAKOM T. 2015. A new species valuable help of our University President Dr. Jesus from the genus Gorochovitettix (Tetrigidae: Metro- Antonio G. Derije in implementing our research. Finally, dorinae) from Thailand. Zootaxa 3990(3): 444–450. the authors would like also to thank and acknowledge TUMBRINCK J. 2014. Taxonomic revision of the Cla- Josip Skejo for the identification of the specimens and for donotinae (Orthoptera: Tetrigidae) from the islands sharing his knowledge on pygmy grasshoppers. of South-East Asia and from Australia, with general remarks to the classification and morphology of the Tetrigidae and descriptions of new genera and species from New Guinea and New Caledonia. Biodiversity, REFERENCES Biogeography and Nature Conservation in Wallacea BOLÍVAR I. 1887. Essai sur les Acridiens de la tribu des and New Guinea 2: 345–396. Tettigidae. Annales de la Sociét Entomologique de TUMBRINCK J, SKEJO J. 2017. Taxonomic and biogeo- Belgique 31: 175– 313, pls. 4–5. graphic revision of the New Guinean genus Ophiotettix GÜNTHER K. 1938. Revision der Acrydiinae: I sec- Walker, 1871 (Tetrigidae: Metrodorinae: Ophiotettigini tions Tripetalocerae, Discotettigiae, Lophotettigiae, trib. nov.), with the descriptions of 33 new species. Cleastratae, Bufonidae, Cladonotae, Scelimenae verae. Biodiversity, Biogeography and Nature Conservation Mitt Zool Mus Berlin 23: 299–437. in Wallacea and New Guinea 3: 525–580, pls. 104–124. MOHAGAN AB, LEAŃO EP, MELENCION MG, PA- TANO JR. RP, HONGCO AL, AMOROSO VB. 2020. Yellow Striped Giraffehopper Spartolus pugionatus Stål, 1877 comb. resurr. (Tetrigidae: Ophiotettegini) inhabits Mindanao Island of the Philippines’ archi- pelago. Zootaxa 4722(6): 591–600.

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