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Accepted by W.M. Weiner: 30 Nov. 2018; published: 24 Jan. 2019
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
1175-5334
(online edition)
Copyright © 2019 Magnolia Press
Zootaxa 4550 (2): 221
–
235
https://www.mapress.com/j/zt/
Article
221
https://doi.org/10.11646/zootaxa.4550.2.4
http://zoobank.org/urn:lsid:zoobank.org:pub:C8D2B580-C156-4075-8FD1-E4A111DAC33F
New European Lepidocyrtus Bourlet, 1839 (Collembola, Entomobryidae)
with the first description of feeding-related dancing behaviour in Collembola
EDUARDO MATEOS
1,3
& MARKO LUKIĆ
2
1
Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals; Facultat de Biologia; Universitat de Barcelona; Avinguda Dia-
gonal 643, 08028 – Barcelona; Spain. E-mail: emateos@ub.edu
2
Croatian Biospeleological Society, Demetrova 1, HR-10 000 Zagreb, Croatia. E-mail: marko.lukic@hbsd.hr
3
Corresponding author
Abstract
The study of a springtail population from Krka National Park (Croatia) has allowed us to describe the new species Lepi-
docyrtus chorus sp. nov. and its dance-like behaviour. This study represents the first record of peculiar dancing behaviour
related to search for food and feeding among Collembola. The new species is molecularly and morphologically assigned
to the European Lepidocyrtus lignorum-group. Sequences of COXII and EF-1α genes, chaetotaxy and behaviour clearly
help to differentiate the new species from the other species in the group.
Key words: Lepidocyrtinae, chaetotaxy, food preferences
Introduction
Lepidocyrtus Bourlet, 1839 is one of the genera with the highest number of species within the Collembola. Several
molecular studies have concluded that, due to the occurrence of cryptic species, the actual number of Lepidocyrtus
species is probably much higher than the species number currently described (Soto-Adames 2002; Cicconardi et al.
2010; Cicconardi et al. 2013; Mateos et al. 2018; Zhang et al. 2018a). Such molecular findings encourage the
taxonomists to search for small morphological differences between populations (usually interpreted as intraspecific
variability) as indication of speciation (Zhang et al. 2018b). Also, differences in habitat selection between
populations could help to detect cryptic species (Zhang et al. 2018a). The use of behavioural features in
collembolan species descriptions is very scarce. This is mainly because behaviour studies require the observation
of living specimens, while springtails for taxonomical studies are usually obtained dead from samples using some
sort of extractor (Pesson 1971). Even the diet is usually not documented in the species descriptions, although these
data are relatively easily obtainable by analysing the gut content of specimens mounted on slides using light
microscopy.
Collembola can show a generalist type (consuming a wide variety of food) or specialist type (consuming a
specific type of food) strategy of exploitation of trophic resources (Hasegawa & Takeda 1995). Also, as Hopkin
(1997) pointed out, the opportunistic nature of the feeding behaviour of many species of Collembola may be one
reason for their successeful colonization of various microhabitats. Studies dealing with Collembola diet seem to
conclude that the majority of euedaphic and hemiedaphic species are generalists and ingest whatever fungi, lichens,
decomposing vegetation or detritus; epiedaphic species may also feed on living vegetation, pollen and algae
(Hopkin 1997 and references therein) while some cave species are recorded to ingest clay-like material (Lukić et
al. 2010). Entomobryidae species have chewing mandibula type and seem to be fundamentally fungivores, some of
them herbivores (Malcicka et al. 2017). Commonly, Lepidocyrtus species can be seen walking on the soil surface
or even on vegetation (especially those bigger Lepidocyrtus species). Therefore, it can be expected that these
species include plant material in their diet.
In situ behavioural data for Collembola are scarce. Somewhat better documented is the mating behaviour in
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several Symphypleona species. The most elaborated courtship is described in Sminthuridae and Bourletiellidae
where the males have modified antennae to clasp the female, and where some species perform a peculiar dance-like
behaviour prior to sperm transfer (Betsch 1974; Blancquaert 1981; Kozlowski & Aoxiang 2006). Dance-like
behaviour for purpouses other than reproduction have not been described in Collembola so far.
In a study of European Lepidocyrtus species-groups, Mateos et al. (2018) pointed out that four specimens of an
unnamed Lepidocyrtus species (Lepidocyrtus sp., sample code LP383) could represent a new species. These
specimens belong to the same population that is the object of the present study in which we confirmed the status of
the new species through detailed morphological analysis. The objective of the present paper is to describe this new
species, its feeding preferences and dance-like behaviour that seems to be related to the search for food.
Materials and methods
In the course of scientific campaigns in the Krka National Park (Croatia) done by ML and colleagues, populations
of Lepidocyrtus species were observed in April 2015, October 2016 and September 2018. In 2015 and 2018 several
specimens were filmed alive and hand-collected for study; in 2016 specimens were only photographed and filmed.
Photos and video were made using iPhone5, Olympus Tough TG-3 and Canon 80D with Canon MP-65 macro lens.
Video material was recorded by Marko Lukić on April 2015 and October 2016, and by Dino Grozić on September
2018. Video is available on YouTube (https://youtu.be/8pspWYQroEI) and deposited on Figshare (https://doi.org/
10.6084/m9.figshare.7380836.v1) where it can be freely accessed and downloaded in full resolution.
For morphological studies the specimens were mounted on slides with the head separated from the body. The
specimens were cleared using Nesbitt fluid or lactic acid and then slide-mounted in Hoyer medium (Palacios-
Vargas & Mejía 2007). The slides were studied under a phase contrast microscope. Genetic sequences of four
specimens of the studied population (specimen codes LP383-1 to LP383-4, Table 1) were used in Mateos et al.
(2018); the body skin (after DNA extraction) and the head of these four specimens were also cleared and mounted
on slides.
TABLE 1. Lepidocyrtus chorus sp. nov. GenBank accession numbers of sequenced genes of four specimens of the type
series (see Mateos et al. 2018).
For the taxonomic descriptions the following terms and codes were used: For dorsal cephalic chaetotaxy the
“AMS” nomenclature system (see Soto-Adames 2010); the equivalence between "RST" system (Gisin 1967a and
Wang et al. 2003 for chaetae R
1s
) and "AMS" system macrochaetae notation is: R
0
=A
0
, R
1s
=A
2
a, R
1
=A
2
, R
2
=A
3
,
R
3
=M
1
, S=M
2
, T=S
3
, P
o
=Pa5. For labial palp Fjellberg (1999). For labial chaetotaxy Gisin (1964). For postlabial
chaetotaxy Soto-Adames (2010). For clypeal chaetotaxy Yoshii & Suhardjono (1992). For interocular chaetotaxy
Mari-Mutt (1986). For dorsal chaetotaxy schemes of thoracic and abdominal segments Gisin (1967b), Szeptycki
(1972, 1979), Wang et al. 2003 and Mateos (2008). For tergal specialized chaetae (S-chaetae) Zhang & Deharveng
(2015).
Abbreviations and symbols in text and figures: ant.—antennal segment, th.—thoracic segment, abd.—
abdominal segment, I–VI—segment numbers, pse—pseudopore.
Taxonomic section
Family Entomobryidae Schäffer, 1896
Specimen Code COXII EF-1α
LP383-1 MF095522 MF095609
LP383-2 MF095523 -
LP383-3 MF095524 MF095610
LP383-4 MF095525 MF095611
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DANCING BEHAVIOUR IN LEPIDOCYRTUS
Genus Lepidocyrtus Bourlet, 1839
Lepidocyrtus chorus Mateos & Lukić sp. nov.
Figs 1–31, Table 1
Type material. Holotype: female on slide (slide code: CRBA-77842), Krka National Park, village Oklaj, Town
Šibenik, hidropowerplant Miljacka, Croatia, 95 m above sea level, N44º00’04.0” E16º01’05.9”, on stone steps
(Figs 1–2), hand collecting, 29.iv.2015, leg. M. Lukić. Paratypes: 16 females on slides (slide codes LP383-1 to
LP383-09, CRBA-77843, and six slides with code CLL4558), and 18 specimens (of unknown sex) in a vial with
absolute ethanol (vial code LP383 (3 specimens) and CLL4558 (15 specimens)); same data as holotype. 4 females
on slides (code: CLL5100) and 1 specimen (of unknown sex) in a vial with absolute ethanol (vial code CLL5100),
25.ix.2018, leg. N. Sudar; same data as holotype.
The holotype and paratype CRBA-77843 are deposited at the Centre de Recursos de Biodiversitat Animal,
Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain (http://www.ub.edu/crba/). Paratypes LP383-1 to
LP383-09 on slides and three specimens in absolute ethanol (vial code LP383) deposited at the E. Mateos
collection, Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat
de Barcelona, Barcelona, Spain. 10 paratypes (CLL4558, six specimens; CLL5100, four specimens) on slides and
16 specimens in absolute ethanol (CLL4558, 15 specimens; CLL5100, 1 specimen) deposited at the Croatian
Biospeleological Society Collection, Zagreb, Croatia.
Diagnosis. Trunk uniformly white, with one lateral dark-violet spot on each side of abd.IV. Th.II projecting
over head. Ant.I-II, legs, ventral tube and posterior region of manubrium with scales. Apical bulb on ant.IV absent.
Labial chaetae M
1
M
2
REL
1
L
2
in “p row” well developed and ciliated, R shorter. Dorsal cephalic and body
macrochaetae formula as A
0
[A
2a
]A
2
A
3
Pa
5
/00/0101+3. Without chaeta s on abd.IV.
Molecular diagnosis. This species includes all populations that cluster with COXII and EF-1α sequences of
the individuals LP383-1 to LP383-4 (Table 1, see also Mateos et al. 2018), with significant support in an adequate
molecular delimitation model.
FIGURES 1–4. Lepidocyrtus chorus sp. nov. Type locality and habitus. 1, stone steps, photo by Tin Rožman; 2, surface of the
stone steps where specimens were filmed and collected; 3, habitus in situ; 4, specimens contacting while grazing. Photos 2, 3
and 4 by Marko Lukić.
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FIGURES 5–8. Lepidocyrtus chorus sp. nov. holotype. 5, habitus lateral (in alcohol); 6, dorsal head (in alcohol); 7 habitus of
lateral body (on slide) showing pollen grains coming out of the intestine; 8 dorsal head (on slide).
Etymology. The specific name refers to the dance-like behaviour observed in situ. In latin “chorus” means “a
dancer”.
Description. Holotype body length 1.6 mm (without head nor furca), paratypes 1.4–1.7 mm. Live specimens
of silver color (due to coating of scales, Figs 3–4), specimens in alcohol white with a dark-violet lateral spot on
abd.IV (Fig. 5). Th.II projecting over head (Fig. 5). Head with a dark-violet apical triangular spot between antennae
bases (Fig. 6). Ant.II-III-IV slightly violet. Scales densely covering dorsal and ventral surfaces of head, trunk, legs,
ventral tube and manubrium, dorsal surface of ant.I-II, and anterior surface of dens (Figs 7–8).
Antennal length to head diagonal length ratio (head diagonal measured from cervical edge to apex of mouth
part) 1.5–1.7, holotype 1.7. Relation of antennal joints I–IV as 1:1.7–1.9:1.4–1.7:2.7–3.4, in holotype as
1:1.7:1.7:2.7. Ant.I with three dorsolateral small acute chaetae in a triangle (antennal-I-organ sensu Huther, 1986).
Ant. III sense organ composed of two bent sensory rods partially behind a cuticular fold (Fig. 9). Ant. IV without
apical bulb.
Clypeus with twelve ciliated chaetae (3 in row pf, 5 in row f, and 2–2 in rows L
1
–L
2
, respectively).
Arrangement of chaetae on labrum 4/554, prelabral chaetae ciliated, first and second row of labral chaetae smooth,
apical row branched (Fig. 10). Labrum intrusion inverted U-shaped, labral edge with four minute rounded labral
papillae with one-pointed end (the lateral papillae) and three-pointed end (the central papillae) (Fig. 10). Labial
palp with lateral process on papilla E slightly curved, with rounded apical end and reaching apex of papilla (Fig.
11). Outer maxillary palp with two smooth chaetae and three smooth sublobal chaetae (Fig. 12).
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Labium chaetotaxy formed by 5 smooth chaetae (a1–a5) in anterior row; basal row with ciliated chaetae
M
1
M
2
REL
1
L
2
(Fig. 13) with R smaller than other chaetae (ratio of R/M~0.4). Postlabial chaetotaxy (Fig. 13) with
4+4 ciliated chaetae along ventral cephalic groove.
Dorsal cephalic macrochaetae formula A
0
A
2
A
3
Pa
5
(Fig. 14), but also with pair of smaller supplementary
macrochaetae A
2a
between A
0
and A
2
; maximum number of macrochaetae An on head 13+13.
Eye patches dark blue. Diameters of eyes A–F about the same. Eyes G and H slightly smaller (A:G; A:H ≈
1.5). Interocular chaetotaxy (Fig. 14) with s, t, q chaetae and 2–3 intraocular scales.
FIGURES 9–13. Lepidocyrtus chorus sp. nov. 9, ant.III apical organ; 10, labrum; 11, outer labial papilla (left side); 12,
maxillary palp (right side); 13, labial and postlabial chaetotaxy (right side).
In Fig. 15 are represented all the elements composing dorsal body chaetotaxy. Dorsal body macrochaetae
formula 00/0101+3 (m3 on abd.II, C1+B4, B5, B6 on abd.IV). Dorsal chaetotaxy of th.II–III and abd.I as in Figs
16–18. Th.II with 2 lateral S-chaetae (al and ms) and without macrochaetae in dorsal position. Th.III with a lateral
sensillum (al) between two ciliated chaetae. Abd.I with a lateral S-microchaeta (ms) external to a6. Chaetotaxy of
abd.II–III as in Figs 19–20. Abd.II chaetotaxy between the two dorso-medial trichobothria with mesochaetae a2,
a3, a2p,m3e, p4, sens as and macrochaeta m3; macrochaeta m5 with socket of similar size of macrochaeta m3.
Abd.III with S-chaetae as and ms; chaeta d3 present. Chaetae associated with trichobotria on abd.II–III fan-shaped.
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Chaetotaxy of abd.IV as in Fig. 21; macrochaetae B4, B5, B6, C1, D3, E2, E3, E4, F1, F2, F3 and T6 broader with
broad socket (bcM in Fig. 15-a), while D2, De3, D3p, E1, E4p, F3p, Fe4, Fe5, r3 and T7 thinner with smaller
socket (tcM in Fig. 15-b); macrochaeta F2 above macrochaeta E3; the ratio of distances between macrochaetae
C1–B4/B4–B6 1.1–1.3; accessory chaeta s associated with trichobotrium T2 absent; all chaetae associated with
trichobotria on abd.IV (D1, a, m, pe, pi) fan-shaped; sens chaetotaxy composed by 2 anterior dorsomedial elongate
S-chaetae (S in Fig. 21 and Fig. 15-e), as and ps. Dorsal chaetotaxy of abd.V as in Fig. 22; with S-chaetae as,
acc.p4 and acc.p5.
FIGURE 14. Lepidocyrtus chorus sp. nov., dorsal head chaetotaxy (left side).
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DANCING BEHAVIOUR IN LEPIDOCYRTUS
Trochanteral organ with 12–14 smooth spiny chaetae forming a V shape pattern (Fig. 23). Ungues (Fig. 24)
with paired basal teeth at 54% from inner edge, one sub-equal median tooth at 70%, and a tiny apical tooth at 86%
from inner edge, respectively; three external teeth, 2 paired laterally and 1 unpaired basally, also present; unguiculi
lanceolate, with denticles along outer edge, some specimens with unguiculi II-III smooth or with tiny denticles;
tibiotarsal tenent hair spatulate, smooth and as long as claw; ratio of supraempodial chaeta (smooth chaeta on
tibiotarsus III opposite to tenent hair) / unguiculus is around 0.7.
Ventral tube with a maximum of 5+5 ciliated chaetae on anterior side (Fig. 25) and 15 weakly ciliated chaetae
on posterior side; lateral flap with a maximum of 18 laterodistal chaetae (6 ciliated and 12 smooth, Fig. 26).
Manubrium with 2+2 ciliated apical chaetae on anterior side; manubrial plate with 3–4 inner chaetae and 6–9
chaetae outer to the 2 pseudopores (Fig. 27). Dental tubercle absent. Mucro without spinelet on basal spine (Fig.
28). Ratio manubrium/dens/mucro as 17.5:21.5:1.
Ecology and distribution. The specimens of L. chorus sp. nov. were found on old stone steps in the backyard
of the hydropower plant (Figs 1–2). Limestone steps are situated at 95 m above sea level, at the bottom of a 100 m
deep canyon of the river Krka, partially covered by leaf litter and fine gravel, and overgrown by biofilm. The
region is characterized by warm Mediterranean climate, type Cfsa according to Köppen climate classification
(Milković & Trninić 2007), with mean air temperature when species was observed being 12.1°C for April 2015 and
13.5°C for October 2016 (data for the nearby meteorological station Knin; time period 1949–2017) (data available
at http://www.meteo.hr).
All specimens mounted on slides (17 specimens) collected on 29.iv.2015 had the gut completely and
exclusively full of tricolpate pollen grains possibly of Brassica L. species. This pollen was clearly visible inside the
gut due to the clearing procedure with Nesbitt fluid applied to the specimens. The gut of the four mounted
specimens collected on 25.ix.2018 contained plant material, fungal hyphae, conidia, pollen grains and brown
amorphous material. Pollen grains of several plants were recorded in three out of four specimens but were not the
dominant type of food in the gut.
This species is known only from its type locality.
FIGURE 15. Lepidocyrtus chorus sp. nov. Dorsal body chaetotaxic structures: a, broad ciliated macrochaeta (bcM); b, thin
ciliated macrochaeta (tcM); c, smooth mesochaeta; d, fan shaped chaeta; e, S-chaeta; f, S-microchaeta, g, trichobothrium; h,
scale; i, pseudoporus; k, bcM socket; m, long tcM socket; o, short tcM socket; p, trichobothrium socket; q, scales socket.
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FIGURES 16–18. Lepidocyrtus chorus sp. nov. 16, th.II dorsal chaetotaxy (left side), pse—pseudoporus, circles–ciliated
chaetae; 17, th.III dorsal chaetotaxy (left side), pse—pseudoporus; 18, abd.I dorsal chaetotaxy (left side), pse—pseudoporus.
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Dancing behaviour. Video is available on YouTube (https://youtu.be/8pspWYQroEI) and deposited on
Figshare (https://doi.org/10.6084/m9.figshare.7380836.v1). Peculiar dance-like behaviour of the L. chorus sp. nov.
was observed during the sampling on 29.iv.2015 and 25.ix.2018. Two types of dance could be identified: ‘grazing
dance’ and ‘walking dance’. During grazing dance individuals retain their head position while feeding and at the
same time make rapid circular clockwise and counter clockwise movement of the abdomen (Figs. 29–30, for
example see video at 00:37). When finished with grazing individuals continue with walking dance where they
progress with the movement in a certain direction and at the same time continue with the rapid circular movement
of the abdomen (Fig. 31, for example see video at 00:30 and 01:13). Individuals were usually few centimetres apart
from each other and there was no obvious interaction between them. When coming in closer contact, they did not
change their behaviour and continue with the dance, usually moving away from each other. On 07.x.2016,
additional footage of this dance-like behaviour was captured with macro lenses that revealed more details. The
behaviour of the specimens on this occasion was similar, although the circular movement of the abdomen was less
conspicuous (for example see video at 02:22). Individuals were also observed grazing without circular movement
of the abdomen. On this occasion two specimens were photographed in close interaction while grazing (Figs 3–4).
FIGURES 19–20. Lepidocyrtus chorus sp. nov. 19, abd.II chaetotaxy (left side), black circles—broad ciliated macrochaetae,
pse—pseudoporus; 20, abd.III complete chaetotaxy (left side), broad black circles—broad ciliated macrochaetae, small black
circles—thin ciliated macrochaetae, pse—pseudoporus.
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FIGURE 21. Lepidocyrtus chorus sp. nov., abd.IV chaetotaxy (left side), broad black circles—broad ciliated macrochaetae,
small black circles—thin ciliated macrochaetae.
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FIGURES 22–28. Lepidocyrtus chorus sp. nov. 22, abd.V chaetotaxy (left side), broad black circles—broad ciliated
macrochaetae, small black circles—thin ciliated macrochaetae; 23, trochanteral organ; 24, third leg apex with unguis,
unguiculus and tenent hair; 25, ventral tube, anterior view (left side); 26, ventral tube left lateral flap; 27, manubrial plate (left
side), empty circles—ciliated chaetae, filled circles—pseudopora; 28, mucro.
Discussion. Morphological characters clearly assign Lepidocyrtus chorus sp. nov. to the Lepidocyrtus
lignorum-group (sensu Mateos 2011). Also, genetic sequences done by Mateos et al. (2018) clearly place the new
species in this European species group. Currently L. lignorum-group is composed by 12 species (13 with the
inclusion of L. chorus sp. nov.), namely L. barbulus Mateos, 2011, L. instratus Handschin, 1924, L. intermedius
Mateos, Escuer & Álvarez-Presas, 2018 (in Mateos et al. 2018), L. juliae Mateos, 2011, L. lignorum (Fabricius,
1793), L. peisonis Traser & Christian, 1992, L. ruber Schött, 1902, L. tellecheae Arbea & Jordana, 1990, L. traseri
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Winkler, 2016, L. uzeli Rusek, 1985, L. vexillosus Loksa & Bogojević, 1967 and L. violaceus Lubbock, 1873. All
of them have trunk macrochaetotaxy formula 00/0101+3. The dorsal head macrochaetotaxy formula A
0
A
2
A
3
Pa
5
is
also shared by all species of the group (and also by L. chorus sp. nov.) except L. intermedius (A
0
A
2
Pa
5
), L. ruber
(A
0
A
2
A
3
) and L. vexillosus (A
0
A
2
Pa
5
)
FIGURES 29–31. Lepidocyrtus chorus sp. nov. Schematic drawings of two types of dance. 29, ‘grazing dance’, clockwise
direction of a single individual; 30, ‘grazing dance’, counter clockwise direction of a single individual; 31, ‘walking dance’, red
line denotes a path of the head, black line denotes a path of the abd.VI. Black arrows indicate direction of the circular
movement of abdomen. Schematic drawing of the species made by Iva Čupić. For more details see paragraph ‘Dancing
behavior’ and recorded video.
Lepidocyrtus chorus sp. nov. shares the body colour pattern with L. vexillosus (one dark spot on each side of
abd.IV), but can be clearly differentiated from it because L. vexillosus lack dorsal cephalic macrochaeta A3 and, in
the foot complex, has the unguis paired basal teeth in more apical position (76% from the inner edge), very reduced
unguis apical tooth, and unguiculus without denticles (see Loksa & Bogojević, 1967). By the characteristic body
colour pattern L. chorus sp. nov. clearly differs from all the other species of the L. lignorum-group; further
differences include the morphology of abd.IV chaetae r3 (thin ciliated macrochaeta in L. chorus sp. nov. and
smooth mesochaeta in all the other species) and T6 (broad ciliated macrochaeta in L. chorus sp. nov. and thin
ciliated macrochaeta in all the other species). Other particular differences of L. chorus sp. nov. with each above
mentioned species include: two M chaetae in labial chaetotaxy (more than two in L. barbulus), mesothorax slightly
projecting over the head (strongly projecting in L. instratus), without ocular chaeta q and lateral pseudopores on
abd.IV (present in L. juliae, unpublished data), unguiculus acuminate (truncate in L. peisonis, L. ruber and L.
uzeli), apex of third row of labral chaetae branched (simple in L. tellecheae), abd.IV chaeta B6 broad ciliated
macrochaeta (thin ciliated macrochaeta in L. traseri), ratio of distances between macrochaetae C1–B4/B4–B6 1.1–
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1.3 (0.53–0.75 in L. lignorum and 0.61–0.72 in L. violaceus). Also L. chorus sp. nov. clearly differs from L.
barbulus, L. juliae, L. intermedius, L. lignorum, L. tellecheae and L. violaceus in the phylogenetic analyses of
genes CoxII and EF-1α done by Mateos et al. (2018).
Analyses of gut content revealed definite preference of L. chorus sp. nov. for feeding on pollen of just one
plant species (possibly of a Brassica species) at the time of the sampling on 29.iv.2015, while on 25.ix.2018 the gut
was filled with plant material, fungal hyphae, conidia, brown amorphous material but also with pollen of several
plant species. Unfortunately, filmed specimens on 07.x.2016 are not available for the study of gut content. In the
detailed overview of Collembola as pollen feeders, Kevan & Kevan (1970) gave several dozen of Collembola
species, among them at least three Lepidocyrtus species, that have been recorded ingesting pollen either directly by
visiting flowers or probably feeding on wind-borne pollen. Pollen wall characteristics (porosity, thickness, and
composition) are responsible for differences in digestibility among pollen types by animals (Roulston & Cane
2000). Some Collembola species, like Onychiurus pseudofimetarius Folsom, can digest the pollen wall (Scott &
Stojanovich 1963), but not all species possess this digestive ability. To crack open the pollen wall mechanically is
another method used to extract pollen content (Roulston & Cane 2000), and the mandibular molar plate of
Lepidocyrtus could be useful for this method of digesting pollen grains. Some pollen grains in the gut of L. chorus
sp. nov. had the wall broken meaning that their content was digested. With the data available we can hypothesize
that L. chorus sp. nov. feeds exclusively on pollen grains during bloom of certain plants and favors this type of
food but also feed oportunistically during other seasons.
Feeding preference and occasional grazing during dancing of L. chorus sp. nov. suggest that such behaviour is
probably related to feeding and searching for the wind-borne pollen deposited on the stone surface and possibly
other type of food. In support comes the fact that during dancing no courtship or spermatophore transfer has been
observed and that subadults and juvenile specimens have also been observed dancing, leading to conclusions that it
is not related to mating. Somewhat similar dance related to search for food is described for the blowfly Phormia
regina (Meigen), where specimens perform a series of loops and spirals rather than straight line movement when
they come in contact with the sugar (Dethier l957, Nelson 1977).
To our knowledge, this is the first record of peculiar dancing behaviour related to feeding among Collembola.
Laboratory experiments on L. chorus sp. nov. is needed to confirm that the dance is triggered by the presence of
certain type of food and exclusively related to feeding.
Acknowledgements
We would like to thank Iva Čupić for schematic drawing of the species, Dino Grozić for video recording, Tin
Rožman for image editing and discussion on dancing behaviour, Natalija Sudar for collecting fresh material and
Mark Judson for improving the English style of the title. Wanda M. Weiner, Nikolas G. Cipola and Daniel Winkler
provided helpful comments that improved the manuscript. This study is partially funded by the Krka National Park
(Croatia).
References
Arbea, J.I. & Jordana, R. (1990) New species of Pseudosinella and Lepidocyrtus from Navarra (Northern Iberian Peninsula).
Spixiana, 13 (1), 25–31.
Betsch, J.M. (1974) Contribution a l'etude de la reproduction chex les Bourletiellinae (Collemboles, Symphypleones).
Pedobiologia, 14, 179–81.
Blancquaert, J.P. (1981) Mating behaviour in some Sminthurididae (Collembola) with reference to the systematics of
Symphypleona. Pedobiologia, 22, 1–4.
Bourlet, A. (1839) Mémoire sur les Podures. Mémoires de la Société des Sciences de l' Agriculture de Lille, 1, 377–417.
Cicconardi, F., Fanciulli, P.P. & Emerson, B.C. (2013) Collembola, the biological species concept and the underestimation of
global species richness. Molecular Ecology, 22, 5382–5396.
https://doi.org/10.1111/mec.12472
Cicconardi, F., Nardi, F., Emerson, B. C., Frati, F. & Fanciulli, P.P. (2010) Deep phylogeographic divisions and long-term
persistence of forest invertebrates (Hexapoda: Collembola) in the north-western Mediterranean basin. Molecular Ecology,
19, 386–400.
MATEOS & LUKIĆ
234
·
Zootaxa 4550 (2) © 2019 Magnolia Press
https://doi.org/10.1111/j.1365-294X.2009.04457.x
Dethier, V.G. (1957) Communication by insects: physiology of dancing. Science, 125, 331–336.
https://doi.org/10.1126/science.125.3243.331
Fabricius, J.C. (1793) Entomologia Systematica Emendata et Aucta, Secundum Classes, ordines, genera, species adjectis
synonimis, locis, observationibus, descriptionibus. Vol . 2. C. G. Proft, Hafniae, 519 pp.
Fjellberg, A. (1999) The labial palp in Collembola. Zoologischer Anzeiger, 237, 309–330.
Fjellberg, A. (1999) The labial palp in Collembola. Zoologischer Anzeiger, 237, 309–330.
Gisin, H. (1964) Collemboles d’Europe VII. Revue Suisse de Zoologie, 71 (4), 649–678.
Gisin, H. (1967a) Deux Lepidocyrtus nouveaux pour l’Espagne. Eos, 42 (3–4), 393–396.
Gisin, H. (1967b) Espèces nouvelles et lignées évolutives de Pseudosinella endogés. Memórias e Estudos do Museu Zoológico
da Universidade de Coimbra, 301, 5–25.
Handschin, E. (1924) Die Collembolenfauna des Schweizerischen Nationalparkes. Denkschriften der Schweizerischen
Naturforschenden Gesellschaft, 60 (2), 89–174.
Hasegawa, M. & Takeda, H. (1995) Changes in feeding attributes of four collembolan populations during the decomposition
process of pine needles. Pedobiologia, 39 (2), 155–169.
Hopkin, S.P. (1997) Biology of the Springtails (Insecta: Collembola). Oxford University Press, Oxford, 330 pp.
Kevan, P.G. & Kevan, D.K.McE. (1970) Collembola as pollen feeders and flower visitors with observations from the high
Arctic. Quaestiones Entomologicae, 6, 311–26.
Kozlowski, M.W. & S. Aoxiang (2006) Ritual behaviors associated with spermatophore transfer in Deuterosminthurus
bicinctus (Collembola: Bourletiellidae). Journal of Ethology, 24, 103–109.
https://doi.org/10.1007/s10164-005-0162-6
Loksa, I. & Bogojević, J. (1967) Einige neue Collembolen—Arten aus Jugoslawien. Acta Zoologia Academiae Scientiarum
Hungaricae, 13 (1–2), 139–148.
Lukić, M., Houssin, C. & Deharveng, L. (2010) A new relictual and highly troglomorphic species of Tomoceridae
(Collembola) from a deep Croatian cave. ZooKeys, 69, 1–16.
https://doi.org/10.3897/zookeys.69.739
Lubbock, J. (1873) Monograph of the Collembola and Thysanura. The Ray Society for 1871, 276 pp.
Malcicka, M., Berg, M.P. & Ellers, J. (2017) Ecomorphological adaptations in Collembola in relation to feeding strategies and
microhabitat. European Journal of Soil Biology, 78, 82–91.
https://doi.org/10.1016/j.ejsobi.2016.12.004
Mari-Mutt, J.A. (1986) Puerto Rican species of Lepidocyrtus and Pseudosinella (Collembola: Entomobryidae). Caribbean
Journal of Sciences, 22(1–2), 1–48.
Mateos, E. (2008) The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae). Zootaxa, 1769, 35–59.
Mateos, E. (2011) New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae). Zootaxa, 3108, 25–40.
Mateos, E., Escuer, P., Galina, B., Riutort, M & Álvarez-Presas, M. (2018) Untangling Lepidocyrtus (Collembola,
Entomobryidae): new molecular data shed light on the relationships of the European groups. Invertebrate Systematics, 32,
639–651.
https://doi.org/10.1071/IS17056
Milković, J. & Trninić, D. (2007) Meteorological and hydrological properties of the Krka river basin. In: Marguš, D. (Eds.),
Zbornik radova sa simpozija Rijeka krka i Nacionalni park Krka: prirodna i kulturna baština, zaštita i održivi razvitak.
Narodne novine, 2007, pp. 79–91.
Nelson, M.C. (1977) The blowfly's dance: role in the regulation of food intake. Journal of Insect Physiology, 23 (5), 603–611.
https://doi.org/10.1016/0022-1910(77)90055-5
Palacios-Vargas, J.G. & Mejía, B.E. (2007) Técnicas de colecta montaje y preservación de microartrópodos edáficos.
Universidad Nacional Autónoma de México, México, 74 pp.
Pesson, P. (Ed.) (1971). La vie dans les sols: aspects nouveaux, études expérimentales. Coll. Géobiologie, écologie,
aménagement, Gauthier-Villars, Paris, 471 pp.
Roulston, T.H. & Cane, J. H. (2000) Pollen nutritional content and digestibility for animals. Plan Systematics and Evolution,
222, 187–209.
https://doi.org/10.1007/BF00984102
Rusek, J. (1985) New Palearctic Lepidocyrtus and Pseudosinella species (Collembola: Entomobryidae). Věstník
Československé Společnosti Zoologické, 49, 132–146.
Schäffer, C. (1896) Die Collembolen der Umgebung von Hamburg und benachbarter Gebiete. Mitteilungen aus dem
Naturhistorischen Museum in Hamburg, 13, 149–216.
Schött, H. (1902) Études sur les Collemboles du Nord. Bihang Svenska Vetenskaps-Akademiens Handlingar, 28 (4), 1–48.
Scott, H.J. & Stojanovich, C.T. (1963) Digestion of juniper pollen by Collembola. Florida Entomologist, 46, 189–191.
https://doi.org/10.2307/3493630
Soto-Adames, F.N. (2002) Molecular phylogeny of the Puerto Rican Lepidocyrtus and Pseudosinella (Hexapoda: Collembola),
a validation of Yoshii's 'colour pattern species'. Molecular Phylogenetics and Evolution, 25, 27–42.
https://doi.org/10.1016/S1055-7903(02)00250-6
Soto-Adames, F.N. (2010) Two new species and descriptive notes for five Pseudosinella species (Hexapoda: Collembola:
Zootaxa 4550 (2) © 2019 Magnolia Press
·
235
DANCING BEHAVIOUR IN LEPIDOCYRTUS
Entomobryidae) from West Virginian (USA) Caves. Zootaxa, 2331, 1–34.
Szeptycki, A. (1972) Morpho-systematic studies on Collembola III. Body chaetotaxy in the first instars of several genera of the
Entomobryomorpha. Acta zoologica cracoviensia, 17, 341–372.
Szeptycki, A. (1979) Chaetotaxy of the Entomobryidae and its phylogenetical significance. Morpho-systematic studies of
Collembola. IV. Polska Akademia Nauk, Zakład Zoologii Systematycznej i Doświadczalnej, Państwowe Wydawnictwo
Naukowe, Warszawa and Kraków, 219 pp.
Tömösváry, Ö. (1882) Adatok hazánk Thysanura-faunájához. Magyar Tudományos Akadémia Mathematikai és
Természettudományi Közlemények, 18, 117–131, 1 pl.
Traser, G. & Christian, E. (1992) Lepidocyrtus peisonis sp. n., ein neuer Springschwanz aus dem Neusiedlersee-Gebiet
(Collembola: Entomobryidae). Folia Entomologica Hungarica, 52, 119–121.
Wang, F., Chen, J.-X. & Christiansen, K. (2003) Taxonomy of the genus Lepidocyrtus s.l. (Collembola: Entomobryidae) in East
and Southeast Asia and Malaysia, with description of a new species from the People's Republic of China. The Canadian
Entomologist, 135, 823–837.
https://doi.org/10.4039/n02-106
Winkler, D. (2016) A new species of Lepidocyrtus (Collembola, Entomobryidae) from the Börzsöny Mountains, Hungary.
Zootaxa, 4150 (4), 388–400.
https://doi.org/10.11646/zootaxa.4150.4.2
Yoshii, R. & Suhardjono, Y.R. (1992) Collembolan fauna of Indonesia and its affinities III: Collembola of Timor Island. Acta
Zoologica Asiae Orientalis, 2, 75–96.
Zhang, F. & Deharveng, L. (2015) Systematic revision of Entomobryidae (Collembola) by integrating molecular and new
morphological evidence. Zoologica Scripta, 44, 298–311.
https://doi.org/10.1111/zsc.12100
Zhang, B., Chen, T.W., Mateos, E., Scheu, S. & Schaefer, I. (2018a) Cryptic species in Lepidocyrtus lanuginosus (Collembola:
Entomobryidae) are sorted by habitat type. Pedobiologia—Journal of Soil Ecology, 68, 12–19.
https://doi.org/10.1016/j.pedobi.2018.03.001
Zhang, F., Jantarit, S., Nilsai, A., Stevens, M.I., Ding, Y. & Satasook, C.(2018b) Species delimitation in the morphologically
conserved Coecobrya (Collembola: Entomobryidae): A case study integrating morphology and molecular traits to advance
current taxonomy. Zoologica Scripta, 47 (3), 342–356.
https://doi.org/10.1111/zsc.12279
