Research Article |
Corresponding author: Filip Trnka ( filip.trnka88@gmail.com ) Academic editor: Miguel Alonso-Zarazaga
© 2016 Filip Trnka, Robert Stejskal, Jiří Skuhrovec.
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:
Trnka F, Stejskal R, Skuhrovec J (2016) The morphology of the immature stages of two rare Lixus species (Coleoptera, Curculionidae, Lixinae) and notes on their biology. ZooKeys 604: 87-116. https://doi.org/10.3897/zookeys.604.9018
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The mature larvae and pupae of Lixus (Ortholixus) bituberculatus Smreczyński, 1968 and L. (Dilixellus) neglectus Fremuth, 1983 (Curculionidae: Lixinae: Lixini) are described and compared with known larvae of 21 other Lixus and 2 Hypolixus taxa. The mature larva and pupa of L. bituberculatus are the first immature stages described representing the subgenus Ortholixus. The larva of L. neglectus, in the subgenus Dilixellus, is distinguished from the known larvae of four species in this subgenus by having more pigmented sclerites on the larval body. All descriptions of mature larvae from the tribe Lixini, as do all known species from the tribe Cleonini, fit the diagnosis of the mature larva of the Lixinae subfamily. Furthermore, new biological information of these species in the Czech Republic, Slovakia and Romania is provided. For L. bituberculatus, a chicory, Cichorium intybus L. (Asteraceae), is identified as a host plant, and L. neglectus is found on dock Rumex thyrsiflorus Fingerh. (Polygonaceae). Both species are probably monophagous or oligophagous. Adults of L. bituberculatus often inhabit host plants growing in active, dry and sunny pastures with sparse patches without vegetation, being mostly active during the night in April/May and then again in September, when the highest activity levels are observed. Adults of L. neglectus inhabit dry grasslands on sandy soils with host plants, being active during the day from May to September, with the highest level of activity in May/June and September. The larvae of both species are borers in the stem and root of the host plant, and they pupate in root or root neck. Adults leave the pupation cells at the end of summer and do not hibernate in the host plants. Finally, Romania is a new geographic record for L. bituberculatus.
Weevil, mature larva, pupa, larval development, life cycle, host plant, Cichorium intybus , Rumex thyrsiflorus , Central Europe, Palaearctic region
The genus Lixus Fabricius, 1801, belongs to the tribe Lixini Schoenherr, 1823 in the subfamily Lixinae Schoenherr, 1823 (family Curculionidae Latreille, 1802), and approximately 500 species have been described globally (
Lixus bituberculatus Smreczyński, 1968 belongs to the subgenus Ortholixus Reitter, 1916, which includes 18 species in the Palaearctic region (
Lixus neglectus Fremuth, 1983 belongs to the subgenus Dilixellus Reitter, 1916, which includes 31 species in the Palaearctic region (
Knowledge of the immature stages and life histories of both species is important for taxonomy as well as practical applications and can help to more effectively protect these species. In this paper, we describe the immature stages of both species and provide details of their life history based on field observations in the Czech Republic, Slovakia and Romania.
The material used to describe the immature stages was collected, and field observations were conducted in the localities mentioned below:
Lixus (Ortholixus) bituberculatus Smreczyński, 1968
Material examined. ROMANIA: Caraș-Severin County: Sfânta Elena env.; 44°40'24.1"N, 21°43'2.0"E; survey dates: 9-VI-2012, 1–2-IX-2012, 18–23-V-2013, 5-VIII-2014 (3 larvae), 6-VIII-2014 (2 larvae, 1 pupa), 8-VIII-2014 (7 larvae, 3 pupae); all leg. & det. F. Trnka, coll. J. Skuhrovec. Habitats: pastures (cattle, sheep, goats), road margins and dry grasslands. Bedrock: limestone. Altitude: 400 m a. s. l. (see Fig.
Lixus (Dilixellus) neglectus Fremuth, 1983
Material examined. CZECH REPUBLIC: Břeclav District: Lanžhot env.; 48°41'21.04"N, 16°56'3.40"E; survey date: 19-VII-2014. Habitat: dry grassland and blown sand, THG01 Potentillo heptaphyllae-Festucetum rupicolae (
Rearing and life cycle observations were conducted during the 2014–2015 vegetation growing seasons. Laboratory observations were conducted in Olomouc (49°35'36"N, 17°15'3"E) and in Znojmo, Czech Republic (48°51'31"N, 16°2'40"E).
Part of the larval and pupal material was preserved in Pampel fixation liquid (4 parts glacial acetic acid, 6 parts 4% formaldehyde, 15 parts 95% ethyl alcohol and 30 parts distilled water) and used for the morphological descriptions. These specimens are now deposited in the Group Function of Invertebrate and Plant Biodiversity in Agrosystems of the Crop Research Institute (Prague, Czech Republic). Plants were identified by the collectors. Slides were prepared following
The observations and measurements were made using a light microscope with calibrated oculars (Olympus BX 40 and Nikon Eclipse 80i), and the following characteristics were measured for each larva: head width, length of the body (larvae fixed in a C-shape were measured in segments), width of the widest part of the body (metathorax or abdominal segments I–IV).The length and width of the widest part of the body was measured for each pupa. The thorax and abdomen were not sclerotised, and it is unlikely that the fixation process altered the weevils’ proportions; measurements of these parts are given for comparison purposes only.
Drawings were made with a drawing tube on a light microscope and processed by a computer program (Adobe Photoshop, Corel Photo-Paint 11, GIMP 2). The thoracic spiracle is located on the prothorax near the boundary of the prothorax and mesothorax, as shown in the drawing (see Figs
We used the terms and abbreviations for the setae of the mature larva and pupa studied in
The count of some of the setae on the epipharynx (especially ams and mes) have not been completely resolved. According to
Measurements (in mm). Body length: 6.5–10.4 (mean 9.2). The widest part of the body (metathorax and abdominal segments I–II) measuring up to 2.8. Head width: 1.4–1.7 (mean 1.5).
General. Body stocky, slightly curved, rounded in cross section (Fig.
Colouration. Head light brown or brown with a distinct pale pattern around the frontal suture (Figs
Vestiture. Setae on body thin, relatively short, light yellow or orange.
Head capsule (Fig.
Antennae located at the end of the frontal suture on each side, membranous and slightly convex basal article bearing one conical triangular sensorium, relatively long; basal membranous article with 5 sensilla different in both shape and length (Fig.
Clypeus (Fig.
Mouth parts. Labrum (Fig.
Thorax. Prothorax distinctly smaller than meso- and metathorax. Metathorax almost of equal length as abdominal segments I–IV. Spiracle bicameral. Prothorax (Fig.
Abdomen. Abdominal segments I–IV of almost equal length, subsequent abdominal segments decreasing gradually to the terminal parts of the body. Abdominal segment X reduced to four anal lobes of unequal size, the dorsal being distinctly the largest, the lateral pair equal in size, and the ventral lobe very small. Anus located terminally. Spiracles bicameral, the eight abdominal spiracles located laterally, close to the anterior margin of abdominal segments I–VIII. Abdominal segments I–VII (Figs
Measurements (in mm). Body length: 8.0–10.4 (♂ 8.0–10.4; ♀ 9.8). The widest part of the body, commonly between the apex of the meso- or metafemora: 2.6–3.5.
Colouration. Body white to yellowish (Fig.
Morphology (Figs
Habitats, adults, immature stages and life cycle of Lixus bituberculatus. 14 Adult 15 Adult hiding in host plant rosette 16 Ovipositional mark 17 Eggs in the host plant stem 18 Feeding marks in the stem 19 Mature larva in the root crown 20 Pupa and pupation cell 21 Habitat in Romania and Cichorium intybus host plant.
Chaetotaxy (Figs
Habitats. Adults (Fig.
Adult behaviour. During the day, adults stay among the rosette leaves of the host plant (Fig.
Host plants. Adults and larvae were observed feeding on chicory Cichorium intybus L. (Asteraceae), in the studied localities (Fig.
Life cycle. Lixus bituberculatus is an univoltine species. Adults feed on leaves, but larval development occurs in the basal part of the stem and in the root (Figs
Rearing of the larvae. For laboratory breeding, 10 mature larvae were collected on August 8th, 2014, but only three pupated under our laboratory conditions. The remaining seven larvae primarily died due to drying of the host plants. The first fresh adult hatched on September 12th and the other two on September 15th, 2014.
Measurements (in mm). Body length: 10.5–13.5 (mean 12.5). The widest part of the body (metathorax and abdominal segments I–II) measuring up to 3.3. Head width: 1.8–2.1 (mean 2.0).
General. Body stocky, slightly curved, rounded in cross section (Fig.
Colouration. Head light brown or brown (Figs
Vestiture. Setae on body thin, relatively long to very long, light yellow or orange.
Head capsule (Fig.
Antennae located at the end of the frontal suture on each side, membranous and slightly convex basal article bearing one conical triangular sensorium, relatively long; basal membranous article with 3 sensilla different in both shape and length (Fig.
Clypeus (Fig.
Mouth parts. Labrum (Fig.
Thorax. Prothorax distinctly smaller than meso- and metathorax. Metathorax almost of equal length as abdominal segments I–IV. Spiracle bicameral. Prothorax (Fig.
Abdomen. Abdominal segments I–V of almost equal length and subsequent abdominal segments decreasing gradually to the terminal parts of the body. Abdominal segment X reduced to four anal lobes of unequal size, the dorsal being distinctly the largest, the lateral pair equal in size, and the ventral lobe very small. Anus located terminally. Spiracles bicameral, the eight abdominal spiracles located laterally, close to the anterior margin of abdominal segments I–VIII. Abdominal segments I–VII (Figs
Measurements (in mm). Body length: 9.4–12.7 (♂ 9.4–12.7; ♀ 10.0) and the widest part of the body, commonly between the apex of the meso- or metafemora: 2.8–3.8.
Colouration. Body yellow (Fig.
Morphology (Figs
Habitats, adults, immature stages, host plants and life cycle of Lixus neglectus. 35 Adult 36 Adult hiding in host plant rosette 37 Ovipositional mark and larva feeding marks (frass) 38 Mature larva 39 Pupa 40 Fresh, not fully coloured adult 41 Habitat in Czech Republic with host plant, Rumex thyrsiflorus 42 Detail of host plant rosette.
Chaetotaxy (Figs
Habitats. Adults live in dry grasslands and meadows with sandy substrates (wind-blown river sand) (Fig.
Adult behaviour. Adult beetles (Fig.
Host plants. Adults and their immature stages were observed exclusively on dock, Rumex thyrsiflorus Fingerh. (Polygonaceae) (Figs
Life cycle. Lixus neglectus is an univoltine species. Adults feed on leaves, and larvae are stem and root borers (Fig.
Rearing of the larvae. For laboratory breeding, 15 mature larvae were collected on July 13th, 2014, but only two of them pupated in our laboratory conditions. The remaining larvae died primarily due to drying of the host plants. Both of the adults hatched on July 30th.
Comparison with larvae of other Lixus species. To date, larvae of 21 Lixus and two Hypolixus species have been described (
The precise general description of the larvae of the genus Lixus, which can be summarized by 19 character sets, has been presented by
Differential diagnosis of mature larvae of both described species and the most similar or relative species.
L. (Dilixellus) bardanae (Fabricius, 1787) | L. (Dilixellus) desbrochersi Hoffmann, 1957 | L. (Dilixellus) neglectus Fremuth, 1983 | L. (Dilixellus) probus Faust, 1886 | L. (Dilixellus) punctiventris Boheman, 1835 | L. (Epimeces) filiformis (Fabricius, 1781) | L. (Eulixus) kiritshenkoi Ter-Minasian, 1985 | L. (Ortholixus) bituberculatus Smreczyński, 1968 | |
---|---|---|---|---|---|---|---|---|
Endocarina | unknown | present, length unknown | more than the half length of frons | short | more than the half length of frons | more than the half length of frons | more than the half length of frons | more than the half length of frons |
Number of des | unknown | 4 | 5 | 5 | 5 | 5 | 5 | 5 |
Number of fs | unknown | 5 | 5 | 3 | 5 | 5 | 5 | 5 |
Number of les | unknown | 2 | 2 | unknown | 3 | 1 | unknown | 2 |
Number of ves | unknown | 2 | 2 | unknown | 2 | unknown | unknown | 2 |
Position of lrms1-3 | in a triangle | only 2 setae | in a triangle | in a triangle | in a triangle | in a triangle | in a line | in a triangle |
Number of als | unknown | 6 | 4 | 4 | 5 | 3 | 3 (or 4) | 4 |
Number of ligs | 2 | 2 | 3 | 3 | 2 | 2 | 1 | 3 |
Number of mbs | 1 | unknown | 1 | 1 | 2 ? | 1 | 0 | 1 |
More pigmented sclerites on larval body, not only on pronotum | unknown | absent | present | absent | absent | present | absent | absent |
Number of prns | unknown | 8 | 10 | 10 | 10 | 10 | 13 | 10 |
Number of pds on Abd. seg I- VII | unknown | 5 | 5 | unknown | 6 | 6 | unknown | 6 |
Number of ds on Abd. seg IX | unknown | unknown | 3 | unknown | 6 | 2 | 3 | 4 |
Number of ps on Abd. seg IX | unknown | unknown | 2 | unknown | 3 | 2 | 1 | 3 |
Number of ts on dorsal lobe on Abd. Seg. X | unknown | unknown | 0 | 7 * | 0 | 0 | 2 * | 0 |
Number of ts on ventral lobe on Abd. Seg. X | unknown | unknown | 0 | 2 * | 0 | 0 | 2 * | 0 |
Number of ts on lateral lobe on Abd. Seg. X | unknown | unknown | 2 | 0 * | 3 | 3 (dorsoventral) | 0 * | 3 |
The biology and development of these two Lixus species are very similar as both species are stem and root (crown) borers. In the genus Lixus, root borers, such as L. (Ortholixus) angustus (Herbst, 1795); L. (Compsolixus) ochraceus Boheman, 1842; L. (Dilixellus) punctirostris Boheman, 1842; L. (Dilixellus) punctiventris Boheman, 1835; and L. (Ortholixus) vilis (Rossi, 1790) (
This is the first report of L. bituberculatus from Romania, and it probably has a larger area of distribution including Bulgaria, Hungary, Romania and Slovakia (
Lixus neglectus has been found exclusively on Rumex thyrsiflorus, but the distribution of its host plant covers the majority of Europe (
Knowledge of the immature stages and life histories of insects can help protect endangered species (including the species presented here) more effectively. The detailed descriptions of the larva and pupa and their comparison with known descriptions reported here demonstrates the possibility of identifying species in their immature stages. Future detailed biological and morphological studies can yield unique information on the factors determining host specificity in this insect group and will provide useful background information for planning efficient biocontrol of invasive plant species. The issue of using some insects as biological control agents is a key topic in both the basic and applied research on invasive plants. Our results will significantly contribute to basic research but will also have practical implications for conservation biology and/or biological control.
The study by Filip Trnka was supported by a grant from Palacký University in Olomouc (IGA_PrF_2015008) and that of Jiří Skuhrovec was supported by a grant from the Czech Ministry of Agriculture (Mze ČR) RO0416. We thank Adriana Marvaldi (Argentina) and Rafal Gosik (Poland) for commenting on the manuscript and for valuable discussions about larval and pupal chaetotaxy. We are sincerely grateful to Pavel Špryňar (Prague, Czech Republic) for notes about Rumex thyrsiflorus and to Martin Dančák (Olomouc, Czech Republic) for the identification of this species. We also thank Jiří Krátký and Jan Pelikán (both of Hradec Králové, Czech Republic) for the notes on the biology of L. bituberculatus at the Slovakian sites. The manuscript was edited for English language by American Journal Experts.