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Turkish Journal of Zoology Turk J Zool(2015) 39: 1034-1040© TÜBİTAKdoi:10.3906/zoo-1401-17

Taxonomic study of subfamily Scymninae (Coleoptera: Coccinellidae)with one new record from Gilgit-Baltistan, Pakistan

Muhammad ASHFAQUE1,*, Farman ULLAH2, Muhammad Ather RAFI1, Falak NAZ1

1Department of Plant and Environmental Protection, National Agricultural Research Center, Islamabad, Pakistan2Department of Plant Protection, University of Agriculture, Peshawar, Pakistan

* Correspondence: mashfaque@gmail.com

1. IntroductionCoccinellid beetles (Coccinellidae: Coleoptera), commonly known as ladybirds, lady beetles, or ladybugs, are among the best-known beneficial predatory insects. Many works recognize 6 subfamilies within this family, including Chilocorinae, Coccinellinae, Coccidulinae, Scymninae, Sticholotidinae, and Epilachininae. Of these, only one subfamily (Epilachininae) is phytophagous; the rest are predacious in nature. Vandenberg (2000) provided a list of 6000 species in 370 genera of Coccinellidae worldwide, while Ślipiński (2007) reported 6000 species in 490 genera. They are of economic importance due to their predatory activity against soft-bodied insects like aphids, jassids, psyllids, whiteflies, scale insects, and mealy bugs. They also prey on small larvae, insect eggs, and phytophagous mites, which are injurious to agricultural and forest plantations. Predation by adults and larvae of the coccinellid beetles can have a major impact on populations of immature stages of these insects (Rafi et al., 2005).

Although subfamilies of the Coccinellidae are more or less worldwide in distribution, many species within these subfamilies are restricted to particular biogeographical regions. The Indo-Pakistan subcontinent is known to have over 300 species of Coccinellidae (Rahatullah et al., 2011).

Initial documentation of predatory coccinellids of Pakistan was done by Irshad (2001, 2003) and Irshad and Khan (2005). Details regarding predatory coccinellid

species from Pakistan and current knowledge on the predatory coccinellid beetles of Gilgit-Baltistan are mainly based on the work of Rafi et al. (2005). In this compilation, only 9 species of predatory coccinellids belonging to 3 subfamilies were listed from this area.

Some members of the subfamily Scymninae are predacious on tetranychid mites and are known as acriphages, while others feed on scale insects and are known as coccidophages. The subfamily is distributed worldwide. Fürsch (1996) reported 53 genera and 25 subgenera in 10 tribes, while Kuznetsov (1997) reported 72 genera in 9 tribes.

Irshad (2001) reported 71 species of coccinellids from Pakistan, but Irshad (2003) reduced this list to 61 species by removing the doubtful species. Similarly, Rafi et al. (2005) listed 75 species of predatory ladybird beetles from Pakistan. All of these compilations are based on external morphology of the adult specimens, which might result in identification mistakes at the species level.

Gilgit-Baltistan lies between 72°N and 75°N and between 35°E and 37°E; biogeographically, the area is in the Palearctic region and belongs to the dry mountain subecological zone of Pakistan. The area is highly diverse and climatic conditions vary from extreme cold to extreme hot spots, with diverse flora and fauna. The area has many apple and grape plantations, which have mite and scale insect infestations. As already stated, Scymnus

Abstract: The fauna of the subfamily Scymninae (Coccinellidae: Coleoptera) of Gilgit-Baltistan was explored and studied. This study confirmed the occurrence of 4 species in 2 genera of Scymninae. These include 2 species in genus Scymnus (S. posticalis Sicard, 1913 and S. nubilus Mulstant, 1850), and 2 species in genus Stethorus (Stethorus gilvifrons (Mulstant, 1850) and S. pauperculus (Weise, 1895)). Among these 4 species, S. posticalis Sicard is reported here as a new record from the study area. A description of each species is given, along with color plates of adult specimens and genitalia. Remarks pertaining to taxonomic discussion, history, taxon status, hosts, habitat, identification key, and distribution of each species in the study area are also given.

Key words: Coccinellidae, Scymninae, fauna, Scymnus, Stethorus, taxonomy, distribution, Gilgit-Baltistan

Received: 10.01.2014 Accepted/Published Online: 07.07.2015 Printed: 30.11.2015

Research Article

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coccinellids are predators of these pests; therefore, there is a need to explore the Scymnus coccinellids of Gilgit-Baltistan. Moreover, proper taxonomic studies are necessary for developing biological control-based insect pest management strategies (Irshad and Haq, 2010).

2. Materials and methods2.1. The study area – Gilgit-BaltistanGilgit-Baltistan (formerly the Northern Areas of Pakistan) is spread over an area of 72,496 km2 and is administratively divided into 7 districts: Astore, Diamer, Gilgit, Ghanche, Ghizer, Hunza-Nager, and Skardu. The area lies between 72°N and 75°N and between 34.5°E and 37°E. About 44% of the area is covered by mountains (rocks, wetlands, etc.), 50% is alpine pasture, 4% forests, and 1% cultivable waste, while only 1% is under cultivation. Three high mountain ranges, namely the Himalayas, Karakorum, and Hindu Kush, are found in the area. The area is home to 5 of the world’s highest peaks of above 8000 m and about 50 peaks with elevations of 7000 m. Along with other world-famous peaks, Nanga Parbat (known as Killer Mountain) and K2 (Mount Godwin-Austen) are located in the area. This area is surrounded by China, India, and Afghanistan, and it is separated from Tajikistan by the narrow Wakhan strip.2.2. CollectionFor collection of the coccinellid species, surveys were conducted in all 7 districts of Gilgit-Baltistan from 2006 to 2011, mostly in the months of May through September, as the majority of the areas of Gilgit-Baltistan are accessible only during these months due to harsh weather conditions. Each locality was visited fortnightly or monthly depending upon the accessibility of the area. Standard collection procedures were applied. About 120 ladybird beetle specimens were collected. Field data of each specimen was recorded. In addition to the fresh collections, the housed collection of the National Insect Museum (NARC), Islamabad, was also examined.2.3. Genitalia extraction and examinationFor genitalia extraction, the method of Majerus and Kearns (1989) was followed with some modifications. The specimens were softened by putting them into hot water for 1 to 2 min. With the help of two entomological needles, the abdomen was detached from the body and boiled in 10% potassium hydroxide solution for 30 min to dissolve excess tissue and partially clear opaque structures. The abdomen was cleaned in hot water and transferred to pure glacial acetic acid for 5 min. To dehydrate the abdomen, it was first immersed in 80% ethanol and then in absolute alcohol for 5 min. Finally, the abdomen was moved to clove oil. The processed abdomen was put on a cavity slide with a drop of glycerin, and the genitalia were extracted with the help of two entomological needles under a stereoscope.

Male genitalia were mounted onto a plastic strip adhesive with hydrosoluble glue, and the female genitalia onto a strip of transparent plastic with Euparal. 2.4. Description To minimize redundancy, only characteristics peculiar to a given lower-ranking taxon are presented in its description. The species were identified and described following the literature of Kapur (1958), Canepari and Milanese (1997), Katakura et al. (2001), Inayatullah et al. (2005), and Rafi et al. (2005).

3. ResultsThe results of the present study revealed that there are 4 species in 2 genera of Scymninae (Coccinellidae) in Gilgit-Baltistan, Pakistan. Distribution of Scymninae species in the study area is shown in Figure 1.3.1. Subfamily: Scymninae Mulsant, 1846Synonyms: Scymninae Mulsant, 1846; Scymniens Mulsant, 1846; Scymninae Della Beffa, 1912.3.2. DiagnosisBody small to medium in size. Eyes and dorsum of body with dense pubescence. Antennae short, 9- to 11-segmented, with distinct club. Terminal segment of maxillary palpus with truncate apex, cylindrical. Mentum and submentum relatively widely articulated. Mandibles with 1 usually bifid tooth at apex. Pronotum anteriorly narrowed. Tarsi cryptotetramerous.3.3. Key to the genera of subfamily Scymninae of Gilgit-Baltistan

1. Pronotum broadly rounded at middle of anterior margin. Last segment of maxillary palpi narrowed ..................................................................................... Stethorus1. Pronotum longitudinally truncate at middle of anterior margin. Last segment of maxillary palpi cylindrical ........................................................... Scymnus

3.4. Genus: Scymnus Kugelann, 1794Type species: Scymnus nigrinus Kugelann, 1794, by subsequent designation of Westwood (1838–1840).Synonyms: Scymnus Kugelann, 1794; –Mulsant, 1846; –Crotch, 1874; –Korschefsky, 1931.3.4.1. Scymnus nubilus Mulsant, 1850 Synonyms: Scymnus nubilus Mulsant, 1850; –Bielawski, 1972; –Booth and Pope, 1989.

Scymnus (Scymnus) nubilus Korschefsky, 1931.Scymnus curtisii Mulsant, 1850 (synonymized by

Booth and Pope, 1989); Scymnus suturalis Motschulsky, 1858; –Crotch, 1874; –Korschefsky, 1931; –Iablokoff-Khnzorian, 1972.

Scymnus stabilis Motschulsky, 1866; –Crotch, 1874; –Weise, 1900; –Korschefsky, 1931.

Scymnus lateralis Sicard, 1913; –Korschefsky, 1931; –Pang and Gordon, 1984.

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Material examined: 3 ♂ 5 ♀ Pak. GB, Gilgit, Jaglot, 22.VI.2006 (Ather) (NIM); 1 ♂ 5 ♀ Pak. GB, Gilgit, Jaglot, 06.VI.2007 (Amjad) (NIM).

Diagnosis: Body small, elongate, moderately convex as shown in Figure 2. Head light brown to dark brown. Head deeply inserted, visible from above with eyes large and brown. Pronotum dark brown, darker in middle with lighter reddish brown posterior and anterior margins. Elytra ground color yellowish to reddish brown, punctate with a dark brown to black sutural stripe from basal margin and gradually narrowed toward apex, lateral margins narrowly dark brown to black at middle. Antennae small, segmented. Basal segment is thick, broader than and about twice as long as the second segment. Second segment is as long as and twice as broad as the third segment. Body dark brown from below, densely covered with fine, short, transparent, yellow hairs.

Genitalia: Phalobase: Trab long, thick, curved at middle. Basal piece short and rectangular. Parameres thick, slightly longer than median lobe, slightly compressed at base, tips rounded with long sparse hairs. Median lobe broad for most of its length except apex, which is pointed and slightly curved as shown in Figure 3.

Jaglot

Gulmit

Scymnus nubilus

Scymnus posticalis

Stethorus gilvifrons

Stethorus pauperculus

Figure 1. Distribution of Scymninae species in Gilgit-Baltistan.

Figure 2. Adult of Scymnus nubilus.

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Remarks: This species is very similar to S. (Neopullus) hoffmanni in general appearance and coloration, and can be differentiated by the male genitalia. Booth and Pope (1989) synonymized S. curtisii Mulsant and S. lateralis Sicard, and gave the valid name of Scymnus nubilus Mulsant.

Host: It is a general predator of aphids, scale insects, and mites.

Habitat: It can be found on the lower sides of fruit trees like apple and walnut, and on grape vines.

Local distribution: Jaglot, Gilgit.World distribution: Bangladesh, China, India,

Myanmar, Nepal, Pakistan, Sri Lanka.3.4.2. Scymnus posticalis Sicard, 1913Synonyms: Scymnus posticalis Sicard, 1913; Scymnus (Pullus) posticalis Korschefsky, 1931; –Pong, 1984. Scymnus hilaris Weise, 1879; –Lewis, 1896. Pullus hilaris Ohta, 1929. Pullus hilaris ab. awanus Ohta, 1929; –Sasaji, 1971. Scymnus (Pullus) hilaris Sasaji, 1971. Scymnus (Scymnus) ishidai Araki, 1963; –Sasaji, 1971. Scymnus (Nephus) inops Smirnoff, 1973.

Material examined: 1 ♂ 2 ♀ Pak. GB, Hunza-Nager, Gulmit, 04.VI.2007 (M. Ashfaque) (NIM); 2 ♂ 3 ♀ Pak. GB, Hunza-Nager, Gulmit, 12.VI.2008 (Ashraf) (NIM).

Diagnosis: Body small, oval, highly convex, ground color black and densely pubescent (Figure 4). Head brownish black, not visible from above, eyes small, brownish black. Pronotum black, densely pubescent, transverse, curved inward, posteriorly pushing scutellum. Scutellum visible and black. Elytra shiny black except anal portion, which is light reddish brown.

Genitalia: Phalobase: Trab long, thick, distally curved, and expanded. Basal piece rectangular. Parameres short, comparatively thin, tips pointed and with long hairs. Median lobe thick, broad at base, gradually tapering toward apex, tip rounded with long hairs on dorsal and distal portions. Siphon: Capsule unique, asymmetrical, both arms forming 180° angle, outer arm short, inner arm long. Tube cylindrical, moderate in thickness, abruptly curved at base, then broadly curved at middle, distal portion comparatively thin, tip flattened with a narrow process directed downward. Male genitalia of Scymnus posticalis shown in Figure 5.

Remarks: This relatively small black coccinellid species resembles other members of genus Scymnus like S. nubilus and S. pauperculus, as all 3 species are similar in size and body coloration. However, this species is remarkably different in the male genitalia structure from the other 2 species. Thapa (2000) reported this species from Nepal. Agarwala and Yasuda (2001) reported this species as a predator of Aphis gossypii from India. Poorani (2002) also listed S. posticalis in the Indian checklist of predatory coccinellids.

Host: It is a general predator of aphids, scale insects, and mites.

Habitat: It can be found on fruit trees like apple and walnut, and on grapes.

Local distribution: Gulmit, Hunza.

Figure 3. Male genitalia of Scymnus nubilus.

Figure 4. Adult of Scymnus posticalis.

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World distribution: China, India, Japan, Myanmar, Nepal.3.5. Genus: Stethorus Weise, 18853.5.1. Stethorus gilvifrons (Mulstant, 1850)Synonyms: Scymnus gilvifrons Mulsant, 1850; –Crotch, 1874; –Korschefsky, 1931; –Kapur, 1948; –Mathur and Srivastava, 1966. Scymnus (Stethorus) gilvifrons Weise, 1885.

Material examined: 3 ♂ 4 ♀ Pak. GB, Gilgit, Jaglot, 03.VII.2003 (Falak Naz) (NIM); 2 ♂ 2 ♀ Pak. GB, Gilgit, 04.VI.2007 (M. Ashfaque) (NIM); 3 ♀ Pak. GB, Gilgit, Jaglot, 15.VI.2008 (Amjad) (NIM).

Diagnosis: Body small, slightly oval, widest at middle, convex, black, coarsely punctate, pubescent with rather long white hairs as shown in Figure 6. Head mostly black with anterior half testaceous and sparsely punctate. Pronotum and elytra black. Dorsal surface with grayish, moderately long, sparse, semierect hairs. Legs testaceous. Male genitalia with thin parameres, shorter than median lobe, median lobe very long, curved at subdistal portion, tip of siphonal tube blunt.

Male genitalia: Phalobase: Trab very short and distally expanded. Basal piece: Small and semicircular. Median lobe: Very long, cylindrical, narrow and tapering toward apex, bent toward parameres at subdistal portion slightly and without hairs. Parameres: Very thin, about three-quarters of median lobe without hairs, apex with a pair of setae. Siphon: Siphonal capsule simple, without an outer hook but inner hook elongated and apically bifurcated, siphonal tube thin, long, forming a complete loop with pointed tip as shown in Figure 7.

Remarks: The type locality of this species is Derbent, Caucasus (USSR). Kapur (1948), while working on the genus Stethorus Weise of Old World species, described this species. He also reported some materials of this species from Mastung (Balochistan) and Faisalabad (formerly Lyallpur) (Punjab), Pakistan, collected while feeding on

Figure 5. Male genitalia of Scymnus posticalis.

Figure 6. Adult of Stethorus gilvifrons.

Figure 7. Male genitalia of Stethorus gilvifrons.

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mites of apple and castor oil plants. It was also reported by Rafi et al. in 2005 from northern Pakistan without consulting genitalia.

This species may be confused with another Stethorus species, S. pauperculus. Both species are very similar in general appearance and coloration. However, it can be distinguished from S. pauperculus by the structure of the male genitalia. The siphon of S. gilvifrons forms a complete loop, while that of S. pauperculus is somewhat straight. Some authors have incorrectly illustrated the male genitalia of this species with S. siphonulus. This species is also confused with S. wollastoni Kapur (Syn. S. minimus) due to similarities in coloration, especially the testaceous interior part of head.

Host: It is a general predator of mites.Habitat: It can be found in fruit orchards and on

isolated fruit trees like pear, apple, and walnut, and on grapes.

Local distribution: Jaglot, Gilgit.World distribution: Cyprus, India, Iran, Italy, Pakistan,

Saudi Arabia, Yemen. 3.5.2. Stethorus pauperculus (Weise, 1895)Synonyms: Scymnus (Stethorus) pauperculus Weise, 1895; Stethorus pauperculus Weise, 1900; –Kapur, 1948.

Material examined: 2 ♂, 2 ♀ Pak. GB, Gilgit, 03.VI.2003 (Ather) (NIM); 1 ♂ 5 ♀ Pak. GB, Gilgit, Jaglot, 03.VII.2003 (Falak Naz) (NIM); 3 ♂ 1 ♀ Pak. GB, Gilgit, 04.VI.2007 (M. Ashfaque) (NIM).

Diagnosis: Body small with yellow mouth parts. Elytra and thorax wholly black, devoid of spots, pubescence distinctly apparent, legs brownish, short, and profusely setose. Adult is shown in Figure 8.

Genitalia: Phalobase: Trab with short apex slightly expanded. Basal piece: Semicircular. Parameres: Long, slender, gradually tapering toward apex forming hairs like tip. Median lobe: Very long cylindrical thickness up to three-quarters of its length, then slightly turned and tapering toward apex. Siphonal tip: abruptly turned and pointed. Siphon capsule absent, small tube replacing capsule. Siphonal tube turned abruptly, slightly bent at middle, tip blunt. Male genitalia are given in Figure 9.

Remarks: This species also resembles other Stethorus species. Its distinguishing characters from S. gilvifrons are given under the remarks for S. gilvifrons. This species can be distinguished from S. yunnanensis by comparing male genitalia. Siphonal tube in S. pauperculus is somewhat straight at the base, while that of S. yunnanensis is semicircular at the base. Median lobe of S. pauperculus is comparatively thin with rounded tip, whereas it is broad with notched tip in S. gilvifrons.

Host: It is a general predator of mites.Habitat: It can be found in fruit orchards and on

isolated fruit trees like pear, apple, and walnut, and on grapes.

Local distribution: Jaglot, Gilgit.World distribution: India, Malaysia, Pakistan,

Thailand, Yemen.

Figure 8. Adult of Stethorus pauperculus.

Figure 9. Male genitalia of Stethorus pauperculus.

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4. DiscussionPreviously, Irshad (2001, 2003) and Rafi et al. (2005) reported 3 species of subfamily Scymninae from the Northern Areas of Pakistan (now Gilgit-Baltistan). These include Scymnus nubilus Mulstant, 1850; Stethorus gilvifrons (Mulstant, 1850); and Stethorus pauperculus (Weise, 1895). During the present study, surveys were conducted throughout the Gilgit-Baltistan region for ladybird beetles of the subfamily Scymninae. The taxonomic study of the collected specimens confirmed the occurrence of 4 species in 2 genera of subfamily Scymninae in the region. The identified species occurring in Gilgit-Baltistan are Scymnus nubilus Mulstant, S. posticalis, Stethorus gilvifrons,

and S. pauperculus. Among these, Scymnus posticalis is a new record for the Gilgit-Baltistan region, a high-altitude dry mountain area of Pakistan. The taxonomic position of these species was confirmed by genitalia morphology; previously, identification was carried out only through external morphology of the adults, which may result in misidentification. Micrococcinellids, especially species of genera Scymnus and Stethorus, are similar in appearance and need to be identified through genitalia examination. The findings are significant, with 4 confirmed records of Scymninae, and could serve as a baseline study for the region of Gilgit-Baltistan.

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