The scarab beetle tribe Pentodontini (Coleoptera, Scarabaeidae, Dynastinae) is the largest tribe in the subfamily Dynastinae including over 500 species that are distributed in the world (Endrödi, 1985;Ratcliffe and Cave, 2015). Distribution of the genus Pentodon Hope, 1837 is restricted to the Palaearctic and Oriental regions and the genus comprises 14 species and 18 subspecies (Krell, 2016). Pentodon quadridens (Gebler, 1844) comprises 4 subspecies and Korean species is regarded as P. quadridens bidentulus by Endrödi’s geographic location map (Kim, 2001). One of European Pentodon species, the larvae of P. idiota is also known as an agricultural pest attacking on roots of sugarcane and maize (Gentry, 1965;Fora et al., 2013). Neotropical Pentodontini species also attack on crop roots such as sugarcane, rice, corn, and tobacco (Margarita et al., 2015).

The subfamily Dynastinae is one of the most popular groups in the family Scarabaeidae because of its charismatic appearance, and only three species are known from Korea, i.e., Trypoxylus dichotomus dichotomus, Eophileurus chinensis, and P. quadridens bidentulus (Kim, 2011). Unlike two former dynastine scarab beetles, there is significant lack of taxonomic and ecological information on P. quadridens bidentulus. Kim (1997) recorded P. quadridens (sensu lato) from Banwol area (Gyeonggi-do) for the first time in Korea. Additionally, Kim (2001) reported P. quadridens bidentulus from Seosan (Cungcheongnam-do) and Anmyeondo (Chungcheongnam-do) which are located in the west coast of Korea, but their life histories and immature stages are largely unknown. Since many P. quadridens bidentulus adults and larvae were collected from Sihwaho reclaimed land, we were able to describe the larva and the pupa of P. quadridens bidentulus for the first time. We also discussed biological notes, distribution, and life cycle of the species under natural habitats and the laboratory condition.

Materials and Methods

Hundreds of adults of P. quadridens bidentulus were collected by light-trap and larvae were discovered from the soil about 3-10 cm deep covered by cogongrass (Imperata cylindrica var. koenigii: Gramineae) which is a dominant species in Sihwaho reclaimed land with the average soil salinity (ECe) is 0.8 dS/m (Kim, 2013). Collected larvae were brought to the laboratory and reared in laboratory conditions (25-26℃) in separate small plastic cups filled with fermented oak sawdust and soil brought from their habitat.

Third instar larvae and pupae used for morphological studies were kept in the freezer for about 1 hour and dissected or after melting in cold water, photographed and examined. This method enabled the state of the specimen to be photographed in the same state as it was alive. Dissected parts were preserved in 90% ethanol and also kept in the freezer. External features were examined under the Leica MZ6 stereo microscope. Photographs were taken using a Canon EOS 5D Mark III and 1D X Mark II SLR digital cameras equipped with a Canon EF MP-E 65 mm f/2.8 1-5x Macro lens, a 100 mm f/2.8L Macro IS USM, and Mitutoyo M Plan Apo 10x with Canon auto bellows. Partially focused images of each specimen were combined using Zerene photo stacker software (Zerene system, USA).

The description is based on two second instar larvae, thirty-eight third instar larvae, and two pupae. Identification of the immature specimens was determined by association with adults in pupal cells. The terminology for larval description follows Ritcher (1966) and Ratcliffe and Skelley (2011). Specimens used in this study were deposited at the department of applied biology, Kangwon National University (Chuncheon, South Korea).

Pentodon quadridens bidentulus (Fairmaire, 1887)

Third instar

(Figs. 1-4)

Material examined. Thirty-eight third instar larvae with the following data: “Korea: Gyeonggi-do, Hwaseong-si, Songsanmyeon, 37°15'23.84''N, 126°44'44.83''E, 12-Oct-2016, Y. C. Jang, P. J. Cho.”

Description. Dorsal body length 29-45 mm (= 37 mm; SD = 4.0; n = 38), C-shaped, slightly thick and creamy-white, with numerous long setae. Cranium (Fig. 1A and B): Width of head capsule 6.1-7.8 mm (= 7.0; SD = 0.46 mm; n = 38). Color reddish-brown to brown. Surface moderately punctate on frons (F) with numerous long and minute yellowish setae, epicranium (E) less densely punctate. Postclypeus (PSC) and preclypeus (PC) rugose. Epicranial suture (ES) and frontal suture (FS) distinct well. Frons: Surface with 4 exterior frontal setae (EFS) and 2 posterior frontal setae (PFS) on each side and with 6 anterior frontal setae (AFS). Each anterior angle with 2 setae (AAS). Epicranium with 4-5 dorsoepicranial setae (DES), 46-50 epicranial hairs distributed irregularly. Five paraocellar setae (POS) on each side. Ocellus (O) absent. Clypeus: Trapezoidal with straight sides. Surface of postclypeus with 2 anterior clypeal setae (ACS) and 2 external clypeal setae (ECS) on each side. Labrum: Surface nearly symmetrical with rounded, not angulate, lateral margin, with 5 posterior labral setae (PLS) and 2 posterolateral labral setae (PLLS) on each side. Epipharynx (Fig. 1C): Asymmetrical, with left lateral margin slightly angulate in the middle. Haptomeral process (HP) notched forming 3 teeth. Right chaetoparia (RCPA) with 80-82 spine-like setae, left chaetoparia (LCPA) with 110-115 spine-like setae. Acroparia (ACR) with about 10 long, stout, slightly curved setae. Corypha (CO) with 15 long, thick setae. Acanthoparia (ACP) with 15 short, curved, spine-like setae on each side. Pedium (P) longer than wide and without setae. Dexiotorma (DX) sclerotized, slightly broad, and elongate. Laetorma (LT) shorter than dexiotorma. Pternotorma (PTT) sclerotized and rounded. Haptolachus (HL) with 8-10 short setae. Sclerotized plate (SP) on right nesium (RN) well developed. Sense cone (SC) on left nesium (LN) well-sclerotized, rounded. Crepis missing. Left mandible (Fig. 2A and D): Form falcate. Scissorial region with blade-like apical tooth (S₁ + S₂ fused), separated from S₃ by scissorial notch (SN). S₄ small, barely distinct. Scrobis (SCR) with about 20 long, thick setae. Acia (AC) well developed and acute, with 2 basolateral setae. Ventral surface with elongate-oval stridulatory area (STA) with about 36 narrowly separated, subparallel ridges. Molar lobe (ML) large, not subdivided with a tuft of 7-8 ventral molar setae (VMS). Preartis (PA) distinct, concave. Ventral process (VP) large. Brustia (BR) with about 6 long setae. Postartis (PTA) large, spherical. Right mandible (Fig. 2B and C): Form falcate Scissorial region with blade-like apical tooth (S₁ + S₂ fused), separated from S₃ by scissorial notch (SN). S₄ absent. Scrobis (SCR) with about 19 long, thick setae. Dorsal surface with 2 long setae line of scissorial notch (SN). Preartis (PA) distinct, concave. Ventral surface with elongate-oval stridulatory area (STA) with about 34 narrowly separated, subparallel ridges. Ventral process (VP) well-developed, broadly rounded. Brustia (BR) with 5 a tuft of 5 long setae. Calx (CA) large, with 6 basolateral setae (BLS). Molar area with a tuft of 6 ventral molar setae (VMS). Molar crown with 3 distinct blunt lobes (M_1-3). Postartis (PTA) large, spherical. Maxilla and labium (ventral view, Fig. 3A): Galea (GA) and lacinia (LAC) fused, forming mala (MA). Mala with 4 sclerotized unci (UN) at apex and about 20 strong, long setae. Maxillary palpus (MP) 4-segmented; apical segment long and spindle-shaped; 2nd segment with 2 long setae; 3rd segment curved at apex almost same length as apical segment; basal segment twice shorter then 3rd segment. Mentum subdivided into 3 sclerites: postmentum (PMP) with 4 setae on each side and prementum (PM_1-2). Labial palpus (LP) with 2 segments, spindle-shaped apical segment almost same length as basal segment. Maxilla and labium (dorsal view, Fig. 3B): Stridulatory area of left maxilla with row of 10 stridulatory teeth (SD), stridulatory area of right maxilla with row of 7 teeth, teeth becoming increasingly smaller basally. Glossa (GL) with 36 short and 50 long setae. Hypoopharyngeal sclerome (HSC) asymmetrical, right side with tooth-like process produced dorsally; apex of left side elevated and protruded. Lateral lobes (LL) with about 16 long setae each. Antenna (Fig. 4B): Antenna (A) 5-segmented, basal segments thicker than others, apical segment on dorsal surface with one large dorsal sensory spot (DSS). Segments 2 and 4 subequal in length, each slightly shorter than 3rd segment; terminal segment about half length of segment 2. Thorax (Fig. 4D): Prothoracic spiracle about 0.6-0.7 mm long, 0.5-0.6 mm wide; respiratory plate light brown, ovally C-shaped, spiracular bulla rounded, slightly elevated; respiratory plate with about 37 holes across diameter at middle. Dorsum of pronotum and prescutum segments II and III each with transverse row of long slender setae. Legs (Fig. 4A and D): Tarsal claws falcate, posterior tarsal claws shorter than protarsal and middle tarsal claws. Coxa, trochanter, femur, and tibiotarsus of all legs transparent and creamy-yellow with numerous long, stout setae. Abdomen (Fig. 4D): Abdominal spiracles subequal in size with prothoracic spiracle except last small one. All abdominal spiracles subequal in size. Abdominal tergites I-VII with many tiny, short, spine-like setae. Raster (Fig. 4C): Surface without palidia. Campus (C) with 8 setae. Teges (T) with over 100 short, spine-like setae. Anal slit (ASL) transverse.

Remarks. Second instar larva is similar as third instar larva except maximum width of head capsule 3.7-4.0 mm. Larvae of P. quadridens bidentulus can be easily distinguished from those of all other known Korean Dynastinae by the following characteristics: Head reddish-brown to brown, rugose, slightly punctate with many hairs; antenna with one large dorsal sensory spot at first segment (Fig. 1A and B, Fig. 4B, Fig. 5A and B).

Pentodon quadridens bidentulus (Fairmaire, 1887)

Pupae

(Fig. 6)

Material examined. One male pupa reared from third instar larva with the following data: “Korea: Gyeonggi-do, Hwaseong- si, Songsan-myeon, 37°15'23.84''N, 126°44'44.83''E, 12-Oct-2016, Y. C. Jang, P. J. Cho.” One female pupa reared from eggs laid by females with following data: “Same locality, 02-Aug-2017, Y. C. Jang.”

Description. Male pupa (Fig. 6A-D). Length 24.7 mm; greatest width 13.1 mm. Body elongate, oval, stout, smooth, apparently glabrous but covered with short micro pubescence. Color yellowish brown. Head: Bent downward, vertex dorsally visible. Mandibles, maxillary and labial palpi tubercle-like. Mandibular thecae triangular expanded ventrally, antennal thecae largely expended, stout, ear-shaped. Thorax: Pronotum trapezoid, lateral margin rounded. Pronotal spiracle placed between anterior and medial legs; almost hidden by pronotal thecae and elytral thecae. Mesonotum and metanotum well differentiated. Scutellum inverted triangular-shaped, reached half of metanotum. Elytral and posterior wing thecae closely appressed, turned downward and partially cover hind legs; elytral thecae extending to middle of abdominal segment III; posterior wing thecae extending to middle of abdominal segment IV. Protibia with 3 distinct teeth on external edge. Mesotibia and metatibia with 2 swellings at apices; characters indicative to spines seen in adults (Fig. 7A and B); the external swelling short, blunt; the inner swelling twice as long as the external swelling. Abdomen: Segment I concealed ventrally and revealed dorsally. Dioneiform organs (DO) present between segments I-II, II-III, III-IV, IV-V, VI-VII, and VII-VIII. Tergite IX with large ventral lobes with tuft of thin, short setae. Spiracle I-IV ovate, prominent with dark-brown scleroma, I covered by wing thecae, spiracles V-VIII conspicuous but closed compared to I-IV. Sternite IX smaller than others, with genital ampulla. Genital ampulla (Fig. 6D) sub-trapezoidal, genitalia with basal notch. Urogomphi absent.

Female pupa (Fig. 6E). Length 26.1 mm; greatest width 14.2 mm. Same with male, except following characteristics: Ventral tergite IX not concave at middle as male. Sternite IX anteriorly convex in males, but not in females with genital pore with “W” shaped. Genital ampulla subtrapezoidal in shape.

Life history and biology (Fig. 8A-F)

Pentodon quadridens bidentulus can be found in a very restricted area located in the reclaimed land and the seaside. The habitat, Sihwaho reclaimed land, is located near an artificial lake created by the seawall and all other localities where they have been collected are located on the west coast of the Korean peninsula. The females lay eggs in the soil near the root of cogongrass (depth: 5-10 cm). Larvae were always found under its roots in the field between July and October.

Cogongrass is regarded as a serious invasive pest in the United States, and it was escaped from packing materials and a livestock forage grass from Japan and the Philippines in the early 1900s. Some stemborers (Lepidoptera and Diptera species) have been used for biological controls of cogongrass, however attempt to use root attackers in cogongrass control program has not been made so far (Overholt et al., 2016). Although larvae of Leucothyreus albopilosus, one of the scarab species known as a serious pest in oil palm plantations, were found on the roots of cogongrass, their impact on cogongrass was not known (Martinez et al., 2013).

Larvae of P. quadridens bidentulus are saprophagous mainly fed on humus in the soil similar to other dynastine scarab beetles (Ratcliffe and Cave, 2015). However, in this study, we report that they also feed on cogongrass roots based on our observation in the field and the laboratory condition. Root feeding habits of the larvae of P. quadridens bidentulus are similar to Melolonthinae and Rutelinae, but it is rare in Dynastinae (Ritcher, 1958). It is known that only members of Pentodontini and Cyclocephalini among Dynastinae feed on plant roots (Ratcliffe and Cave, 2015). Like larvae of Melolonthinae and Rutelinae species, larvae of P. quadridens bidentulus also move well and hold cogongrass roots using their legs, in which no observation has been made among other dynastine species. Since all immature stages of larvae and adults were found in the mid October 2016, it seems that they can hibernate at all stages except eggs and pupae in winter. To hibernate, the larvae dig the soil down around 30 cm underground in the winter (observed on 17 Dec. 2017).

Adults are probably nocturnal, but no adults except dead ones were collected at night until we turned on light for collecting. Adult emergence occurs from June to August (Kim, 2001) and according to our observation, the peak of occurrence is in the middle of July to early August. When light was turned off at night, they burrow into the soil quickly. It is largely unknown what adults feed on in the field but they feed on insect jelly including protein very well in laboratory conditions.

Breeding condition (25-26℃): The larvae hatched about 10-14 days after oviposition. The first instar took about two weeks, the second instar about 3-4 weeks and the third instar 8-10 weeks. Pupating occurred in a pupating cell near the side of the plastic cup. The pupal period lasted about 2 weeks before eclosion. After the eclosion, the color of the adult was reddish brown and some adults remained in for months. But when they started to move and ate the food, the body color turned black.

Adults were kept in laboratory conditions (25-26℃) in 20 liter plastic containers, filled with about 15 cm layer of the substrate, composed of soil and grasses which were brought from their natural habitats. Commercial insect jellies including sugar and protein were supplied for breeding adults. Three months later, twenty larvae were found in one of several breeding containers and reared separately in small plastic cups, filled with fermented oak sawdust and soil brought from their natural habitats with cogongrass roots. However, the growth rate of the larvae was very poor and only two larvae were survived and became adults. Contrary to the larvae hatched from the laboratory, almost all 1st-3rd instar larvae collected from the field and reared in same condition in the laboratory became adults.