Research Article |
Corresponding author: Masoumeh Shayanmehr ( shayanm30@yahoo.com ) Academic editor: Louis Deharveng
© 2017 Adrian Smolis, Masoumeh Shayanmehr, Nataliya Kuznetsova, Elham Yoosefi Lafooraki.
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:
Smolis A, Shayanmehr M, Kuznetsova N, Lafooraki EY (2017) Three new remarkable species of the genus Endonura Cassagnau, 1979 from the Middle East and Central Asia (Collembola, Neanuridae, Neanurinae, Neanurini). ZooKeys 673: 135-151. https://doi.org/10.3897/zookeys.673.12084
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New species belonging to the genus Endonura is described and illustrated in detail. Endonura longirostris sp. n., from northern Iran, is distinctive due to an exceptionally elongate buccal cone compared to that of most other species of the genus. Other characteristic features of the species are the white body with pigmented eyes, a reduced chaetotaxy of the lateral part of the head, the thorax II–III and abdomen I–III with free chaetae De2 and 3, and abdomen IV with particularly short chaetae Di1. The main characteristics of Endonura paracentaurea sp. n. include a white body with dark pigmented eyes, a nonogival labrum, the presence of tubercles Di on the first thoracic segment and of microchaetae on the rudimentary furca. Endonura turkmenica sp. n. can be recognized by its bluish-grey body, labral chaetotaxy, free chaetae E on the head, and notably short chaetae De3 on the thorax and the abdomen. Short remarks on the possible importance of labral modifications are also provided.
Feeding habits, Iran, labral modifications, springtails, taxonomy, Turkmenistan
Amongst springtails, primitive and wingless insects, the subfamily Neanurinae is one of the most diversified, widespread, and species-rich systematic units and evolutionary lineages. Up to date, Neanurinae encompasses nearly 800 species, classified into six tribes (
In 2008, the first author redefined Endonura as follows (
The examination of rich materials of Neanurinae from northern Iran and Turkmenistan has revealed three unknown species of the genus. One of them seems to be particularly remarkable because of an exceptionally elongated and pointed labrum. Descriptions of all the three taxa are provided with comments on their affinities and the significance of labral modifications in the taxonomy and ecology of the genus and the subfamily Neanurinae.
Terminology and layout of the tables used in the paper follow
General morphology:
Abd abdomen,
Ant antenna,
AOIII sensory organ of antennal segment III,
Cx coxa,
Fe femur,
Scx2 subcoxa 2,
T tibiotarsus,
Th thorax,
Tr trochanter,
VT ventral tube.
Groups of chaetae:
Ag antegenital,
An chaetae of anal lobes,
ap apical,
ca centroapical,
cm centromedial,
cp centroposterior,
d dorsal,
Fu furcal,
vc ventrocentral,
Ve or ve ventroexternal,
Vea ventroexternoanterior,
Vem ventroexternomedial,
Vep ventroexteroposterior,
Vel ventroexternolateral,
Vec ventroexternocentral,
Vei ventroexternointernal,
Vi or vi ventrointernal,
Vl ventrolateral.
Tubercles:
Af antenno–frontal,
Cl clypeal,
De dorsoexternal,
Di dorsointernal,
Dl dorsolateral,
L lateral,
Oc ocular,
So subocular.
Types of chaetae:
A, B, C, D, E, O, So, L, Dl cephalic chaetae,
Ml long macrochaeta,
Mc short macrochaeta,
Mcc very short macrochaeta,
me mesochaeta,
mi microchaeta,
ms s–microchaeta,
S or s chaeta s,
bs s–chaeta on Ant IV,
miA microchaetae on Ant IV,
iv ordinary chaetae on ventral Ant IV,
or organite of Ant IV,
brs border s–chaeta on Ant IV,
i ordinary chaeta on Ant IV,
mou cylindrical s–chaetae on Ant IV („soies mousses”),
x labial papilla x,
L’ ordinary lateral chaeta on Abd V,
B4, B5 ordinary chaetae on tibiotarsi.
The specimens were cleared in Nesbitt’s fluid, subsequently mounted on slides in Swan’s medium and studied using a Nikon Eclipse E600 phase contrast microscope. Figures were drawn with camera lucida and prepared for publication using Adobe Photoshop CS3.
Institutions of depository of materials:
Holotype: adult female on slide, Iran, Mazandarn province, Behshahr region, Abbas-Abad forest (36°40'N; 53°32'E), leaf litter and soil, 28.III.2013, leg. E. Yoosefi Lafooraki (
Endonura longirostris sp. n.: 1 apical bulb, dorsal view 2 apical bulb, ventral view 3 dorsal chaetotaxy of Ant III–IV 4 chaetotaxy of head and Th (holotype), dorsolateral view 5 ventral chaetotaxy of Ant III 6 tubercle L of Abd IV 7 dorsal chaetotaxy of Abd III–VI 8 chaetotaxy and ventral sclerifications of labrum 9 sensillum of Abd V 10 chaeta Di1 of Abd V.
Chaetotaxy of Endonura longirostris sp. n.: cephalic chaetotaxy dorsal side.
Tubercle | Number of chaetae | Types of chaetae | Names of chaetae |
---|---|---|---|
Cl | 4 |
Ml
me |
F G |
Af | 8 |
Ml Mc Mcc or mi mi |
B A C D |
Oc | 3 |
Ml
Mc Mcc |
Ocm Ocp Oca |
Di | 2 |
Ml
Mcc |
Di1 Di2 |
De | 2 |
Mc
Mcc |
De1 De2 |
Dl | 4 |
Ml Mc or Mcc mi |
Dl5 Dl1 Dl2, Dl4 |
(L+So) | 8 |
Ml
mi me |
L1, L4, So1 L2 So3–6 |
Segment, Group | Number of chaetae | Segment, Group | Number of chaetae adult |
---|---|---|---|
I | 7 | IV ap |
or, 8 S, i, 12 mou, 6 brs, 2 iv |
II | 11 | ||
III | 5 sensilla AO III | ||
ve | 5 | 8 bs, 5 miA | |
vc | 4 | ca | 2 bs, 3 miA |
vi | 4 | cm | 3 bs, 1 miA |
d | 5 | cp | 8 miA, 1 brs |
Terga | Legs | ||||||||
---|---|---|---|---|---|---|---|---|---|
Di | De | Dl | L | Scx2 | Cx | Tr | Fe | T | |
Th I | 1 | 2 | 1 | - | 0 | 3 | 6 | 13 | 19 |
Th II | 3 | 2+s | 3+s+ms | 3 | 2 | 7 | 6 | 12 | 19 |
Th III | 3 | 3+s | 3+s | 3 | 2 | 8 | 6 | 11 | 18 |
Sterna | |||||||||
Abd I | 2 | 3+s | 2 | 3 | VT: 4 | ||||
Abd II | 2 | 3+s | 2 | 3 | Ve: 5; chaeta Ve1 present | ||||
Abd III | 2 | 3+s | 2 | 3 | Vel:4; Fu: 4–5 me, 0 mi | ||||
Abd IV | 2 | 2+s | 3 | 5–6 | Vel: 4; Vec: 2; Vei: 2; Vl: 4 | ||||
Abd V | (3+3) | 7+s | Ag: 3; Vl: 1, L’: 1 | ||||||
Abd VI | 7 | Ve: 14; An: 2mi |
Juvenile on slide, Iran, Mazandarn province, Noor region, Kadirsar village (36°26'N; 51°49'E), leaf litter and soil, 1.III.2013, leg. E. Yoosefi Lafooraki (
The name longirostris refers to an exceptionally long buccal cone of this species.
Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone exceptionally long, labrum ogival. Head with chaetae A, B, C and D. Chaetae O and E absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with 4 and 8 chaetae respectively. Tubercles Di on Th I absent. Tubercles De on Th II and III with 3 and 4 chaetae respectively. Tubercles L on Abd III and IV with 3 and 5-6 chaetae respectively. Abd IV and V with 8 and 3 tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5 short.
General. Body length (without antennae): 0.50 (juvenile) to 1.45 mm (holotype: 1.45 mm). Colour of the body white. 2+2 medium black eyes, in a typical arrangement for the genus (one anterior and one posterior eyes, Fig.
Chaetal morphology. Dorsal ordinary chaetae of five types: long macrochaetae, short macrochaetae, very short macrochaetae, mesochaetae and microchaetae. Long macrochaetae thick, slightly arc-like or straight, narrowly sheathed, feebly serrated, apically rounded (Fig.
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant III–IV as in Fig.
Mouthparts. Buccal cone particularly long with labral sclerifications ogival. Labrum chaetotaxy: 0/2, 4 (Fig.
Dorsal chaetotaxy and tubercles. Chaetotaxy of head reduced, chaetae E, O, Dl3, Dl6, So2 and L3 absent (Fig.
Ventral chaetotaxy. On head, groups Vea, Vem and Vep with 3, 3, 3-4 chaetae respectively. Group Vi on head with 6 chaetae. On Abd IV, furca rudimentary without microchaetae. On Abd IV, tuberle L with one chaeta free (Fig.
Legs. Chaetotaxy of legs as in Table
Because of the presence of particularly elongated mouthparts and substantial reduction of chaetotaxy on lateral part of head, E. longirostris sp. n. strongly resembles E. cretensis (Ellis, 1976), known to date from Greece (Crete,
Viewing the recently published key to Endonura species (Smolis et al. 2016b), E. longirostris sp. n. is placed the nearest to E. saleri Fanciulli et Dallai, 2008, described from northeastern Italy (
Holotype: adult female on slide, Iran, Mazandarn province, Behshahr region, Abbas-Abad forest (36°40'N; 53°32'E), rooting wood, 28.III.2013, leg. E. Yoosefi Lafooraki (
Endonura paracentaurea sp. n.: 11 dorsal chaetotaxy of Ant III–IV 12 ventral chaetotaxy of Ant III 13 chaetotaxy of head and Th I–II (holotype), dorsolateral view 14 chaetotaxy of tubercle De of Th III 15 dorsal chaetotaxy of Abd I–VI 16 furca rudimentary 17 chaeta Di1 of Abd V 18 sensillum of Abd V 19 chaetotaxy and ventral sclerifications of labrum.
Chaetotaxy of Endonura paracentaurea sp. n.: cephalic chaetotaxy dorsal side.
Tubercle | Number of chaetae | Types of chaetae | Names of chaetae |
Cl | 4 |
Ml
me |
F G |
Af | 8 |
Ml
Mc mi |
B A C, D |
Oc | 3 |
Ml
Mc mi |
Ocm Ocp Oca |
Di
|
2 |
Ml
Mc |
Di1 Di2 |
De | 2 |
Mc
Mcc |
De1 De2 |
Dl | 6 |
Ml
Mcc mi |
Dl5, Dl1 Dl3, Dl4 Dl2, Dl6 |
(L+So) | 8 |
Ml
mi me |
L1, L4, So1 L2 So3–6 |
Segment, Group | Number of chaetae | Segment, Group | Number of chaetae adult |
---|---|---|---|
I | 7 | IV ap |
or, 8 S, i, 12 mou, 6 brs, 2 iv |
II | 11 | ||
III ve |
5 sensilla AO III | ||
5 | 8 bs, 5 miA | ||
vc | 4 | ca | 2 bs, 3 miA |
vi | 4 | cm | 3 bs, 1 miA |
d | 5 | cp | 8 miA, 1 brs |
Terga | Legs | ||||||||
---|---|---|---|---|---|---|---|---|---|
Di | De | Dl | L | Scx2 | Cx | Tr | Fe | T | |
Th I | 1 | 2 | 1 | - | 0 | 3 | 6 | 13 | 19 |
Th II | 3 | 2+s | 3+s+ms | 3 | 2 | 7 | 6 | 12 | 19 |
Th III | 3 | 3+s | 3+s | 3 | 2 | 8 | 6 | 11 | 18 |
Sterna | |||||||||
Abd I | 2 | 3+s | 2 | 3 | VT: 4 | ||||
Abd II | 2 | 3+s | 2 | 3 | Ve: 5–6; chaeta Ve1 present | ||||
Abd III | 2 | 3+s | 2 | 3 | Vel:4–5; Fu: 4–5 me, 4–5 mi | ||||
Abd IV | 2 | 2+s | 3 | 6 | Vel: 4; Vec: 2; Vei: 2; Vl: 4 | ||||
Abd V | (3+3) | 5+s | Ag: 3; Vl: 1, L‘: 1 | ||||||
Abd VI | 7 | Ve: 13–14; An: 2mi |
The name “paracentaurea” refers to a strong similarity of the new species to E. centaurea.
Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone short, labrum nonogival. Head with chaetae A, B, C and D. Chaetae O and E absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with six and eight chaetae respectively. Tubercles Di on Th I present. Tubercles De on Th II and III with three and four chaetae respectively. Tubercles L on Abd III and IV with three and six chaetae respectively. Abd IV and V with eight and three tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5 short.
General. Body length (without antennae): 0.90 to 1.65 mm (holotype: 1.65 mm). Colour of the body white. 2+2 small black eyes, in a typical arrangement for the genus (Fig.
Chaetal morphology. Dorsal ordinary chaetae of five types: long macrochaetae, short macrochaetae, very short macrochaetae , mesochaetae and microchaetae. Long macrochaetae thick, slightly arc-like or straight, narrowly sheathed, feebly serrated, apically rounded or pointed (Figs
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant III–IV as in Fig.
Mouthparts. Buccal short with labral sclerifications nonogival. Labral chaetotaxy: 0/2, 4 (Fig.
Dorsal chaetotaxy and tubercles. Head without chaetae E, O, So2 and L3 (Fig.
Ventral chaetotaxy. On head, groups Vea, Vem and Vep with 3, 4, 4 chaetae respectively. Group Vi on head with 6 chaetae. On Abd IV, furca rudimentary with 4-5 microchaetae without visible chaetopores (Fig.
Legs. Chaetotaxy of legs as in Table
Morphologically, E. paracentaurea sp. n. strongly recalls E. centaurea Cassagnau et Péja, 1979, a form shortly described from Greece (
Holotype: male on slide, Turkmenistan, south-western part of the country (Balkan velayat), Magtymguly (previously Kara-Kala) Area, foothills of the southern slope of the Kopet Dag mountain range, near village Juvankala, right tributary of Sumbar river, leaf litter under elm Ulmus spp, 4.II.1977, leg. A. Babenko, A. Uvarov, T. Zheltikova (
Endonura turkmenica sp. n.: 20 dorsal chaetotaxy of Ant III–IV 21 apical bulb, ventral view 22 apical bulb, dorsal view 23 ventral chaetotaxy of Ant III 24 tubercle L of Abd IV 25 ventral sclerifications of labrum 26 sensillum of Abd V 27 chaeta Di2 of Abd V 28 chaeta Di3 of Abd V 29 chaeta Di1 of Abd V 30 chaetotaxy of labrum 31 chaetotaxy of head and Th (holotype), dorsolateral view 32 chaetotaxy of Abd II 33 leg II, chaetotaxy of T and Fe, lateral view 34 chaetotaxy of Abd V–VI, dorsolateral view.
Chaetotaxy of Endonura turkmenica sp. n.: cephalic chaetotaxy dorsal side.
Tubercle | Number of chaetae | Types of chaetae | Names of chaetae |
---|---|---|---|
Cl | 4 |
Ml
Mc |
F G |
Af | 10 |
Ml
Mc Mcc |
B A, E C, D |
Oc | 3 |
Ml
Mc mi |
Ocm Ocp Oca |
Di
|
2 |
Mc
Mcc |
Di1 Di2 |
De | 2 |
Ml
Mcc |
De1 De2 |
Dl | 6 |
Ml
Mcc mi |
Dl5, Dl1 Dl3, Dl4 Dl2, Dl6 |
(L+So) | 8 |
Ml
Mcc me |
L1, L4, So1 L2 So3–6 |
Segment, Group | Number of chaetae | Segment, Group | Number of chaetae adult |
---|---|---|---|
I | 7 | IV ap |
or, 8 S, i, 12 mou, 6 brs, 2 iv |
II | 12 | ||
III ve |
5 sensilla AO III | ||
5 | 8 bs, 5 miA | ||
vc | 4 | ca | 2 bs, 3 miA |
vi | 4 | cm | 3 bs, 1 miA |
d | 5 | cp | 8 miA, 1 brs |
Terga | Legs | ||||||||
---|---|---|---|---|---|---|---|---|---|
Di | De | Dl | L | Scx2 | Cx | Tr | Fe | T | |
Th I | 1 | 2 | 1 | - | 0 | 3 | 6 | 13 | 19 |
Th II | 3 | 2+s | 3+s+ms | 3 | 2 | 7 | 6 | 12 | 19 |
Th III | 3 | 3+s | 3+s | 3 | 2 | 8 | 6 | 11 | 18 |
Sterna | |||||||||
Abd I | 2 | 3+s | 2 | 3 | VT: 4 | ||||
Abd II | 2 | 3+s | 2 | 3 | Ve: 6; chaeta Ve1 present | ||||
Abd III | 2 | 3+s | 2 | 3 | Vel: 5; Fu: 7 me, 0 mi | ||||
Abd IV | 2 | 2+s | 3 | 6 | Vel: 4; Vec: 2; Vei: 2; Vl: 4 | ||||
Abd V | (3+3) | 5+s | Ag: 3; Vl: 1, L’: 1 | ||||||
Abd VI | 7 | Ve: 14; An: 2mi |
The name turkmenica is derived from Turkmenistan, the name of the country where the species was found.
Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone relatively long, labrum ogival. Head with chaetae A, B, C, D and E. Chaeta O absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with six and eight chaetae respectively. Tubercles Di on Th I absent. Tubercles De on Th II and III with three and four chaetae respectively. Tubercles L on Abd III and IV with three and six chaetae respectively. Abd IV and V with eight and three tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5medium size.
General. Body length (without antennae): 0.50 (juvenile) to 1.45 mm (holotype: 1.45 mm). Colour of the body bluish-grey. 2+2 large black eyes, in a typical arrangement for the genus (Fig.
Chaetal morphology. Dorsal ordinary chaetae of five types: long macrochaetae, short macrochaetae, very short macrochaetae, mesochaetae and microchaetae. Long macrochaetae relatively thin, straight, narrowly sheathed, serrated, apically pointed (Fig.
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant III–IV as in Fig.
Mouthparts. Buccal cone long with labral sclerifications ogival (Fig.
Dorsal chaetotaxy and tubercles. Head without chaetae O, So2 and L3 absent (Fig.
Ventral chaetotaxy. On head, groups Vea, Vem and Vep with 3, 4, 4 chaetae respectively. Group Vi on head with six chaetae. On Abd IV, furca rudimentary without microchaetae. On Abd IV, group L without free chaeta (Fig.
Legs. Chaetotaxy of legs as in Table
Endonura turkmenica sp. n. seems to be the closest E. ceratolabralis Smolis et al., 2016 recently described from western part of Iran (
Unlike most springtails, members of the family Neanuridae completely lack a molar plate on the mandibles and have suctorial mouthparts. Therefore, they are sometimes called sucking forms in contrast to chewing taxa, where mandibles comprise an outlined structure. The highest degree of simplicity of this part of body can be observed within the subfamily Neanurinae, where the majority of genera and species are characterized by a styliform maxilla consisting of no more than one dentate lamella and a thin mandible, usually tridentate with an apical tooth seldom subdivided. For this reason, authors of taxonomic descriptions have usually devoted little attention to the construction of such elements as mandibles or maxillae. Additionally, characteristics of other mouth structures, e.g. the labrum, are frequently omitted from most papers. Interestingly, observations on the genus Endonura and other Neanurinae show that the apical part of the labrum can be modified, and its shape is constant and characteristic of the species. In the light of these facts, this mouthpart element is very useful and should be added to the list of diagnostic features in the Neanurinae taxonomy.
Up to date, two main types of shapes of the apical part of the labrum have been observed within Endonura and other Neanurinae: nonogival and ogival (
Recent observations and studies on the diet of some Neanurinae species probably provide an answer to the above question (
We thank Dr. László Dányi and Prof. Pietro Paolo Fanciulli for reviewing and their helpful comments on the manuscript. The work was financially supported by the Russian Foundations for Basic Research (grant 16-04-01228) and the Institute of Environmental Biology, Faculty of Biological Science, University of Wrocław, Poland (project no. 1076/Ś/IBŚ/2017).