Research Article |
Corresponding author: Krzysztof Pawlęga ( krzysztof.pawlega@up.lublin.pl ) Academic editor: Miguel Alonso-Zarazaga
© 2018 Ewelina Szwaj, Jacek Łętowski, Krzysztof Pawlęga.
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:
Szwaj E, Łętowski J, Pawlęga K (2018) The morphology of the preimaginal stages of Cleopomiarus micros (Germar, 1821) (Curculionidae, Coleoptera) and notes on its biology. ZooKeys 798: 45-62. https://doi.org/10.3897/zookeys.798.27173
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As yet little is known of the bionomics of weevils of the genus Cleopomiarus Pierce, 1919; current knowledge is limited to data on the morphology and biology of the preimaginal stages of certain species. This paper includes original information on the life cycle of Cleopomiarus micros (Germar, 1821). It presents the morphology of the egg, last larva (L3) and pupa. Data on the host plant (Jasione montana L.) and breeding plant (Campanula patula L.) and on the oviposition and phenology of the species are updated. The anatomy of the third-stage larva of C. micros shares certain traits with other species of the tribe Mecinini Gistel, 1848. Comparison of the morphology of preimaginal stages of C. micros with those previously described for other species of the genera Cleopomiarus and Miarus Schönherr, 1826 – previously considered the same genus – reveals species differences in larval body length, colour of the body and epicranium, and chaetotaxy of head and body.
Central Europe, developmental stage, host plant, mature larva, Mecinini , oligophagy, pupal stage
The tribe Mecinini Gistel, 1848 is currently represented by six genera worldwide, of which five (Cleopomiarus Pierce, 1919, Gymnetron Schoenherr, 1825, Mecinus Germar, 1821, Miarus Schoenherr, 1826 and Rhinusa Stephens, 1829) are known from the Palearctic fauna and one, Rhinumiarus Caldara, 2001, was discovered in the Neotropical realm (
The analysis of previously known adult forms and their preimaginal stages reveals a number of morphological characters common to the tribe Mecinini. In the larvae, these are as follows: head usually with 3 distinct pairs of setae (des) and with long, unbranched endocarina, which together with the epicranial suture extends 2/3 the length of the head; labial palpus usually with 1 segment – if there are 2 segments the basal segment is not distinctly separated; hypopharynx with usually 4, less often 2 or 6 epithelial anteromedial setae; premental rounded, less often pointed; sclerites of the prosternum joined or free, numbering 0, 2, 4 or 6; thoracic and abdominal spiracles uni- or bicameral depending on the genus, abdominal spiracles located laterally on the intersegmental membrane, tubes well defined from atrium (
The genus Cleopomiarus includes 40 species dispersed throughout the world. Palearctic species (19 spp) are associated with plants of the genera Adenophora Fisch., Campanula L., Jasione L. and Phyteuma L. (Campanulaceae, Campanuloideae), whereas beetles from southern Africa and Mexico live on plants of the genera Codonopsis Wall., Lightfootia L’Hér., Roella L. and Wahlenbergia Schrad. ex Roth from the same subfamily (Campanuloideae), as well as on representatives of the genus Lobelia L. from the subfamily Lobelioideae (
As yet little is known of the bionomics of insects of the genus Cleopomiarus. Certain data on the morphology and biology of preimaginal stages can be found in
In the present study the immature stages of Cleopomiarus micros are described. This is a rare, psammophilous species, found only in certain areas. It inhabits sand, dunes, ruderal communities, forest clear-cuts, and thickets. It has previously been recorded in southern, western and central Europe, as far north as northern Denmark and southern Sweden. It has also been recorded in North Africa. In the literature it has been described as a monophage living exclusively in the flowers of sheep’s bit scabious, Jasione montana L. (
The objective of the study is to describe the morphology and biology of the preimaginal stages of Cleopomiarus micros, which is one of the rarest representatives of its genus in Poland.
The material for the study consisted of developmental stages (egg, three larval instars and adult) of Cleopomiarus micros, isolated in the laboratory from plants of the genus Campanula L.: C. bononiensis L., C. glomerata L., C. patula L., C. persicifolia L., C. rapunculoides L., C. sibirica L., and C. trachelium L., as well as from Jasione montana. The plants were collected in the field in the Lublin region: Łysaków 50°45'40.96"N, 22°11'17.31"E, Podzamcze Reserve near Bychawa 51°01'24.85"N, 22°31'59.04"E, Nasutów 51°22'31.29"N, 22°31'07.32"E, Spiczyn 51°19'59.47"N, 22°44'29.63"E, Jakubowice Murowane 51°16'21.26"N, 22°38'15.52"E, Łęczna 51°18'09.7"N, 22°51'47.8"E, Ciechanki Łańcuchowskie 51°16'37.00"N, 22°55'28"E, Niedzieliska 50°41'57.07"N, 23°05'00.75"E, Kąty 50°42'21.98"N, 23°06'58.73"E, Gródek 50°46'58.18"N, 23°56'47.04"E and Czumów 50°46'28.79"N, 23°58'05.68"E. The lack of knowledge of the host plants and breeding plants of the species was the reason for the wide range of species examined from these plant genera. The selection and distribution of habitats with potential host plants were based on the results of faunistic studies in which insects of the genera Miarus and Cleopomiarus have been caught (
Adult insects were collected by hand directly from host plants and isolated from samples collected with an entomological net in 8 × 25 series at the sampling sites over the entire growing period of the plants, from May to September, on sunny days without wind, between 10:00–16:00 local time, once a month for a period of three years (2009–2011).
Part of the individual developmental stages of these insects were fixed in 70% ethyl alcohol and a part incubated (in a ratio 1:4 – ¼ to fixation, ¾ to incubation). Breeding of preimaginal stages was carried out in Petri dishes lined with filter paper, placed in a breeding chamber with constant temperature parameters (daytime minimum 25 °C, daytime maximum 35 °C, minimum at night 15 °C, maximum at night 20 °C), humidity (60%), light intensity and duration (day 16 h, night 8 h), in order to obtain all developmental stages of the beetles (egg, three larval instars, pupa and adult) and describe their biology.
Observations of the ecology of adult beetles were also conducted in the laboratory on individuals bred together with their host plants in glass insulators at 25 °C with a 14:10 photoperiod.
Two methods were used to prepare microscope slides, as described in
Egg white, transparent, teardrop-shaped, ca. 0.45 mm long, ca. 0.21 mm wide. Chorion surface smooth and shiny (120× magnification).
First larval instar (L1) – white body, slightly transparent. Body length ca. 1 mm (0.96–1.07 mm), width ca. 0.46 mm (0.42–0.51 mm). Clearly visible pale brown head ca. 0.23 mm long (0.21–0.27 mm) and ca. 0.16 mm wide (0.13–0.20 mm). Larva with sparse setae, pedal tubercles nearly imperceptible. Anterior stemmata present.
Second larval instar (L2) – creamy white body, also with sparse setae. Length body ca. 2.15 mm (2.02–2.41 mm), width ca. 1.01 mm (0.90–1.09 mm). Intersegmental grooves clearly visible, pedal lobes lightly outlined. Head pale grey, length ca. 0.4 mm (0.38–0.42 mm), width ca. 0.27 mm (0.26–0.28 mm). Anterior stemmata clearly visible.
Third larval instar (L3) – body massive, strongly curved, rounded in cross-section, creamy-white, ca. 3.41 mm long (3.12–3.73 mm) and ca. 1.51 mm wide (1.38–1.80 mm) (Figures
Mature larva (L3), lateral view: prns pronotal setae, vpls ventropleurolateral setae, pda pedal tubercle (area), ps pedal setae, lsts laterosternal setae, prs prodorsal seta, pds postdorsal setae, dpls dorsopleural setae, ss spicular setae, vpls ventropleurolateral setae, msts mesosternal seta, sts sternal setae, pls pleural setae.
Head: Oval, dark brown, ca. 0.62 mm long (0.59–0.65 mm), ca. 0.42 mm wide (0.40–0.44 mm). Frontal suture distinct, Y-shaped, touching antennae. Endocarina distinct, long, unbranched, together with epicranial suture extends 2/3 length of head (Figure
Clypeus wider than long (ca. 0.11 mm × 0.03 mm), trapezium-shaped. Anterior margin concave, 2 pairs of short, sharp, thorn-shaped microsetae (cls1,2) along posterior margin, between them sensilla (Figures
Mouthparts: Labrum more then 2× wider than long (ca. 0.06 mm × 0.02 mm), with 3 pairs of setae (lrms1-3) of varying length – lrms3 the shortest and lrm1 the longest (Figures
Labium – prementum (prms) nearly oval, with 2 pairs thorn-shaped microsetae (ligs1,2) near anterior margin and 4 pairs of hair-like micro- and macrosetae arranged in 2 rows in middle and at base (prlbs1-4). Prementum base (prmsc) rounded, weakly sclerotized. Labial palpus (lba) longer than wide with 2 segments of similar length, basal segment weakly separated from distal (Figure
Thorax: Prothorax with 7 long setae (prns) on dorsal side, 2 long ventropleurolateral setae (vpls), 7 setae on pedal tubercle (pda), including 2 micro- and 5 macrosetae – ps1-3, lsts1-4, and 1 ventral seta (msts) (Figure
Abdomen: Abdominal segments I–VII with 1 prodorsal microseta (prs), 4 (2 macro- and 2 micro-) postdorsal setae (pds), 1 spicular seta (ss), 1 dorsopleurolateral microseta (dpls), 2 ventropleurolateral setae (vpls) and 1 mesosternal seta (msts). Macrosetae clearly extend beyond outline of body and are several times longer than microsetae. Segment VIII with similar chaetotaxy as previous segment. Abdominal segment IX with 2 dorsal microsetae (pls) and 2 ventral microsetae (sts) of similar length (Figure
The female and male morphology is externally very similar at the pupal stage, with a significant difference only in the length of the rostrum, which is longer in the female and its apex extends to the middle of the second tarsal segment of the prolegs; in the male the rostrum is short and its apex extends to the end of the first segment.
Body: Length ca. 3.33 mm (2.95–3.53 mm), width ca. 1.41 mm (1.15–1.67), colour dark brown (Figures
Head: Head capsule with 2 pairs of sos. Female rostrum longer (ca. 0.68 mm), broader in middle with 1 pair brs, 2 pairs drs and 1 pair es, and extends to end of segment II of first pair of legs. All setae on rostrum short, spinescent (Figures
Pupa, lateral view: aps apical pronotal setae, lps lateral pronotal s., dps discal pronotal s., bps basal pronotal s., sos supraorbital s., brs basirostral s., drs distriostral s., es epistomal s., fes femoral s., msts mediosternal s., pls pleural s., vpls ventropleural s., pds postdorsal s., pc urogomphi (pseudocerci).
Thorax: Pronotum broad (width ca. 1.12 mm, length ca. 0.65 mm) with 5 pairs of apical pronotal setae (aps1-5), 3 pairs of lateral pronotal setae (lps1-3), 2 pairs of discal pronotal setae dps and 3 pairs of basal pronotal setae (bps1-3) (Figures
Abdomen: Tergites of abdominal segments I–VII of similar width, gradually narrowing slightly towards rear, with 4 pairs of setae pds (2 macro- and 2 micro-) arranged alternately, parallel to posterior margin of segment (Figure
Analysis of eight plant species of the family Campanulaceae revealed that Cleopomiarus micros uses Jasione montana as a food source for the imago and Campanula patula for breeding larvae. The presence of these two plants at the same habitat provides ideal conditions for the occurrence of the species (Figure
– Adult insects feed on sheep’s bit scabious (Jasione montana).
– Following copulation at the beginning of June, females choose a different plant species of the same family – spreading bellflower (Campanula patula) – to lay their eggs.
– Single eggs are laid on the wall of the ovary (seed chamber). Unlike in other beetle species of this genus, delicate traces of oviposition appear on the plant’s epiderm. To lay an egg the female uses a natural hollow on the exterior of the seed chamber, which she gently gnaws and enlarges (Figure
– The L1 larva bores a tunnel to the inside of the chamber. Subsequent larval instars (L2 and L3) eat the contents of the seed chamber. After seven days of growth the L3 larva transforms into a pale brown pupa, and after another four days into an imago. As observed, the adult leaves the seed through cracks formed during its drying prior to germination.
– One generation per year was noted in the species.
– The insect does not cause cecidia in the breeding plant.
Cleopomiarus micros (Germar, 1821): 10 mature larva 11 pupa 12 the environment of the species 13 place lay eggs on the plant breeding 14 labrum and clypeus (L3) (dorsal view): lrms labral setae, cls clypeus s. 15 apical part of the maxilla: ms microseta 16 antennae (at) 17 labial palpus (lbp).
The results of the study, the first morphological description of the preimaginal stages of the species Cleopomiarus micros, serve to verify and supplement previous scant data on the biology of the species. Previous data on the morphology of the preimaginal stages of representatives of the genus Cleopomiarus concern only C. graminis, C. hispidulus, and Miarus campanulae, which in the old taxonomic system belonged to the genus Miarus (
The morphology of the L3 larvae and pupa of C. micros does not differ from the typical characters of preimaginal stages of weevils of the tribe Mecinini (
Certain anatomical traits of C. micros are common to species of Mecinini tribe, but less frequent. As mentioned in the Introduction, the head of species of this tribe usually has 3 pairs of des. In C. micros there are 4 pairs, as in Rhinusa bipustulata (Rossi, 1792) or Gymnetron miyoshii Miyoshi, 1922 (
Comparison of the morphology of C. micros with previously described preimaginal stages (L3 and pupa) of species of the genera Cleopomiarus and Miarus (previously the same genus) on the basis of previously described features reveals species differences in larval body length, the colour of the body and epicranium, and the chaetotaxy of the head and body (
Diagnostic features of the mature larvae of Cleopomiarus micros, C. graminis, C. hispidulus and Miarus campanulae (‘-’ indicates lack of descriptive data).
Traits | Character | Cleopomiarus micros |
Cleopomiarus graminis ( |
Cleopomiarus hispidulus ( |
Miarus campanulae ( |
---|---|---|---|---|---|
Head | Epicranium | pes1-3; des1-3,5; des4 absent; les1-2; fs1-6; oc present; cls1-2 and 1 sa | – | – | – |
Antennal sensorium | slightly elongated, finger-shaped, with 4 sa | short, conical | elongated | finger-shaped | |
Mouthparts | Mandible | 2 apical teeth, incisive margin with tooth, mds1-2, 1 sa | 2 apical teeth, incisive molar edge with tooth | – | 2 apical teeth, mds1-2 |
Labrum | lrms1-3 | lrms1-3 | – | lrms1-3 | |
Epipharynx | 1 pair ams, als1, 3 pair mes, long epipharyngeal rods present | ams1-3, als1-3, 2 pair eps (mes) short epipharyngeal rods present | – | – | |
Maxilla | 1 stps, pfs1-2, 2 sa, mxp2 segments, basal with 1 sa and accessory process, apical segment with 1 sa; dms1-7 and vms1-3 | mxp2 segments, 8 maxilla setae (dms and vms) | – | mxp2 segments, maxilla setae present | |
Labium | pms1-3; premental sclerite „Y” shaped; prms1-4; ligs1-2; lbp2 segments – lbp longer then wide, basal segment with 1 sa, segments of similar length, basal segment fairly well defined | premental sclerite rounded, lbp 2 segments – lbp longer then wide, 2nd segments as long as wide, basal segment rather well defined | – | premental sclerite rounded, lbp2 segments – lbp as long as wide, 2nd segments distinctly longer then wide, basal segment not well defined | |
Thorax | Th1 | prns1-7, vpls1-2, ps1-3, lsts1-4, 1 msts | pda with 3 setae (ps1-3) | – | a few setae on dorsal plate, pda with 3 setae (ps1-3), vpls with 1 setae, 1 msts |
Th2 | 1 prs, pds1-4, 1 as, ps1-3, lsts1-4, 1msts, 1 as | pda with 3 setae (ps1-3) | – | 1 pair prs, pds1-4, ps1-3, as1-2 | |
Th3 | same as Th2 | pda with 3 setae (ps1-3) | – | same as Th2 | |
Abdomen | Abd I–VII | 1 prs, pds1-4, 1 dpls, vpls1-2, 1 msts | – | – | – |
Abd VIII | same as AbI–VII | – | – | – | |
Abd IX | ds1-2, sts1-2 | – | – | – | |
Abd X | anal x-shaped, without setae |
anal x-shaped |
anal x-shaped |
anal x-shaped |
|
Spiracles | Thorax | bicameral | bicameral | bicameral | bicameral |
Abdomen | bicameral | bicameral | bicameral | bicameral |
Differences between the species analysed were also noted in the size and colour of the pupal body. In C. micros the body is 2.95–3.53 mm long and dark brown, whereas the yellow-white pupa of C. graminis reaches a length of 3.4–5.0 mm and the body of the M. campanulae pupa is 2.5–3.0 mm long and white (
The development of the Mecinini species is correlated with the phenology of the breeding and host plants and is strongly dependent on the environmental conditions prevailing at a given site. In the case of C. micros, a necessary condition for the presence of the beetle is the co-occurrence of plants of the species Campanula patula, in which it develops, and Jasione montana, which constitutes the food base for adults. This was confirmed by the observations in the field and experiments in the laboratory. The species was not found when only one of the listed plant species was present in the environment. Among the species from genus of Miarus and Cleopomiarus so far studied, only C. micros develops in such a way – development in a one species of plant and feeding on another. This indicates that this species is oligophagous. Until now, it would have been described as a monophag (
Understanding of the morphology of the adult larva of the described species allows for the recognition of potential generic features for the labial palp of Cleopomiarus species. They are: the ratio of length to its width – the labial palp is longer than wider, the apex is clearly longer than wider, and the basic segment is pronounced. Morphological descriptions of the next species of the genera Miarus and Cleopomiarus will probably allow other generic features to be distinguished, and, in turn, for the production of a key to identify mature larvae.
The data presented herein provide new information on the biology and ecology of the species. Previous data covered only its living environment, host plant and the number of generations per year (
Diagnostic features of pupae of Cleopomiarus micros, C. graminis and Miarus campanulae (‘-’ indicates lack of descriptive data).
Traits | Cleopomiarus micros |
C. graminis ( |
Miarus campanulae ( |
|
---|---|---|---|---|
Head | sos1-2, brs1, drs1-2, es1 | – | os1-2, sos1, vs1, rs1 (drs) | |
Thorax (one side) | Pronotum | aps1-5, lps1-3, dps1-2, bps1-3 | – | as1-3(aps), ls1-2 (lps), ds1 (dps), pls1 (bps) |
Mesonotum | msns1-3 | – | 3 sas (msns) | |
Metanotum | mtns1-3 | – | 3 sas (mtns) | |
Abdomen (one side) | pds1-4, dpls1-2, | – | 4 pairs of setae | |
Legs | 1 fes | – | 1 fes | |
Pseudocerci | pointed, slightly curved | pointed, curved | pointed, massive, arched |
The authors would like to thank the English native Sara Wild –for the correction of the manuscript and Professor Bernard Staniec and Jarosław Pawelec from the Maria-Curie Skłodowska University in Lublin for the possibility of taking pictures by scanning microscopy. They also extend their gratitude to the reviewers, Dr Adriana Marvaldi and Dr Rafał Gosik, for the useful comments that helped to improve the manuscript.