Revision of the genus Coccidula Kugelann (Coleoptera, Coccinellidae)

Karol Szawaryn; Oldřich Nedvěd; Amir Biranvand; Tomasz Czerwiński; Romain Nattier

doi:10.3897/zookeys.1043.65829

Abstract

The genus Coccidula Kugelann includes five species distributed in the Holarctic, with one species in North America and four in Palearctic region. Coccidula belongs to the tribe Coccidulini which historically was treated as a separate subfamily within ladybird beetles, but recent studies confirmed its placement as a tribe within the broadly defined subfamily Coccinellinae. All species are revised and a new synonymy of Lithophilus naviauxi Duverger with C. litophiloides Reitter is proposed. Light and electron microscopy pictures support morphological descriptions. An identification key to all species is also provided.

Keywords

Coccinelloidea, ladybirds, morphological revision, new synonym, taxonomy

Introduction

The classification of ladybird beetles (Coccinellidae) has changed dynamically in the last decade mainly due to molecular approaches. Although several studies have been conducted at the family level, none of them gave robust classification of the family (Seago et al. 2011; Robertson et al. 2015). Historically, the family was divided into six or seven subfamilies (Sasaji 1968; Kovář 1996) but more recent treatments based on morphology and molecules support just two, Microweiseinae and Coccinellinae (Ślipiński 2007; Seago et al. 2011; Robertson et al. 2015). However, recent analysis of a large molecular dataset (Che et al. 2021) revealed the existence of the third monotypic subfamily Monocoryninae.

The genus Coccidula Kugelann, 1798 was traditionally placed in the subfamily Coccidulinae (Sasaji 1968; Kovář 1996), nonetheless, in the new classification of ladybirds it was proposed to be one of the tribes (Coccidulini) within the broadly defined subfamily Coccinellinae. Seago et al. (2011) synonymized this tribe with Scymnini, however, after the analyses by Robertson et al. (2015) and Che et al. (2021) both are once again treated as independent tribes. Coccidulini are one of the most problematic groups of ladybirds as in the traditional classification they contain numerous genera with just superficial external similarity based mainly on hairy body surface and relatively long antennae. Consequently, in all molecular analyses they do not form a monophyletic group (Seago et al. 2011; Robertson et al. 2015; Che et al. 2021). The tribe is distributed worldwide with moderate diversity in the Palearctic (Kovář 2007) and African regions (Fürsch 2007; Tomaszewska 2010), rich in South America (Gordon 1994), but the most diverse fauna occurs in South Asia, Australia and neighboring regions (e.g., Ślipiński 2007; Poorani and Ślipiński 2009; Tomaszewska 2010; Tomaszewska and Ślipiński 2011; Szawaryn and Leschen 2019). The largest and most widely distributed is the genus Rhyzobius Stephens, 1831 with more than 100 recognized species (Tomaszewska 2010; Czerwiński et al. 2020) and numerous undescribed species mainly from New Guinea. Interestingly it is also the only genus of Coccidulini with known fossil representatives from the Eocene period discovered in Oise (Kirejtshuk and Nel 2012) and Baltic ambers (Szawaryn and Tomaszewska 2020).

Coccidula is a small genus distributed in the Holarctic, with one species in North America and four in Eurasia. Historically numerous species and varieties have been described based mostly on differences in color pattern, but most of them were subsequently synonymized when genitalia were examined. Gordon (1985) revised the North American species; however, the Palearctic species have not been revised until now. As Coccidulini has never been a subject of morphological cladistic analysis there is no hypothesis about its internal relationship available. However, based on recent molecular analyses (Che et al. 2021), C. scutellata (Herbst, 1783) and Rhyzobius litura (Fabricius, 1787) group in a single clade with the African genus Epipleuria Fürsch, 2001 and African species of Rhyzobius.

The European species are usually found in wetlands and water banks in low and middle elevations (Bielawski 1959). They live on herbaceous emergent grassy vegetation such as reeds, feeding on aphids such as Hyalopterus pruni (Hemiptera: Aphididae). Coccidula rufa is sometimes contrastingly reported also from dry sand dunes and in Finland from cereal fields (Clayhills and Markkula 1974). High prevalence (60–80%) of endosymbiotic bacteria Rickettsia and Wolbachia was reported from Germany (Weinert et al. 2007). Coccidula rufa is univoltine – mating and egg-laying occur in the spring and summer, eggs are laid in batches on reed stems and foliage, larvae develop through the spring and summer, and a new generation of adults emerges in July. All species may be locally and temporally abundant.

The tribe Coccidulini needs comprehensive revision. In the current work we present a morphological revision of all currently known species of Coccidula, the type genus for the tribe. This revision is a first step to understand the morphological diversity of the tribe and may lead to further phylogenetic studies.

Material and methods

Material used of this study is deposited in the following collections:

AJC Andrzej Jadwiszczak Collection, Poland;

ASC Alexander Slutsky Collection, Kharkov, Ukraine;

HNHM Hungarian Natural History Museum, Budapest, Hungary;

NMP National Museum Prague, Czech Republic;

MIZ Museum and Institute of Zoology, Warsaw, Poland;

MNHN Muséum national d’histoire naturelle, Paris, France;

USB University of South Bohemia, České Budějovice, Czech Republic.

Genitalia were dissected, cleared in a 10% KOH solution, washed in water, and placed in glycerol on slides for further study. Female genitalia were stained with chlorazol black. Measurements were recorded as follows: TL – total body length from apical margin of clypeus to apex of elytra; PL – pronotal length from the middle of anterior margin to the middle of the posterior margin; PW – pronotal width across widest part; EL – elytral length along suture including scutellum; EW – elytral width across both elytra at the widest part. Colour images were taken using either a stereo microscope Leica MZ 16 with a digital camera IC 3D; final images were produced using Helicon Focus 5.0X64 and Adobe Photoshop CS6 software, or a stereo microscope Nikon SMZ 1500 with Lumenera digital camera and QuickPhoto software, composite images with deep focus were generated using Zerene Stacker. The SEM photographs were taken in the Laboratory of Scanning Microscopy, MIZ (Warsaw), using a scanning electron microscope HITACHI S-3400N under low vacuum conditions and on JEOL JSM-7401F in Biology Centre CAS (České Budějovice). Terminology used for morphology follows Ślipiński (2007) and Lawrence et al. (2011). In this paper, we follow the classification proposed by Che et al. (2021).

Taxonomy

Family Coccinellidae Latreille, 1807

Subfamily Coccinellinae Latreille, 1807

Tribe Coccidulini Mulsant, 1846

Coccidula Kugelann, 1798

Coccidula Kugelann, 1798: 421. Type species: Chrysomela scutellata Herbst, 1783, by subsequent designation by Crotch 1874.

Strongylus Panzer, 1813: 114.

Cacidula Dejean, 1821: 132. Type species: Chrysomela pectoralis Fabricius, 1792 (=Dermestes rufus Herbst, 1783).

Cacicula Stephens, 1831: 397.

Diagnosis

Representatives of the genus Coccidula with its general body shape may resemble Tetrabrachys Kapur, however, it can be separated based on the structure of the tarsi which are tetramerous in both genera but in Coccidula the first tarsomere is sub-triangularly broadened apically and the second is elongate and distinctly lobbed, while in Tetrabrachys both the first and second are narrow, elongate and without lobes. Moreover, in Tetrabrachys the apical maxillary palpomere is widely securiform, and beetles are brachypterous, while in Coccidula the apical maxillary palpomere is only slightly widened and the second pair of wings is functional. Coccidula is also externally similar to European species of Rhyzobius but it can be separated based on the following characters: body almost parallel sided, elytra covered with punctures of two sizes, larger punctures arranged in nine rows (in C. litophiloides some of them are reduced), base of the pronotum not bordered, while in Rhyzobius the lateral body outline is broadly rounded, the elytra are covered with single sized, randomly arranged punctures, and base of the pronotum with distinct bordering line.

Description

Body elongate-oval, with sides parallel (Fig. 1C–H), body flattened in lateral view, convex in cross-section; dorsum covered with setiferous punctures of two sizes (Figs 7A, 9A), hairs directed forwards on pronotum, backwards on elytra.

Figure 1.

Immature stages and habitus of adult species of Coccidula Kugelann A C. rufa larva B C. rufa pupa C C. lepida, dorsal D C. lepida, ventral E C. litophiloides F C. reitteri G C. rufa H C. scutellata A, B Gilles San Martin, Wikimedia Commons C, D Danny Haelewaters G, H Udo Schmidt. Scale bars: 1 mm (C–H).

Head partially withdrawn into prothorax (Fig. 1C–H); ventral antennal grooves shallow and moderately long, extending to posterior border of an eye (Fig. 3E). Eyes prominent, coarsely facetted (7–8 ommatidia per eye width), ocular canthus distinct, about as long as 4–5 ommatidium diameters; interocular distance about 3× as eye diameter; interfacetal setae present only in basal part; temple behind eye distinctly longer than eye (Fig. 3E). Antennal insertion placed laterally, invisible from above, distance between antennal insertions about same as between eyes; frons around antennal insertions slightly expanded, covering antennal insertions, anterior tentorial pits placed ventrally below antennal insertions. Antennae (Figs 5A, E, 7A, D) longer than maximum head width including eyes, composed of 11 antennomeres (AN); scape simple, without projections, slightly curved; pedicel distinctly narrower than scape, elongate (1.5× longer than wide); AN 3–8 elongate (AN3 ≈ 3.5×; AN8 ≈ 1.3× longer than wide); AN 9–11 forming a loose, asymmetric club, ultimate AN truncate apically. Frontoclypeus short, transverse, anterior margin straight. Labrum entirely exposed, transverse, anterior margin straight. Mandibles asymmetric, bifid apically (Fig. 10G), molar part with basal tooth; prostheca distinct. Maxillary stipes (Figs 2B, 5C, 9C, 10H) with distinct groove for reception of maxillary palp in repose; palpomere 2 shorter than terminal (4^th) one, slightly broadened apically; palpomere 3 about 2.3× shorter than terminal one, subtriangular; terminal palpomere slightly securiform; lacinia with stiff setae on outer margin in apical half, with several additional spurs on surface (Fig. 10H). Labial palps (Figs 3E, 9C) with 3 palpomeres, inserted ventrally on prementum; palpomere 1 very small, apical palpomere as long as and about as broad as penultimate; distance between palp insertions about 1.5–2× as its width. Prementum subquadrate, transverse apically. Mentum trapezoidal, broadest in anterior part, with horseshoe impression at base (Figs 7C, 9C). Submentum broad, transverse, with suture invisible.

Figure 2.

Coccidula lepida LeConte SEM illustrations A pronotum B head and prothorax, ventral C meso and metaventrite D elytra dorsal E ventrite 1. Scale bars: 500 µm (A–C); 1 mm (E, D).

Anterior margin of pronotum weakly, broadly emarginate (Figs 3B, 5B) with anterior corners broadly rounded; lateral margins with moderately (Figs 7B, 9B) to distinctly expanded lateral beads (Fig. 3B), distinctly margined; hind corners sharply pointed; hind margin not bordered. Prothoracic hypomeron smooth, without delimited foveae (Figs 3C, 7C). Prosternum in front of coxae about as long as longitudinal length of procoxal cavity; anterior margin straight or slightly emarginate with distinct border. Prosternal process about 0.4 times of coxal diameter, surface smooth (Fig. 3C) or with lateral carinae (Figs 7C, 9E). Procoxal cavity oval, distinctly bordered anteriorly.

Figure 3.

Coccidula litophiloides Reitter SEM illustrations, paratype HNHM A body, dorsal B pronotum C head and prothorax, ventral D meso and metaventrite E head ventral. Scale bars: 1 mm (A); 500 µm (B–D); 400 µm (E).

Mesoventrite 1.3× longer than its width at the level of mid coxae (Figs 1D, 5D, 7D); mesal surface with deep emargination for receiving tip of prosternal process (Fig. 2C); anterior margin with completely raised border. Meso-metaventral process narrow (Figs 1D, 2C, 5D, 7E), about 0.5 times of mesocoxal diameter, junction slightly arcuate (Figs 2C, 3D, 5D, 7E, 9D), with suture visible. Metendosternite with stalk sub-quadrate, tendons long, separated by a distance of about width of stalk and situated closer to center (Fig. 10I). Scutellar shield pentagonal (Figs 7B, 9B). Elytra at base wider than pronotum, lateral margins clearly visible from above throughout (Figs 2D, 3A, 5A, 7A) (except C. scutellata where it is obscured in basal part, Fig. 9A), surface covered with punctures of double size, smaller irregularly distributed, larger punctures arranged in nine irregular longitudinal rows. Sutural stria absent. Elytral epipleuron narrow, incomplete, reaching base of ventrite 4 (Fig. 1D), with complete bordering line, epipleural foveae absent. Hind wings fully developed or missing (in C. litophiloides). Metaventral postcoxal lines roundly joined medially, complete laterally, straight or descending (Figs 2C, 3D, 5D, 7E, 9D). Metaventrite with discrimen visible in posterior 2/3.

Trochanters simple, subtriangular, without projection (figs 7E, 9D). Tibiae slightly expanded apically with one apical spur on forelegs, and two in mid and hind legs. Tarsi consisting of four tarsomeres, second tarsomere truncate apically; tarsal claws cleft apically (Fig. 9G) with single empodial seta present.

Abdomen in both sexes with 6 ventrites (Fig. 1D); ventrite 1 about as long as ventrites 2–4 combined, ventrite 2 longer than ventrite 3, ventrites 3–5 subequal in length. Abdominal postcoxal lines (Figs 7E, 9D) separate medially, recurved and complete, reaching anterior margin of ventrite, posteriorly reaching about half length of ventrite 1. Ventrite 5 in female posteriorly rounded (Fig. 7F), in male truncate (Fig. 9F). Ventrite 6 rounded in both sexes.

Male terminalia. Tegmen (Figs 4A, B, 8A, B, 10A, B) symmetrical; parameres articulated with penis guide. Penis (Figs 4C, 8C, 10C) slender, pointed apically; penis capsule asymmetrical with outer arm reduced, inner arm well developed. Apodeme of male sternum IX simple, not broadened apically (Figs 8D, 10D). Tergite X broadly rounded, semicircular (Figs 8D, 10D).

Figure 4.

Coccidula litophiloides Reitter A tegmen, lateral B tegmen, inner C penis, lateral D spermatheca. Scale bar: 500 µm (A–D).

Figure 5.

Coccidula reitteri Dodge SEM illustrations, HNHM A body, dorsal B pronotum C head and prothorax, ventral D meso and metaventrite E antenna. Scale bars: 1 mm (A); 500 µm (B–D); 300 µm (E).

Female terminalia. Coxites (Figs 10F) distinctly elongate, subtriangular; styli small but visible, bearing several short setae; infundibulum absent (Figs 4D, 8E, 10E); sperm duct simple. Spermatheca (Figs 4D, 8E, 10E) worm-like, without clear ramus or nodulus; spermathecal accessory gland small, elongate. Proctiger elongate, rounded apically (Fig. 10F).

Immature stages

Larva as in Fig. 1A, pupa as in Fig. 1B.

Distribution

Holarctic: Asia, Europe, Africa (North), North America.

Key to species of Coccidula Kugelann

1	Head and epipleurae black (Fig. 1C, D); elytra with humeral area black. Nearctic	C. lepida LeConte
–	Head and epipleurae testaceous; elytra with humeral area testaceous. Palaearctic	2
2	Pronotum with posterior corners pointed, with an angle much less than 90° (Figs 1G, 3B); pronotal lateral margins broadly explanate (Figs 1E, 3B); prosternal process without carinae (Fig. 3C); elytra with missing or reduced rows of large punctures 2 and 3 (counted from the suture)	C. litophiloides Reitter
–	Pronotum with posterior corners not distinctly pointed, with an angle around 90° (Figs 1F–H, 7B, 9B); pronotal lateral margins moderately explanate (Figs 1G, 7B, 9B); prosternal process with distinct lateral carinae (Figs 7C, 9E); elytra with all rows of large punctures well visible	3
3	Prosternal process with lateral carinae very distinct, sinuate, roundly joined to the anterior prosternal margin (Fig. 9E); lateral elytral margins in basal part not visible from above (Fig. 9A); metaventral postcoxal lines narrowly separated on metaventral process (Fig. 9D); specimens entirely testaceous or with more than one black macula on elytra (Fig. 1H); penis guide about half length of parameres (Fig. 10A)	C. scutellata Herbst
–	Prosternal process with lateral carinae straight, sometimes not joined together, extending to level of anterior border of procoxal cavity, not merged to anterior prosternal margin (Figs 5C, 7C); lateral elytral margins in basal part visible from above (Figs 5A, 7A); metaventral postcoxal lines joined on metaventral process (Figs 5D, 7E); specimens entirely testaceous to rufous (Fig. 1G) or with single elongate dark brown to black macula near the elytral suture around middle of elytra (Fig. 1F); penis guide longer than parameres (Figs 6B, 8A)	4
4	Body entirely rufous, sometimes with darker scutellar shield (Fig. 1G); penis guide distinctly curved in lateral view, parameres at base about as broad as in middle (Fig. 8B)	C. rufa (Herbst)
–	Body testaceous with small transverse macula at base of pronotum just above scutellar shield, scutellar shield dark, elytra with single dark brown to black, longitudinal macula on elytral suture around middle of elytra (Fig. 1F); penis guide mildly curved in lateral view, parameres at base distinctly narrower than in middle (Figs 6A, C)	C. reitteri Dodge

Coccidula lepida LeConte, 1852

Figs 1C, D, 2A–E

Coccidula lepida LeConte, 1852: 132.

Coccidula occidentalis Horn, 1895: 114.

Coccidula suturalis Weise, 1895: 132.

Material examined

United States of America: America b., 82, coll. Růžička et Vokál, (1: NMP); Alaska, Mi.1249, Alaska Hwy., Dedman Lk., 6.–7.VII.1968, Campbell & Smetana (1: NMP); Vermont, Korschefsky det. (2: MIZ); Canada: SK, Harris Reservoir, Hwy 21, 10 km S, Maple Creek, April 19 2016, drift D. Larson (1 female: NMP). Type material not studied, deposited in Museum of Comparative Zoology, Cambridge, USA.