Biodiversity Data Journal :
Taxonomy & Inventories
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Corresponding author: Karol Szawaryn (k.szawaryn@gmail.com), Rui-E Nie (nrewsq2021@126.com)
Academic editor: Enrico Ruzzier
Received: 19 Sep 2024 | Accepted: 08 Nov 2024 | Published: 21 Nov 2024
© 2024 Zafar Iqbal, Rashid Azad, Xu Jin, Muhammad Asghar Hassan, Munawar Abbas, Muhammad Nasir, Imran Bodlah, Muhammad Ali, Karol Szawaryn, Rui-E Nie
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Iqbal Z, Azad R, Jin X, Hassan MA, Abbas M, Nasir M, Bodlah I, Ali M, Szawaryn K, Nie R-E (2024) The review of the genus Coccinella (Coleoptera, Coccinellidae) from Pakistan. Biodiversity Data Journal 12: e137417. https://doi.org/10.3897/BDJ.12.e137417
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The genus Coccinella is reviewed with seven species found in Pakistan: C. luteopicta (Mulsant, 1866), C. marussii Kapur, 1973, C. iranica Dobzhansky, 1926, C. transversalis Fabricius, 1781, C. septempunctata Linnaeus, 1758, C. transversoguttata transversoguttata Faldermann, 1835 and C. undecimpunctata Linnaeus, 1758. Information on prey, host plants, distribution and an identification key for Coccinella species in Pakistan is provided. Additionally, newly-sequenced partial COI (cytochrome-c-oxidase subunit I) for C. luteopicta and C. marussii were used to determine their phylogenetic positions within the genus Coccinella.
This study comprehensively reviews the genus Coccinella in Pakistan and highlights Coccinella luteopicta as a new country record. Morphological features of adults, including male genital characters and an identification key to known species in Pakistan are presented. Records of prey, host plants and distributions for all identified species are included. The new data (COI-barcode) shows that C. luteopicta (Mulsant, 1866) was recorded first in Pakistan.
Asia, barcoding, Coccinelloidea, COI, new record, Oriental Region
The family Coccinellidae (Coleoptera) comprises over 6,000 species worldwide (
The genus Coccinella belongs to the tribe Coccinellini within the subfamily Coccinellinae. It was established by Linnaeus in 1758. Subsequently,
Members of this genus are aphidophagous (
Specimens Collection and identification
The adult specimens of ladybird beetles, prey and associated plants were collected from various localities in northern Pakistan during 2015 and 2022. Collected beetles were preserved in 95% ethanol and male genitalia were dissected and cleared in 10% potassium hydroxide (KOH). Specimens were examined and photographed using a Nikon digital camera attached to stereomicroscope SMZ1500. Furthermore, specimens were identified using the following publications:
The following body measurements were taken using an ocular micrometer: total length (TL): from the tip of the clypeus margin to the tip of the elytra; total width (TW): across the widest part of both elytra; head width (HW): in a frontal view; total height (TH): across the highest point of the elytra: pronotal width (PW): at widest part; pronotal length (PL): from the middle of the base to anterior margin of pronotum; elytral length (EL): from apex to base including scutellar shield.
Photographs were edited using Adobe Photoshop CS6 and Helicon Focus 8.1.0. Specimens are deposited at the Laboratory of Biosystematics, Department of Entomology, Pir Mehr Ali Shah Arid Agriculture University Rawalpindi, Pakistan (PMAS-AAUR) and the National Insect Museum, National Agriculture Research Center, Islamabad (NIM).
DNA Barcoding sequencing and analysis
DNA was extracted from the thoracic muscles of the selected adult specimen using the DNeasy Blood and Tissue Kit (Qiagen, Germany) following the manufacturer’s protocol. Amplification targeting a 418 base pair region of the mitochondrial cytochrome oxidase subunit I (COI) gene with invertebrate-specific primers: Primer_F (CCNGAYATRGCNTTYCCNCG) and Primer_R (TANACYTCNGGRTGNCCRAARAAYCA) (
TransAlign (
Coccinella Linnaeus, 1758: 364. Type species: Coccinella septempunctata Linnaeus, 1758, subsequently designated by
Coccinella (Fig.
Adalia luteopicta Mulsant, 1866: 45;
Lioadalia luteopicta:
Coccinella luteopicta:
Body (Fig.
TL: 6.20–6.37 mm; TW: 4.27–4.36 mm; HW: 1.40–1.44 mm; TH: 2.01–2.03 mm; EL/TW: 1.10-1.15; TL/TW: 1.46; PL/PW: 0.52-0.54; PW/EW: 0.65-0.66.
Coccinella luteopicta closely resembles C. transversalis and C. marussii in general appearance, but it can easily be identified by having a reticulate black pattern on the elytra, elytra suture with anterior half-black, penis guide in inner view broader at the base and then gradually tapering towards the blunt tip (Fig.
Pakistan: Gilgit-Baltistan; – India, Nepal, China (Tibet, Yunnan) (
Prey. In the present study, C. luteopicta was feeding on Therioaphis trifolii (Monell) and Brevicoryne brassicae (Linnaeus) (Hemiptera, Aphididae).
Associated Plants. This species was collected from Trifolium alexandrinum Linnaeus (Fabales, Fabaceae) and Brassica oleracea Linnaeus (Brassicales, Brassicaceae) in this study.
Coccinella marussii Kapur, 1973: 374;
Body (Fig.
TL: 5.23–5.64 mm; TW: 3.89–4.09 mm; HW: 1.35–1.43 mm; TH: 1.95–2.34 mm; EL/TW: 1.05; TL/TW: 1.35–1.38; PL/PW: 0.54–0.57.
This species is similar to C. luteopicta and C. transversalis in external appearance, but it can be distinguished by the apex of the penis guide with a small hastate in the inner view (Fig.
Pakistan: Gilgit-Baltistan (
Prey. In the present study, C. marussii predates on Macrosiphum sp. (Hemiptera, Aphididae).
Associated Plants. This species was collected from Rosa webbiana Wallich ex Royle (Rosales) and Ribes sp. (Saxifragales, Grossulariaceae) (current study).
This is a rare species in the family Coccinellidae with limited distribution (
Coccinella transversalis Fabricius, 1781: 97;
Coccinella repanda:
Coccinella contempta:
Body (Fig.
TL: 5.30–547 mm; TW: 4.29–4.37 mm; HW: 1.35–1.39 mm; TH: 2.36–2.38 mm; EL/TW: 1.06–1.08; TL/TW: 1.24–1.26; PL/PW: 0.52–0.55.
Coccinella transversalis can easily be distinguished from C. marussii and C. luteopicta by having three transverse large markings on the elytra and apex of the penis with a slightly dilated and small thread-like appendage at the tip as in Fig.
Pakistan. Azad Jammu and Kashmir (
Prey.
Associated plants. Coccinella transversalis was collected from Heteropogon contortus (Linnaeus) (Poales, Poaceae), Tagetes minuta Linnaeus (Asterales, Asteraceae) and Cyperus rotundus Linnaeus (Poales, Cyperaceae) (current study).
Coccinella iranica Dobzhansky, 1926: 26;
Coccinella (s. str.) iranica:
Body broadly oval and slightly convex, dorsal surface glabrous; head black; mouthparts and antennae dark brown to black; pronotum mostly black with a brownish stripe along anterior margins; scutellar shield black; elytra brown to brownish-yellow with eight irregular black spots, first elongate oval black spot at anterior margin along suture of both elytrons, second large L-shaped black mark at the middle, third oval spot at posterolateral margins and fourth sub-equal black spot near suture at the posterior margin of elytra. Male genitalia: penis apex flattened, with blunt tip; penis guide in inner view with narrow and rounded tip, paramers slightly shorter than the penis guide (
TL: 5.30–547 mm; TW: 4.29–4.37 mm (
Coccinella iranica is similar to C. marussii, but it can be differentiated by the latter from the brownish stripes on the anterior margins and the penis guide with the narrow and rounded tip in the inner view. In C. marussii, pronotal anterior corners with pale yellow quadrangular marks, penis guide with a broad and blunt tip in the inner view (Fig.
Pakistan: Gilgit-Baltistan (
Prey. Unknown from Pakistan.
Associated plants. Unknown from Pakistan.
Coccinella septempunctata Linnaeus, 1758: 365:
Coccinella divaricata Olivier, 1808: 1001;
Coccinella confusa Wiedemann, 1823: 72;
Coccinella brucki Mulsant, 1866: 90;
Body (Fig.
TL: 6.63–7.20 mm; TW: 5.35–5.60 mm; HW: 0.86–0.94 mm; TH: 3.26–3.28 mm; EL/TW: 1.07–1.09; TL/TW: 1.24–1.33; PL/PW: 0.42–0.44; PW/EW: 0.63–0.65.
Coccinella septempunctata can be easily separated from C. transversoguttata and C. undecimpunctata by having seven black spots at the elytra (Fig.
It is a widely distributed species in Pakistan (
Prey.
In this study, this species was found feeding on Acyrthosiphon loti (Theobald), Aulacorthum solani (Kaltenbach), A. pisum Harris, Aphis craccivora Koch, A. fabae Scopoli, A. farinose (Gmelin), A. gossypii Glover, A. spiraecola, A. solanella Theobald, A. punicae Passerini, A. verbasci Schrank, Brachycaudus helichrysi (Kaltenbach), Brevicoryne brassicae (Linnaeus), Capitophorus formosartemisae (Takahashi), Chaitophorus populifolii Essig, Cinara tujafilina (Del Guercio), Eriosoma lanigerum (Hausmann), Hysteroneura setariae (Thomas), Lachnus wichmanni Hille Ris Lambers, Lipaphis erysimi (Kaltenbach), Macrosiphum pachysiphon Hille Ris Lambers, M. rosae (Linnaeus), Meldnaphis donacis (Passerini), Myzocallis pakistanicus Hille Ris Lambers, Myzus ornatus (Laing), Myzus persicae (Sulzer), Periphyllus sp., Phorodon cannabis Passerini, Rhopalosiphum padi (Linnaeus), R. maidis (Fitch), Shivaphis celti Das, Schizaphis graminum (Rondani), Sitobion avenae Fabricius, Tinocallis kahawaluokalani (Kirkaldy), Therioaphis trifolii (Monell), Toxoptera aurantii (Boyer de Fonscolombe), Tuberolachnus salignus Gmelin, Uroleucon carthami (Theobald) (Hemiptera, Aphididae), Adelges (Dreyfusia) knucheli (Schneider-Orelli and Schneider) (Hemiptera, Adelgidae), Drosicha stebbingi Green), D. mangiferae (Green) (Hemiptera, Margarodidae), Planococcus citri (Risso), Phenacoccus solenopsis Tinsely, Maconellicoccus hirsutus (Green) (Hemiptera, Pseudococcidae), Dialeurodes citri (Ashmead) (Hemiptera, Aleyrodidae) Camarotoscena sp., Heteropsylla sp. (Hemiptera, Psyllidae), some species of scale insects (Hemiptera, Diaspididae) and Phyllocnistis sp. (Lepidoptera, Gracillariidae).
Associated Plants. This species was collected from Cumium cyminum (Linnaeus) (Apiales, Apiaceae), Anthemis arvensis (Linnaeus), A. tinctoria Kelwayi, Artemisia sp., A. maritima (Linnaeus), Carthamus oxyacantha Bieberstein, Erigeron canadensis (Linnaeus), Parthenium hysterophorus (Linnaeus), Sonchus asper (Linnaeus) Hill, Tagetes minuta (Linnaeus) (Asterales, Asteraceae), Brassica campestris (Linnaeus), B. campestris var botrytis (Linnaeus), B. oleracea (Linnaeus) (Brassicales, Brassicaceae), Capparis spinosa Linnaeus (Brassicales, Capparaceae), Moringa oleifera Lamarck (Brassicales, Moringaceae), Spinacia oleracea (Linnaeus) (Caryophyllales, Amaranthaceae), Bougainvillea glabra Choisy, Mirabilis jalapa (Linnaeus) (Caryophyllales, Nyctaginaceae), Abies pindrow (Royle ex Don) (Pinales, Pinaceae), Rumex dentatus (Linnaeus), R. hastatus Don (Caryophyllales, Polygonaceae), Tamarix gallica (Linnaeus) (Caryophyllales, Tamaricaceae), Quercus baloot Griffith (Fagales, Fagaceae), Acacia farnesiana Wight et Arnott, Cassia fistula Linnaeus, Dalbergia sissoo Roxburgh, Medicago sativa Linnaeus, Prosopis juliflora (Swartz) de-Candolle, Sophora alopecuroides Linnaeus, Trifolium alexandrinum Linnaeus (Fabales, Fabaceae), Juglans regia Linnaeus (Fagales, Juglandaceae), Clerodendrum philippinum (Osbeck) Mabberley (Lamiales, Lamiaceae), Verbascum thapsus Linnaeus (Lamiales, Scrophulariaceae), Olea europaea Linnaeus (Lamiales, Oleaceae), Duranta erecta Linnaeus, Lantana camara Linnaeus (Lamiales, Verbenaceae), Hibiscus rosa-sinensis Linnaeus (Malvales, Malvaceae), Populus nigra Linnaeus, Salix alba Linnaeus (Malpighiales, Salicaceae), Lagerstroemia indica Linnaeus, Punica granatum Linnaeus (Myrtales, Lythraceae), Thuja sp. (Pinales, Cupressaceae), Psidium guajava Linnaeus, Syzygium cumini (Linnaeus) Skeels (Myrtales, Myrtaceae), Cyperus rotundus Linnaeus (Poales, Cyperaceae), Avena sativa Linnaeus, Arundo donax Linnaeus, Cynodon dactylon (Linnaeus) Persoon, Dactyloctenium aegyptium (Linnaeus) Willdenow, Heteropogon contortus (Linnaeus) Beauvois ex Roemer and Schultes, Phragmites karka (Retzius), Triticum aestivum Linnaeus, (Poales, Poaceae), Berberis lyceum Royle (Ranunculales, Berberidaceae), Cannabis sativa Linnaeus, Celtis eriocarpa Decne. (Rosales, Cannabaceae), Eriobotrya japonica (Thunberg) Lindley, Hippophae rhamnoides Linnaeus (Rosales, Elaeagnaceae), Malus domestica Borkhausen, Prunus avium Linnaeus, P. armeniaca Linnaeus, P. persica (Linnaeus) Batsch, Pyrus communis Linnaeus, P. pyrifolia (Burman) Nakai, Rosa indica Trattinnick (Rosales, Rosaceae), Ficus sp., Morus alba Linnaeus (Rosales, Moraceae), Aesculus indica (Wallich ex Cambessèdes) Hooker (Sapindales, Sapindaceae), Citrus sp. (Sapindales, Rutaceae), Convolvulus arvensis Linnaeus (Solanales, Convolvulaceae), Cestrum diurnum Linnaeus, Solanum nigrum Linnaeus, S. tuberosum Linnaeus, Withania somnifera (Linnaeus) Dunal (Solanales, Solanaceae), Ziziphus mauritiana Lamarck, Z. nummularia (Burman) Wight and Arnott (Rosales, Rhamnaceae) and Urtica dioica Linnaeus (Rosales, Urticaceae) (current study).
Coccinella transversoguttata Faldermann, 1835: 454:
Coccinella transversoguttata var. Sedakovi Weise, 1889: 537.
Coccinella geminopunctata Liu, 1962: 265:
Body (Fig.
TL: 5.23–6.43 mm; TW: 3.95–5.00 mm; HW: 1.28–1.52 mm; TH: 2.15–2.40 mm; EL/TW: 1.10–1.14; TL/TW: 1.29–1.32; PL/PW: 0.51–0.53.
Coccinella transversoguttata transversoguttata is similar to C. undecimpunctata in external structure and colouration, but can be separated from the latter by a diagnostic character; penis-guide in inner view, rhomboidally dilated with apical hastate (Fig.
Pakistan. Gilgit-Baltistan (
Prey.
In the current study, this species has been recorded from the following aphid species: Acyrthosiphon pisum Harris, Lachnus wichmanni Hille Ris Lambers, Macrosiphum pachysiphon Hille Ris Lambers, Aphis craccivora Koch, A. fabae Scopoli, A. nerii Fonscolombe, A. farinose (Gmelin), A. gossypii Glover, Schizaphis graminum (Rondani), Tuberolachnus salignus Gmelin and Toxoptera aurantii (Boyer de Fonscolombe) (Hemiptera, Aphididae).
Associated Plants. It is collected from the following plants: Erigeron canadensis (Linnaeus) (Asterales, Asteraceae), Capparis spinosa Linnaeus (Brassicales, Capparaceae), Convolvulus arvensis Linnaeus (Solanales, Convolvulaceae), Hippophae rhamnoides Linnaeus (Rosales, Elaeagnaceae), Salix alba Linnaeus (Malpighiales, Salicaceae), Sophora alopecuroides Linnaeus (Fabales, Fabaceae), Rumex dentatus (Linnaeus) (Caryophyllales, Polygonaceae), Phragmites karka (Retzius), Triticum aestivum Linnaeus (Poales, Poaceae) and Rosa indica Trattinnick (Rosales, Rosaceae).
See
Coccinella undecimpunctata Linnaeus, 1758: 366; 89;
Coccinella aegyptiaca Reiche, 1861: 212:
Body (Fig.
TL: 4.56–4.91 mm; TW: 3.48–3.67 mm; HW: 1.02–1.27 mm; TH: 1.60–1.84 mm; EL/TW: 1.16–1.19; TL/TW: 1.31–1.34; PL/PW: 0.42–0.45; PW/EW: 0.64.
Coccinella undecimpunctata is similar to C. transversoguttata transversoguttata in general body structure and colouration, but can be separated by having a penis guide gradually tapering towards a blunt apex in inner view (Fig.
Pakistan. Azad Jammu and Kashmir (
Prey.
Associated Plants. It was collected from Brassica oleracea (Brassicales, Brassicaceae) during the current study.
Key to species of the genus Coccinella from Pakistan |
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1 | Elytral suture entirely or partially black | 2 |
– | Elytral suture not black | 4 |
2 | Anterior half of elytral suture black | C. luteopicta |
– | Elytral suture entirely black | 3 |
3 | Elytral scutellar macula large, broadly rounded (Fig. |
C. marussii |
– | Elytral scutellar macula smaller, more elongate oval (Fig. |
C. transversalis |
4 | Pronotum with brownish sub-quadrangular markings at anterior corners | C. iranica |
– | Pronotum with white-yellow quadrangular markings at anterior corners | 5 |
5 | Elytra with seven black spots or sometimes spots merge and form variable black marks (Fig. |
C. septempunctata |
– | Elytra with 11 black spots; pronotal angular spots connected at anterior margins | 6 |
6 | Elytral sutural spot sub-triangular (Fig. |
C. transversoguttata |
– | Elytral sutura spot oval or rounded (Fig. |
C. undecimpunctata |
COI sequences of C. luteopicta (Mulsant) and C. marussii Kapur were obtained and subsequently submitted to Genbank for the first time, with accession numbers PP853180 and PP853181, respectively. The phylogenetic tree was reconstructed based on the COI barcoding sequences using the Maximum Likelihood (ML) and Bayesian Inference (BI) methods (Fig.
Phylogenetic (BI and ML) tree of Coccinella species, based on COI sequences. The numbers displayed on branches represent the Bayesian posterior probability values (left) and bootstrap values for Maximum Likelihood analysis (right). Only branches with bootstrap values above 50% are shown. Sequenced obtained in this study are denoted by an asterisk (*) and newly-submitted sequences to NCBI are highlighted in red and bold.
Taxa used in this study are grouped in three clades. The first one includes single species Coccinella fulgida with moderate supporting values (PP 0.84 and 85). The second consists of sequences representing six species, C. transversoguttata, newly-sequenced C. marussii, C. magnifica, C. californica, C. novemnotata and C. septempunctata. The last clade contains sequences representing C. quinquepunctata, C. hieroglyphica, C. ainu, C. trifasciata, C. undecimpuntata, C. miranda, C. transversalis and newly-obtained sequence of C. luteopicta from Pakistan as the most basal within that clade.
The ladybird beetle species was most extensively studied as a potential biocontrol agent against various soft-sucking insect pests in Pakistan. Coccinella septempunctata Linnaeus is the only representative of this genus with a wide distribution and an extensive prey list, associated with a diverse host plants in Pakistan. In contrast, the three species, C. luteopicta (Mulsant), C. marussii Kapur and C. transversoguttata Faldermann are restricted to the northern regions of Pakistan. This faunistic study is unique compared to the works of
C. septempunctata is a well known polyphagous species recorded to prey on a wide range of soft insects mainly aphids which was also confirmed for the Pakistani populations (
Amongst the seven species of Coccinella recorded from Pakistan, four species are found in both Gilgit-Baltistan and Khyber Pakhtunkhwa Provinces, while Azad Kashmir, Balochistan, Punjab and Sindh each host three species (Fig.
The analysis of newly-obtained partial COI sequences for C. luteopicta and C. marussii from Pakistan, within a broader context of other Coccinella species from around the world, confirmed their status as distinct species within the genus Coccinella. This analysis also suggested possible hypotheses regarding their placement in groups of species, though with weak statistical support. However, previous studies by
The authors sincerely thank Alfried P. Vogler and Thomas J. Creedy of the Natural History Museum, London, United Kingdom, for their assistance with sequencing. Special thanks are also extended to Dr. Muhammad Ather Rafi, Dr. Ahmed Zia and Mr. Anjum Shehzad of the National Insect Museum, Islamabad (NIM), for their support in species identification. This work was supported by grants from the Anhui Provincial University Outstanding Youth Program (No. 2022AH020021) and the National Science Foundation of China (No. 32170443).
The COI sequences of genus Coccinella species used in this study with their GenBank accession numbers.