Descriptions of the mature larva and pupa of the Scaly strawberry weevil, Sciaphilus asperatus (Bonsdorff, 1785) (Coleoptera, Curculionidae, Entiminae) and observations of its biology

Rafał Gosik; Peter Sprick; Tetiana Tiahunova

doi:10.3897/zookeys.873.35922

Abstract

The mature larva of Sciaphilus asperatus is redescribed and illustrated, and the pupa is described for the first time. Supplements to the identification keys for larvae and pupae of selected Palaearctic Entiminae genera and species are given. Data on the life history, especially oviposition capacity and voltinism, of S. asperatus are provided and discussed, and the number of the six larval instars was confirmed. The economic importance of S. asperatus is briefly highlighted.

Keywords

Biology, chaetotaxy, determination, host plants, larval instar, life history, morphology, plant protection, weevils

Introduction

The weevil genus Sciaphilus Schönherr, 1823 contains five valid species: S. humeralis Desbrochers des Loges, 1902 occurs in North Africa, S. helenae Schilsky, 1912 in the Middle East, S. costulatus Kiesenwetter, 1852 and S. ebeninus Chevrolat, 1873 are known from isolated localities in Europe, while S. asperatus (Bonsdorff, 1785), the species treated in this paper, is widespread in the Western Palaearctic, Central Asia (Kazakhstan), and western Siberia (Tomsk region) (Morris 1997; Legalov 2010; Borovec 2013; Alonso-Zarazaga et al. 2017). It was recently accidentally introduced to North America (Bright and Bouchard 2008).

Species of Sciaphilus form a rather uniform group characterized in the adult stage by: (1) small body size (< 6 mm); (2) short rostrum with acute carina close to apex; (3) flat eyes; (4) long, slender antennae; (5) rounded elytra densely covered with oblong, erect and spherical adherent scales, the latter forming a more or less contrasting pattern; (6) femora with a conspicuous tooth (Hoffmann 1950; Smreczyński 1966; Freude et al. 1981). Sciaphilus asperatus (Figs 1–3) is a wingless, parthenogenetic, triploid species (Suomalainen 1969; Morris 1997). The adult is a polyphagous feeder on leaves of many herbs, shrubs and trees, mainly in the herb or even in the lower shrub layer, producing more or less characteristic notches on the leaf edge (Fig. 4). In the larval stage it feeds on the roots of plants like strawberry (Fragaria L.), cinquefoil (Potentilla L.), raspberry, blackberry (both Rubus L.), hawthorn (Crataegus L., all Rosaceae), and primrose (Primula L., Primulaceae). In the Berggarten area of Hannover-Herrenhausen it was regularly found in beds of Astilbe Buch.-Ham. ex D. Don, Tiarella L. (both Saxifragaceae), Epimedium L. (Berberidaceae) and small Rhododendron L. species (Ericaceae) (Sprick and Stüben 2012). In Lublin adults of S. asperatus were observed feeding also on Weigela florida (Bunge) DC. (Caprifoliaceae). In the laboratory, adults readily fed on a great number of plant species from more than 15 families (Willis 1964; Dieckmann 1980; Burakowski et al. 1993; Sprick and Stüben 2012), many of which may also be host plants. It is a eurytopic species reported from a large variety of biotopes, preferring rather moist and shady places. It occurs mostly in forests, bushes, fallow grassland and on river banks, but also in cultivations, like tree nurseries, parks and gardens (Koch 1992; Burakowski et al. 1993; Morris 1997; Gosik 2007; Sprick and Stüben 2012).

Figures 1–3.

Sciaphilus asperatus adult, field photographs (photograph P. Sprick).

Figure 4.

Leaves of Weigela florida with traces of feeding by adults of Sciaphilus asperatus (photograph R. Gosik).

Biology and life-cycle of Sciaphilus asperatus have been described by Willis (1964), Krause (1978), Dieckmann (1980), and Burakowski et al. (1993). Adults are observed on host plants from mid-April to the beginning of October (Dieckmann 1980). The oviposition period in the field extends from late April to the end of July. Eggs are laid in batches between adjoining surfaces which was stated by Marvaldi (1999a) to be a common oviposition type in many Entiminae genera. Willis (1964) reported egg masses of 6 to 157 eggs, while Dieckmann (1980) recorded ca. 80 eggs (several observations). In the laboratory, we observed masses of 21 and 95 eggs (Fig. 23), deposited in two or three rows and glued with a secretion between layers of filter paper, or between the paper or a leaf placed in the box as food supply and the substrate. In the field, eggs are glued between overlapping leaves, to leaf folds, leaf petioles and stems, usually close to the ground (Willis 1964). Dieckmann (1980) and Willis (1964) reported that per year a single specimen can produce up to 880 or to 1000 eggs, respectively.

The larva develops in spring and summer, and this species usually overwinters in the adult stage (Krause 1978). According to Willis (1964), a small number of newly emerged weevils lay eggs – after a rather long pre-oviposition period of 24–31 days (only 12 days in spring) – also between mid-August and the beginning of September, which approximates the life-cycle of S. asperatus to that of many other soil-dwelling weevils by the presence of overwintering adults and larvae (see Gosik et al. 2016, Gosik et al. 2019). S. asperatus pupates between June and August; pupation in the field lasts between 14 and 21 days (Willis 1964).

The economic importance of Sciaphilus asperatus is usually low, compared to that of several Otiorhynchus species. Willis (1964) reported only two cases of severe damage in commercial strawberry cultivations in Northern Ireland and concluded: “From the limited data available it appears probable that severe damage to strawberry plants by larvae of S. asperatus occurs infrequently in Northern Ireland and tends to be associated with areas of light, well-drained soil.” Alford (1999) also restricted the potential economic importance to strawberries: “Weevils from related genera [other than Otiorhynchus] (e.g. Exomias Bedel, 1883 and Sciaphilus) are also of pest status, e.g. on strawberry.” Sprick and Stüben (2012), who studied the soil-dwelling weevil fauna of many tree nurseries, garden centres and parks in Germany, also ranked this species in the category of minor economic importance: “Species that usually rarely cause damage”. In a study from North America, S. asperatus comprised nearly 10% of the total larvae in forest soils (ten sites) from the Great Lakes region in Michigan and Wisconsin (Pinski et al. 2005). S. asperatus sometimes forms rather large populations, which is possible, given its parthenogenesis and oviposition capacity, but Morris (1997) stated that this species rarely occurs in large numbers in Great Britain. In a small number of cultivations, mainly of Rosaceae herbs and preferably strawberries, it achieved large numbers and therefore pest status, too.

The morphology of immatures of Sciaphilus asperatus is still incompletely known. A piece of information on this topic is given by Emden (1950, 1952): his paper contains descriptions of spiracles and the body shape of first larval instars, as well as diagnostic characters at genus and species level. Moreover, differences between first instar larva and the mature larva are provided. But only diagrams of labrum and epipharynx of the first instar larva are presented. On the other hand, the pupa remained still unknown. On the basis of head measurements, Willis (1964) reported the presence of six larval instars in S. asperatus.

Materials and methods

Specimens examined

Eleven mature larvae; eight pupae, 11.07.2013, Hannover-Herrenhausen, Berggarten, botanical garden, collected from a bed of Waldsteinia geoides Willd. (Rosaceae).

All the larvae and pupae were collected in the field at a site where the life cycle had previously been studied using pitfall traps (see Sprick and Stüben 2012). The field work in the consecutive season was concentrated on obtaining materials for morphological study. The mature larva and pupa were described, whereas the first instar larva was used only for measurement purposes in order to ascertain the number of developmental stages (see for example Sprick and Gosik 2014 or Gosik et al. 2019). Immature stages were preserved in 75% ethanol and used for measurements and morphological descriptions.

Slide preparation basically followed May (1994). The larvae selected for study under the microscope were cleared in 10% potassium hydroxide (KOH), then rinsed in distilled water and dissected. After clearing, head, mouthparts and body (thoracic and abdominal segments) were separated and mounted on permanent microscope slides in Faure-Berlese fluid (50 g Gum Arabic and 45 g chloral hydrate dissolved in 80 g of distilled water and 60 cm³ of glycerol) (Hille Ris Lambers 1950). The specimens and slides are deposited in the collections of the Department of Zoology, Maria Curie-Skłodowska University (Lublin, Poland).

The study was conducted using a light compound microscope (Ampliwal) with calibrated oculars and a drawing tube (MNR–1). Drawings and outlines were processed by computer software (Corel Photo-Paint X6, Corel Draw X6). The photographs were taken with an Olympus BX63 microscope and processed by Olympus cellSens Dimension software. We follow the chaetotaxy nomenclature proposed by Anderson (1947), Scherf (1964), May (1994), Marvaldi (1997, 1998, 1999b, 2003) and Skuhrovec et al. (2015), with the antennae terminology following Zacharuk (1985).

Morphological abbreviations

Larva

Abd. 1–10 abdominal segments 1–10,

at antenna,

clss clypeal sensorium,

st stemmata,

Se sensorium,

sa sensillum ampullaceum,

sb sensillum basiconicum,

sc sensilla cluster,

lr labral rods,

als anterolateral seta,

ams anteromedial seta,

as alar seta,

cls clypeal seta,

des dorsal seta,

dms dorsal malar seta,

ds dorsal seta,

eps epipleural seta,

eus eusternal seta,

fs frontal seta,

les lateral epicranial seta,

ligs ligular seta,

lrs labral seta,

ls lateral seta,

lsts laterosternal seta,

mbs malar basiventral seta,

mds mandibular seta,

mes median seta,

mps maxillary palp seta,

pda pedal seta,

pds postdorsal seta,

pes postepicranial seta,

pfs palpiferal seta,

pms postlabial seta,

prms prelabial seta,

prns pronotal seta,

prs prodorsal seta,

ps pleural seta,

ss spiracular seta,

stps stipal seta,

sts sternal seta,

ts terminal seta,

Th. 1–3 thoracic segments 1–3,

vms ventral malar seta.

Pupa

as apical seta,

d dorsal seta,

ds discal seta,

es epistomal seta,

fes femoral seta,

os orbital seta,

pas postantennal seta,

rs rostral seta,

sls superlateral seta,

sos superorbital seta,

ss spiracular seta,

ur urogomphi,

v ventral seta,

vs vertical seta.

Results

Description of the mature larva

All data in [mm], (ⁿ: number of exemplars).

First instar larvae: Head width 0.224¹, 0.230¹.

Mature larvae: Head width 1.05¹, 1.10⁵, 1.15³, 1.17²; body length: 3.50¹, 4.00²; 4.50¹, 5.00², 5.50², 6.00³; body width: 1.50⁵, 1.75², 2.00⁴.

Body (Figs 5–9) slender, slightly curved, rounded in cross section. Prothorax slightly bigger than mesothorax; metathorax as wide as mesothorax. Abdominal segments 1–6 of almost equal length; segments 7–9 tapering gradually to the terminal parts of the body; segment 10 reduced to four anal lobes of unequal size: the biggest dorsal, the smallest ventral, both lateral equal in size. Spiracle of thorax bicameral, and of abdominal segments 1–8 annular. Chaetotaxy well developed, setae capilliform, variable in length, light yellow. Each side of prothorax with nine prns of unequal lengths: one long, three moderately long, five short or minute (seven of them placed on pronotal sclerite, next two close to spiracle); two ps (one long, one medium); and one very short eus. Meso- and metathorax (Fig. 5) on each side with one short prs, four pds, variable in length (pds₁, pds₃ and pds₄ medium, pds₂ relatively short), one medium as, one medium and one minute ss, one medium eps, one medium ps, and one short eus. Each pedal area of thoracic segments with six pda, variable in length (seta “z” invisible). Abd. 1–7 (Figs 7–9) on each side with one short prs, five pds, variable in length (pds₁, pds₃, and pds₅ very long, pds₂ and pds₄ very short) and arranged along the posterior margin of each segment, one minute and one long ss, one minute and one long eps, one minute and one medium ps, one short lsts and two short eus. Abd. 8 (Figs 7–9) on each side with one short prs, three pds, variable in length (pds₁ and pds₃ very long, pds₂ very short) and arranged along the posterior margin of the segment, one minute ss, one minute and one long eps, one minute and one medium ps, one short lsts and two short eus. Abd. 9 (Figs 7–9) on each side with three ds (ds₁ and ds₃ very short, ds₂ long), all located close to the posterior margin of the segment, one short and one long ps and two short sts. Each lateral anal lobe (Abd. 10) with a pair of minute ts.

Figures 5–9.

Sciaphilus asperatus mature larva, habitus and chaetotaxy. 5 Thoracic segments, lateral view 6 First abdominal segment, lateral view 7 Abdominal segments 7–10, lateral view 8 Abdominal segments 7–10, ventral view 9 Abdominal segments 6–10, dorsal view. Abbreviations: Th. 1–3 – thoracic segments 1–3, Abd. 1–10 – abdominal segments 1–10, setae: as – alar, ps – pleural, eps – epipleural, ds – dorsal, lsts – laterosternal, eus – eusternal, pda – pedal, pds – postdorsal, prns – pronotal, prs – prodorsal, ss – spiracular, sts – sternal, ts – terminal.

Head (Fig. 10) light to dark yellow with some dark, vertical stripes, suboval, slightly narrowed bilaterally; frontal suture distinct, Y-shaped, endocarina absent. Setae on head capilliform. Des_{1, 2, 3, 5} equal in length; des₁ and des₂ located in centre of epicranium, des₃ placed on frontal suture, des₄ absent, des₅ located anterolaterally. Fs_{4, 5} equal in length, fs₄ located anteromedially, fs₅ anterolaterally, close to epistoma. Les₁ and les₂ equal in length, as long as des₁. Postepicranial area with four very short pes. A pair of small stemmata (st_{1, 2}) located anterolaterally on each side of head, variable in size. Antennae (Fig. 11) inserted at end of frontal suture; antennal segment membranous with cushion–like, relatively short Se, located medially and with seven sensilla of different types: two sa and five sb. Labrum (Fig. 12) semicircular, anterior margin smooth; three pairs of lrs equal in length; lrs₁ and lrs₂ placed medially, lrs₃ laterally. Clypeus (Fig. 12) trapezoid, anterior margin of clypeus gently arcuate inwards; two pairs of cls strongly reduced, vestigial, located posteromedially; clss clearly visible, placed medially between cls. Epipharynx (Figs 13, 14) with three pairs of rod-shaped als of almost equal length; two pairs of ams rod-shaped, variable in size, both distinctly shorter than als; 2 pairs of rod-shaped mes of almost equal length: the first pair placed medially, the second pair anteriorly, very close to ams. There is a pair of sensilla clusters (sc) close to mes₂. Labral rods elongate, curved outwards (both form a shape close to “Y”). Anterior margin of epipharynx smooth, medial part serrate due to presence of thorn-like asperities placed between labral rods. Labral rods rather short, slightly converging posteriorly. Mandibles (Figs 15–17) distinctly curved, narrow, with divided apex (teeth variable in length). A protruding additional tooth on the cutting edge between apex and middle of mandible; single mds capilliform, medium long. Maxilla (Figs 18, 19) with one long stps and two pfs of equal length; mala with seven finger-like dms, variable in size, and four vms (Figs 15, 16); vms rod-like, variable in length, always shorter than dms; mbs very short. Maxillary palpi with two palpomeres, basal with short mps; distal palpomere apically with a group of sensilla, each palpomere with a pore. Basal palpomere distinctly wider and longer than distal, basal to distal length ratio: 1.5:1. Prelabium (Fig. 18) almost rounded with one very long prms, located medially. Ligula with two pairs of capilliform ligs of variable length. Premental sclerite clearly visible, trident-shaped, its posterior extension truncated, expanded at apex. Labial palpi two-segmented; apex of distal palpomere with some sensilla; each palpomere with a pore. Basal palpomere wider and distinctly longer than distal, basal to distal length ratio: 2:1. Postlabium (Fig. 18) with three capilliform pms, the first pair located proximally, the second medially, and the third laterodistally; pms₁ short, pms₂ and pms₃ very long.

Figure 10, 11.

10 Sciaphilus asperatus mature larva, head, frontal view. Abbreviations: at – antenna, st – stemmata, setae: des – dorsal epicranial, fs – frontal, les – lateral epicranial, pes – postepicranial, ves – ventral 11 Sciaphilus asperatus mature larva, right antenna. Abbreviations: se – sensorium, sa – sensillum ampullaceum, sb – sensillum basiconicum.

Figures 12–19.

12 Sciaphilus asperatus mature larva, clypeus and labrum. Abbreviations: clss – clypeal sensorium, setae: cls – clypeal, lrs – labral 13 Sciaphilus asperatus mature larva, epipharynx. Abbreviations: lr – labral rods, setae: als – anterolateral, ams – anteromedial, mes – median 14 Sciaphilus asperatus mature larva, epipharynx (magnification 200×). Abbreviations: lr – labral rods, sc– sensilla cluster, setae: als – anterolateral, ams – anteromedial, mes – median 15–17 Sciaphilus asperatus mature larva, right mandible 15 Lateral view 16 Dorsal view 17 Ventral view. Abbreviations: mds – mandibular seta 18, 19 Sciaphilus asperatus mature larva, body parts 18 Maxillolabial complex, ventral aspect 19 Right maxilla, ventral aspect. Abbreviations: dms – dorsal malar, ligs – ligular, mbs – malar basiventral, mps – maxillary palp, pfs – palpiferal, prms – prelabial, pms – postlabial, stps – stipal, vms – ventral malar.

Description of the pupa

All data in [mm].

Body length: 4.00², 4.75¹, 5.25¹, 5.50⁴; body width: 3.00³, 3.25², 3.50³.

Head width: 1.20⁴, 1.24².

Body moderately slender, straight, whitish. Cuticle densely covered with asperites. Rostrum short, 1.3 times as long as wide, extended beyond procoxae. Antennae relatively long and slender. Pronotum almost 2.0 times as wide as long. Abdominal segments 1–3 of almost equal length, segments 4–6 tapering gradually, 7 semicircular, 8 smaller than previous segments, 9 strongly reduced. Urogomphi short, conical, slightly sclerotized at apex (Figs 20–22).

Chaetotaxy well developed, setae of various lengths and shapes: on head (except vs), rostrum and mandibular thecae, capilliform, straight; on dorsal parts of thoracic (except ls) and abdominal segments, thorn-like. Setae yellowish to brownish, usually located on visible protuberances. Head capsule and rostrum with one pair of vs, two pairs of sos, os, pas, three pairs of rs, and two pairs of es. Vs thorn-like, medium-sized; all sos, os, pas and rs medium long, straight, equal in length; es and mts straight, very short (Fig. 20). Pronotum with two pairs of as, ls, ds, pls, and three pairs of sls. Only ls and sls₃ thin, capilliform, remaining setae thorn-like, placed on distinct protuberances. Sls₂ and sls₃ growing together on a single protuberance (Fig. 22).

Meso- and metathorax each with five pairs of rather small setae forming a line medially. Abdominal segments 1–7 each with 4 pairs of thorn-like ds (placed along posterior margin), and 2 minute, capilliform ls. Dorsal setae on abdominal segments 1 and 2 small, equal in length, on next segments increasing gradually in size; segment 8 with two pairs of minute, capilliform ls, two minute, capilliform vs, and three pairs of ds: first and second thorn-like, third capilliform, ds₂ and ds₃ growing together on a single protuberance; segment 9 with two pairs of minute, capilliform vs, next two with minute setae on each urogomphus (Fig. 22). Apex of femora with 2 fes; fes₁ long, straight, fes₂ short, thorn-like, both placed on protuberances (Figs 20–22).

Figures 20–22.

Sciaphilus asperatus pupa. 20 Ventral view 21 Dorsal view 22 Lateral view. Abbreviations: Th. 1–3 – pro-, meso- and metathorax, Abd. 1–9 – abdominal segments 1–9, ur – urogomphus, setae: as – apical, d – dorsal, ds – discal, es – epistomal, fes – femoral, l, ls – lateral, mts – mandibular theca, os – orbital, pas – postantennal, pls – posterolateral, rs – rostral, sls – superlateral, sos – superorbital, v – ventral, vs – vertical.

Discussion

Sciaphilus asperatus is a common species. Biology and life cycle are in general well known. However, some special aspects of development, such as number of larval instars, voltinism and oviposition capacity have to be discussed herein. Some differences in chaetotaxy between S. asperatus and selected genera from Entiminae are also discussed. Finally, larva and pupa are integrated in current determination keys.

Figures 23–26.

Sciaphilus asperatus immature stages from the laboratory (eggs, L₁ larvae) and from the field (mature larvae, pupae). 23 Eggs 24 First instar larvae 25 Mature larvae and pupae 26 Pupae (photograph P. Sprick).

Larval instar determination

Willis (1964) reported six larval instars, but the diagram on which the results of his measurements are based shows only five. He provides measurement data for 377 larvae. We checked this using the method of Sprick and Gosik (2014) or Gosik et al. (2019): see Tables 1, 2.

The data listed in Table 1 show that the mean values are very close for L₁ larvae: 0.277 mm (our data) and 0.233 mm according to Emden (1952). In mature larvae the range is a little larger but also quite close: 1.117 mm (our data) and 1.215 mm (Emden 1952). The HW of six measured pupae lies within this range. These are the best pre-conditions for larval instar determination (Table 2). The tested Growth Factor (GF) values are around 1.40, as in some other species (see for example Sprick and Gosik 2014 or Gosik et al. 2019).

From Table 2 it can be inferred that larval growth is rather slow: the best approximation in both cases is achieved with GF values < 1.4: 1.37 – 1.38 (1.375) from our own data and 1.39 – 1.40 (1.391) from the data of Emden (1952). These values are much smaller than in Tanymecus (Gosik et al. 2019), where GF values ranged between 1.44 and 1.45. Furthermore, it is immediately obvious that Sciaphilus asperatus has six larval instars and that the indefinite larvae of Emden (1952) (Table 1) belong to the 4^th larval instar.

Table 1.

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Head width data in Sciaphilus asperatus immatures.

Instar	Data [mm]	Mean value (x̅) [mm]	Source
L₁	0.22, 0.23, 0.25	0.233	Emden (1952)
L₁	0.224, 0.23	0.227	own data
Indefinite instar	0.6, 0.67	0.635	Emden (1952)
Mature larvae	1.17, 1.26, 1.38, 1.41	1.215	Emden (1952)
Mature larvae	1.05, 5× 1.10, 3× 1.15, 1.17	1.117	own data
Pupa	4× 1.20, 2× 1.24	1.213	own data

Table 2.

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Larval instar and Growth Factor determination in Sciaphilus asperatus.

Larval instar	GF values to be tested: 1.37/1.38/1.39/1.40/1.43	GF values to be tested: 1.37/1.38/1.39/1.40/1.43
L₁ (measured)	0.227 ¹⁾	0.233 ²⁾
L₂ (calculated)	0.311/0.313/0.316/0.318/0.325	0.319/0.322/0.324/0.326/0.333
L₃ (calculated)	0.426/0.432/0.439/0.445/0.464	0.437/0.444/0.450/0.457/0.476
L₄ (calculated)	0.584/0.597/0.610/0.623/0.664	0.599/0.612/0.626/0.639/0.681
L₅ (calculated)	0.800/0.823/0.847/0.872/0.949	0.821/0.845/0.870/0.895/0.974
L₆ (calculated)	1.096/1.136/1.178/1.221/1.357	1.124/1.166/1.209/1.253/1.393
Mature larvae (measured)	1.117	1.215

Oviposition capacity

Some data are available regarding the egg-laying capacities of Sciaphilus asperatus. According to Emden (1952), the volume of a female’s abdomen is 277 times that of a single egg. In actual fact, however, the available space must be less because of the space requirements of the digestive system, the ovipositor, viscose fluids, bordering structures and others. The highest recorded egg mass was 157 eggs per oviposition event (Willis 1964).

Willis (1964) and Dieckmann (1980) respectively reported ca. 880 and 1000 eggs laid by a single female during one season. But these data are from (or probably from) weevils maintained in the laboratory. The data relating to weevils maintained under outdoor conditions by Willis (1964) resulted in lower values of 450 to 700 eggs per female. If the pre-oviposition period lasts around 10 days (see Willis 1964), there could be 12 egg deposition events between mid-April and the end of July. If this is right, 38 to 60 eggs could be laid per oviposition event under outdoor conditions.

Generations and voltinism

According to the data presented by Krause (1978) and Dieckmann (1980), Sciaphilus asperatus should be a univoltine species: overwintered adults produce eggs, larvae hatch in spring and summer, pupation takes place in summer, and adult weevils of the new generation emerge also in summer. But Burakowski et al. (1993) reported that a small part of the new generation lays eggs in August, producing larvae that overwinter. Moreover Willis (1964) presumed that usually all larvae overwinter. This hypothesis has still to be checked. It appears equally possible that larvae from eggs laid early in the season develop in the same year as is true for many other soil-dwelling weevils (see for example Gosik et al. 2016, Gosik and Sprick 2017).

A species that develops within one season is univoltine, whereas a species that needs longer than one year for its development is semivoltine. Neither definition fits S. asperatus or many other soil-dwelling weevils. Apparently, there is a mix of univoltine summer development, and univoltine or semivoltine (if development of the overwintering larvae should last longer than one year) autumn/spring development; in winter there is not usually any development. It seems these definitions are hard to apply to soil-dwelling weevils, as they do not fit the facts very well.

Remarks on chaetotaxy

There are only several small discrepancies between the description of the mature larva given by Emden (1952) and those presently described: e.g. Emden reported two mandibular setae (one prominent and next very small), whereas we observed only a single seta. It is possible that the second (very small) mds visible on the first instar larva was torn off during intensive feeding of the mature larva. Emden (1952) reported on the presence of seven setae on the pedal area of the prothorax, the seventh a minute seta (“z”), and three further minute setae of each lateral anal lobe. We noticed only six setae on each pedal lobe and only two pairs of minute terminal setae on the lateral lobes of the tenth segment.

It is worth stressing that the presently described mature larva of S. asperatus possesses exactly all essential characters listed by Marvaldi (1998) for Entiminae larvae, Type “A”, namely: single as; setae mes₁ close together whereas setae mes₂ placed far one another; mes₂ placed close to ams; sensilla cluster placed between mes₂; labral rods curved outwards; premental sclerite trident-shaped, with posterior extension truncate, expanded at apex.

Supplement to the key to selected genera and tribes of Palaearctic Entiminae larvae

Based on Gosik et al. (2016), Gosik and Sprick (2017), Gosik et al. (2017), and Gosik et al. (2019): in Graptus, Peritelus, and Sciaphilus the key is based on one species each (G. triguttatus triguttatus, P. sphaeroides, and S. asperatus).

(Previous step as in Gosik et al. 2019)

2	Abdominal segment 10 reduced to three lobes; clypeus always with well-developed median furrow; meso- and metathorax each with single ss (sps)	*Sitonini (Andrion, Charagmus, Coelositona, Sitona)*
(next steps as in Gosik and Sprick 2017)
–	Abdominal segment 10 reduced to four lobes; clypeus smooth; meso- and metathorax each with 2–3 ss (sps)	2a
2a	All spiracles (thoracic and abdominal) bicameral	Otiorhynchus (Otiorhynchini)
(next steps as in Gosik et al. 2016)
–	At least abdominal spiracles annular	2b
2b	Meso- and metathorax with 3 ss each, Se conical	Graptus (Byrsopagini)
–	Meso- and metathorax with 2 ss each, Se cushion-like	2c
2c	Head unicolour. All spiracles annular. Each pedal area with 4 pda, abdominal segment 8 with 4 prs; abdominal segment 9 with 4 ds	Peritelus (Peritelini)
–	Head with faint stripes. Thoracic spiracles bicameral, abdominal annular. Each pedal area with 6 pda, abdominal segment 8 with 3 prs; abdominal segment 9 with 3 ds	Sciaphilus (Sciaphilini)
3	All spiracles (thoracic and abdominal) bicameral; head oval	Strophosoma (Brachyderini)
(next steps as in Gosik et al. 2017)
–	All spiracles (thoracic and abdominal) annular; head narrowed bilaterally	Philopedon (Cneorhinini), Tanymecus (Tanymecini)
(next steps as in Gosik et al. 2019)

Upgrade to the key to pupae of selected Palaearctic Entiminae genera and tribes by Gosik and Sprick (2013)

(Previous steps as in the original key)

9	Pronotal and abdominal setae thorn-like, inserted on elongate protuberances	Sciaphilini Sharp, 1891
9a	Body length in both sexes < 4.75 mm, head with 1 pair of os, rostrum with 4 pairs of rs, mandibular thecae without setae; as₁ distinctly smaller than as₂, pronotum with 1 pair of ls and 2 pairs of sls; each abdominal segment 1–7 with 3 pairs of setae, fes₁ and fes₂ equal in length	Exomias Bedel, 1883 (= Barypeithes Du Val, 1854, in part)
9b	Body length of females up to 5.50 mm (usually > 4.75 mm), head with 2 pairs of os, rostrum with 3 pairs of rs, mandibular thecae with 1 pair of mts, as₁ and as₂ equal in size, pronotum with 2 pairs of ls and 3 pairs of sls, each abdominal segment 1–7 with 4 pairs of setae, fes₁ distinctly bigger than fes₂	Sciaphilus Schönherr, 1823

Taking into consideration the shape, number, and distribution of setae, and the general body shape, the pupae of Sciaphilus asperatus and of Exomias pellucidus (Boheman, 1834) are very similar (see Gosik and Sprick 2013). Especially due to hair-like setae on head and rostrum and to thorn-like setae on pronotum and abdomen, which are observed on both species as well as the presence of paired sls growing on single protuberances and the absence of ventral setae on abdominal segments 1–7. This morphological information is coherent with the close systematic position of both species in the tribe Sciaphilini.

Acknowledgements

We would like to express our cordial thanks to Dr Adriana Marvaldi (Buenos Aires) for her very constructive and helpful comments on the manuscript. We express our sincere thanks to Peter Senn (Gdynia) for his linguistic correction of the text. The biology part of this study was supported by the German Federal Agency for Agriculture and Food (BLE, Bonn) and developed from the soil-dwelling weevils project of the Curculio Institute (CURCI).

References

Alford DV (1999) A Textbook of Agricultural Entomology. Wiley-Blackwell, London, 320 pp.

Alonso-Zarazaga MA, Barrios H, Borovec R, Bouchard P, Caldara R, Colonnelli E, Gültekin L, Hlaváč P, Korotyaev B, Lyal CHC, Machado A, Meregalli M, Pierotti H, Ren L, Sánchez-Ruiz M, Sforzi A, Silfverberg H, Skuhrovec J, Trýzna M, Velázquez de Castro AJ, Yunakov NN (2017) Cooperative Catalogue of Palaearctic Coleoptera. Curculionoidea. Sociedad Entomológica Aragonesa, Monografias electrónicas SEA, 8. http://www.sea-entomologia.org [10 November 2017]

Anderson WH (1947) A terminology for the anatomical characters useful in the taxonomy of weevil larvae. Proceedings of the Entomological Society of Washington 49(5): 123–132.

Borovec R (2013) Curculionidae: Entiminae: Sciaphilini In: Löbl I, Smetana A, Catalogue of Palaearctic Coleoptera. Vol. 8. Curculionoidea II. Brill; Leiden, Boston, 377–386.

Bright DE, Bouchard DP (2008) Weevils of Canada and Alaska. Volume 2. Coleoptera, Curculionidae, Entiminae. The Insects and Arachnids of Canada, Part 25. National Research Council of Canada, NRC Research Press, Ottawa, Canada, 327 pp.

Burakowski B, Mroczkowski M, Stefańska J (1993) Chrząszcze (Coleoptera) Ryjkowce – Curculionidae, Catalogus faunae Poloniae 23, 306 pp.

Dieckmann L (1980) Beiträge zur Insektenfauna der DDR: Coleoptera – Curculionidae (Brachycerinae, Otiorhynchinae, Brachyderinae). Beiträge zur Entomologie 30(1): 145–310.

Emden FI Van (1950) Eggs, egg-laying habits and larvae of short-nosed weevils. Eighth International Congress of Entomology, Stockholm 1948: 365–372.

Emden FI Van (1952) On the taxonomy of Rhynchophora larvae: Adelognatha and Alophinae (Insecta: Coleoptera). Proceedings of the Zoological Society of London 122(3): 651–795. https://doi.org/10.1111/j.1096-3642.1952.tb00248.x

Freude H, Harde K, Lohse G (1981) Die Käfer Mitteleuropas. Band 10 (Bruchidae, Anthribidae, Scolytidae, Platypodidae, Curculionidae). Goecke & Evers. Krefeld, 310 pp.

Gosik R (2007) Ryjkowcowate, Col., Curculionoidea zebrane do pułapek lepowych przeciwko szrotówkowi kasztanowcowiaczkowi Cameraria ohridella Deschka & Dimić. Chrońmy Przyrodę Ojczystą 63(5): 3–18.

Gosik R, Sprick P (2013) Morphology and identification of the pupae of several species of soil-dwelling broad-nosed weevils from Central Europe (Coleoptera, Curculionidae, Entiminae). Zootaxa 3731(4): 445–472. Incl. Erratum: Zootaxa 3745(2): 299–300. https://doi.org/10.11646/zootaxa.3731.4.2

Gosik R, Sprick P (2017) Description of the larvae and pupae of eight species of the tribe Sitonini Gistel, 1848 (Coleoptera, Curculionidae) from Central Europe. Zootaxa 4324(3): 401–435. https://doi.org/10.11646/zootaxa.4324.3.1

Gosik R, Sprick P, Czerewko K (2017) Morphology of the larvae of three Central European Strophosoma Billberg, 1820 (Coleoptera, Curculionidae, Entiminae) species. Deutsche Entomologische Zeitschrift 64: 27–42. https://doi.org/10.3897/dez.64.11446

Gosik R, Sprick P, Morris MG (2019) Descriptions of immature stages of four species of the genera Graptus, Peritelus, Philopedon, and Tanymecus and larval instar determination in Tanymecus (Coleoptera, Curculionidae, Entiminae). ZooKeys 813: 111–150. https://doi.org/10.3897/zookeys.813.30336

Gosik R, Sprick P, Skuhrovec J, Deruś M, Hommes M (2016) Morphology and identification of the mature larvae of several species of the genus Otiorhynchus (Coleoptera, Curculionidae, Entiminae) from Central Europe with an update of the life history traits. Zootaxa 4108(1): 1–67. https://doi.org/10.11646/zootaxa.4108.1.1

Hille Ris Lambers D (1950) On mounting aphids and other soft-skinned insects. Entomologische Berichten 13: 55–58.

Hoffmann A (1950) Coléoptères curculionides (Première partie). Paris: Lechevalier. Faune de France 52: 1–486.

Koch K (1992) Die Käfer Mitteleuropas. Vol. 3 (Ökologie). Goecke & Evers, Krefeld: 380 pp.

Krause R (1978) Untersuchungen zur Biotopbindung bei Rüsselkäfern der Sächsischen Schweiz. Entomologische Abhandlungen 42: 1–210.

Legalov AA (2010) Annotated checklist of species of superfamily Curculionoidea (Coleoptera) from Asian part of the Russia. Amurian Zoological Journal 2: 93–132.

Marvaldi AE (1997) Higher level phylogeny of Curculionidae (Coleoptera: Curculionoidea) based mainly on larval characters, with special reference to broad-nosed weevils. Cladistics 13: 285–312. https://doi.org/10.1111/j.1096-0031.1997.tb00321.x

Marvaldi AE (1998) Larvae of Entiminae (Coleoptera: Curculionidae): tribal diagnoses and phylogenetic key, with a proposal about natural groups within Entimini. Entomologica Scandinavica 29: 89–98. https://doi.org/10.1163/187631298X00212

Marvaldi AE (1999a) Eggs and oviposition habits in Entimini (Coleoptera: Curculionidae). The Coleopterists Bulletin 53(2): 115–126.

Marvaldi AE (1999b) Morfología larval en Curculionidae. Acta zoológica Lilloana 45: 7–24. https://doi.org/10.1163/187631298x00212

Marvaldi AE (2003) Key to larvae of the South American subfamilies of weevils (Coleoptera, Curculionoidea). Revista Chilena de Historia Natural 76: 603–612. https://doi.org/10.4067/S0716-078X2003000400005

May BM (1994) An introduction to the immature stages of Australian Curculionoidea. In: Zimmerman EC (Ed.) Australian weevils. Volume II: Brentidae, Eurhynchidae, Apionidae and a chapter on the immature stages by Brenda May. CSIRO Publications, Melbourne, Victoria, 365–728.

Morris MG (1997) Coleoptera: Curculionidae (Entiminae). Broad-nosed weevils. Royal Entomological Society of London. Handbooks for the identification of British weevils 5, part 17a: 1–106.

Pinski RA, Mattson WJ, Raffa KF (2005) : Composition and seasonal phenology of a nonindigenous root-feeding weevil (Coleoptera: Curculionidae) complex in northern hardwood forests in the Great Lakes region. Environmental Entomology 34(2): 298–307. https://doi.org/10.1603/0046-225X-34.2.298

Scherf H (1964) Die Entwicklungsstadien der mitteleuropäischen Curculioniden (Morphologie, Bionomie, Ökologie). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 506: 1–335.

Skuhrovec J, Gosik R, Caldara R, Košťál M (2015) Immatures of Palaearctic species of the weevil genus Sibinia (Coleoptera, Curculionidae): new descriptions and new bionomic data with suggestions on their potential value in a phylogenetic reconstruction of the genus. Zootaxa 3955(2): 151–187. https://doi.org/10.11646/zootaxa.3955.2.1

Smreczyński S (1966) Ryjkowce (Curculionidae). Podrodziny: Otiorhynchinae, Brachyderinae. Klucze do oznaczania owadów Polski 19: 1–130.

Sprick P, Gosik R (2014) Biology and morphology of the mature larva of Mitoplinthus caliginosus (Curculionidae, Molytinae). – SNUDEBILLER: Studies on taxonomy, biology and ecology of Curculionoidea 15, No. 229, CURCULIO-Institute, Mönchengladbach, 10 pp. https://www.curci.de/?beitrag=229

Sprick P, Stüben PE (2012) Rüsselkäfer in anthropogenen Lebensräumen. With 1318 coloured photos, 60 maps und 100 plates, 170 pp. [in German] – SNUDEBILLERextra (CD Rom), Curculio-Institute, Mönchengladbach.

Suomalainen E (1969) Evolution in parthenogenetic Curculionidae. Evolutionary Biology 3: 261–296.

Willis RJ (1964) The bionomics and larval morphology of the otiorrhynchid pests of soft fruit crops. – Thesis, The Queen’s University of Belfast, Northern Ireland, 250 pp, appendix 60 pp.

Zacharuk RY (1985) Antennae and Sensilla. In: Kerkut GA, Gilbert LI (Eds) Comprehensive Insect Physiology, Chemistry and Pharmacology, 6. Pergamon Press, Oxford, 1–69.