Research Article |
Corresponding author: Yoshitaka Kamimura ( kamimura@fbc.keio.ac.jp ) Academic editor: Yasen Mutafchiev
© 2017 Yoshitaka Kamimura, Rodrigo Lopes Ferreira.
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:
Kamimura Y, Ferreira RL (2017) Earwigs from Brazilian caves, with notes on the taxonomic and nomenclatural problems of the Dermaptera (Insecta). ZooKeys 713: 25-52. https://doi.org/10.3897/zookeys.713.15118
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Based on samples collected during surveys of Brazilian cave fauna, seven earwig species are reported: Cylindrogaster cavernicola Kamimura, sp. n., Cylindrogaster sp. 1, Cylindrogaster sp. 2, Euborellia janeirensis, Euborellia brasiliensis, Paralabellula dorsalis, and Doru luteipes, as well as four species identified to the (sub)family level. To date, C. cavernicola Kamimura, sp. n. has been recorded only from cave habitats (but near entrances), whereas the other four organisms identified at the species level have also been recorded from non-cave habitats. Wings and female genital structures of Cylindrogaster spp. (Cylindrogastrinae) are examined for the first time. The genital traits, including the gonapophyses of the 8th abdominal segment shorter than those of the 9th segement, and venation of the hind wings of Cylindrogastrinae correspond to those of the members of Diplatyidae and not to Pygidicranidae. This is the first synopsis of cave-dwelling earwigs of Brazil, one of the most species-rich areas of Dermaptera in the world.
bat guano, cave fauna, Cylindrogaster cavernicola sp. n., Cylindrogastrinae , dermapteran taxonomy, female genitalia, Heterolabis , new synonym, traumatic mating
Dermaptera (earwigs) is a polyneopteran insect order with more than 2000 described species from mainly tropical and warm temperate regions (
Organisms that live in the subterranean environments are frequently classified into three categories (e.g.,
Only two troglobitic earwigs have been reported to date: Anisolabis howarthi Brindle, 1980 (Anisolabididae) of Hawaiian lava caves and Anataelia troglobia Martín and Oromi, 1988 (Pygidicranidae) of a lava cave in La Palma, Canary Islands. These species exhibit the characteristics of true cavernicolous insects, including reduced, apparently non-functional compound eyes, slender appendages, and a less-pigmented integument (
Haplodiplatys milloti (Chopard, 1940) (Haplodiplatyidae), which has been exclusively reported from an entirely dark part of an African cave, has well-developed compound eyes, while the integument is pale and the appendages are slenderer than in related species (
Conversely, eyeless earwigs do not necessarily occur in caves. Anophthalmolabis spp. (Anisolabididae) (
Members of the family Arixeniidae are also considered trogrophilic. These species are phoretic on bats (Cheiromeles torquatus Horsfield, 1824) or are found on bat guano (
Most earwigs found in caves are considered troglophiles that show no apparent specialization for life in dark environments (
As one of the most species-rich areas in the world, approximately 150 species of earwigs have been reported from Brazil (
The 93 dermapteran specimens examined in this study were collected from 2000 to 2015 during surveys of Brazilian cave fauna. All samples were collected manually. Most caves were visited only once in the inventories of subterranean invertebrates conducted in different research projects. Several samples were collected by consulting companies or governmental institutions (ATIVO AMBIENTAL, CARSTE, SPELAYON, or CECAV), for which detailed environmental conditions of the locality are unknown.
All samples were preserved in 70% ethanol after collection, and therefore the body color of some specimens was bleached. To examine wing and genital structures, several adult samples were dried after mounting on cardboard using fish glue. Genitalia were removed from specimens, mounted in Euparal (Waldeck GmbH and Co. KG, Münster, Germany) between two coverslips, and attached to the pin of the respective specimen.
All of the samples examined in this study have been deposited in the Subterranean Invertebrate Collection of Lavras (ISLA), of the Universidade Federal de Lavras (UFLA), Lavras, Brazil, with assignment of sample numbers shown in parentheses below, with the exception of some comparative samples from other depositories.
We follow
Male genitalia
dp denticulated pad
ho horn
pm paramere
rsc rectangular sclerite
tp toothed plate
vg virga
Female genitalia
ap anal plate
gl9 gonoplac (=coxal lobe) IX
gp8 gonapophysis VIII
gp9 gonapophysis IX
lp lateral plate
sa spined area
sp spermatheca
tg10 tergum X
Wing structures
AA3 anal anterior 3
AA4 anal anterior 4
AP anal posterior
BAA1+2 anal anterior 1 + 2 basivenale (anal brace)
BAA3+4 anal anterior 3 + 4 basivenale
C costa
CuA cubitus anterior
CuP cubitus posterior
FAJ anojugal fulcalare
JA jugal anterior
Depositories
ISLA Invertebrados Subterrâneos de Lavras (Subterranean Invertebrates, Lavras) of UFLA
MM Manchester Museum, UK
UFLA Federal University of Lavras, Brazil
YK personal collection of Y. K.
Apart from Cylindrogaster, for which a new species is described, eight organisms were recorded in this study; however, only four were determined to the species level, while four were determined to the (sub)family level.
Holotype ♂, ‘Gruta Apertar | da Hora | Jandaíra RN <= Rio Grande do Norte>’, ‘ISLA | 21101’, ‘15.ii.2010 | Ferreira, R.L. leg.’, ‘HOLOTYPE (male) | Cylindrogaster cavernicola | sp. n. | Det. Y. Kamimura 2017’.
Cylindrogaster cavernicola sp. n. is a median-sized species with a slender abdomen and simple forceps. This species differs from all other species of Cylindrogaster with the combination of the following characters: the well-developed tegmina; pronotum slightly longer than broad; parameres with blunt apices; and short but weakly sinuated virgae.
Male (holotype: Fig.
1-7 Cylindrogaster cavernicola Kamimura, sp. n. (male, holotype): habitus (1), head and thorax (2), tegmina and wings (3), penultimate sternite (4), ultimate tergite and forceps (5), and genitalia (6, 7) 8, 10 Cylindrogaster thoracicus (MM 3637; collected from Itatiaia, Brazil; det. W. D. Hincks): head and thorax (8), and genitalia (10) 9, 11 Cylindrogaster gracilis: head and thorax (9: MM 3677; collected from Itatiaia, Brazil; det. W. D. Hincks), and genitalia (11: MM 3565; collected from Minas Gerais, Brazil; det. W. D. Hincks). Scale bars 3 mm for Fig. 1; 0.5 mm for Figs 2-6, 8-11; 200 ?m for Fig. 7.
The body color of the holotype seems to have been bleached by preservation in ethanol. Body color uniformly pale amber but abdomen darker. Body, including forceps, sparsely pubescent.
Head (Fig.
Female. Unknown.
The subfamily Cylindrogastrinae consists of six species belonging to the Neotropical genus Cylindrogaster (
Proposed classification systems for the infraorder Protodermaptera Zacher, 1910.
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This study |
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Pygidicranidae | Pygidicranidae | Pygidicranidae | Pygidicranidae | Pygidicranidae | Pygidicranidae |
Anataeliinae | Anataeliinae | Anataeliinae | Anataelinae | Anataeliinae | Anataelinae |
Blandicinae | Blandicinae | Blandicinae | Blandicinae | Blandicinae | Blandicinae |
Brindlensiinae | Brindlensiinae | Brindlensiinae | Brindlensiinae | ||
Chaliinae | Challiinae | Chaliinae | Challiinae | Chaliinae | |
Echinosomatinae | Echinosomatinae | Echinosomatinae | Echinosomatinae | Echinosomatinae | Echinosomatinae |
Prolabiscinae | (= Prolabiscinae) | Prolabiscinae | |||
Esphalmeninae | Esphalmeninae | Esphalmeninae | Esphalmeninae | Esphalmeninae | Esphalmeninae |
Pygidicraninae | Pygidicraninae | Pygidicraninae | Pygidicraninae | Pygidicraninae | Pygidicraninae |
Pyragrinae | Pyragrinae | Pyragrinae | Pyragrinae | Pyragrinae | Pyragrinae |
Diplatymorphinae | |||||
Cylindrogastrinae | |||||
Karschiellinae | Karschiellinae | Karschiellinae | Karschiellinae | Karschiellidae | Karschiellidae |
Haplodiplatyidae (sensu |
|||||
Diplatyidae (sensu lato) | Diplatyidae (sensu stricto) | Diplatyidae | |||
Diplatyinae | Diplatyinae | Diplatyinae | Diplatyinae | Diplatyinae | |
Diplatymorphinae | (= Diplatymorphinae) | Diplatymorphinae | |||
(= Cylindrogastrinae) | (= Cylindrogastrinae) | Cylindrogastrinae | Cylindrogastrinae | Cylindrogastrinae |
This new species is allied to C. gracilis Stal, 1855, which was recorded from Brazil (and also possibly from Peru). However, the virga is entirely straight and the parameres are much wider than the length in the latter species (Fig.
1 | Tegmina reduced to small lateral flaps. Ultimate tergite strongly inflated. Forceps well developed, so-called macrolabic | Cylindrogaster bicyclurus |
– | Tegmina not reduced, well developed, normal. Ultimate tergite not or little inflated. Forceps, so-called microlabic | 2 |
2 | Parameres of genitalia triangular with pointed apex | 3 |
– | Parameres of genitalia trapezoid or oval, broader than long, with blunt apex | 4 |
3 | Virga short but sinuated, with a characteristic projection at middle | Cylindrogaster sahlbergi |
– | Virga short, curved but not sinuated, without a characteristic projection at the middle | Cylindrogaster yepezi |
4 | Pronotum (excluding anterior zone tapering to head) apparently longer than broad (Fig. |
5 |
– | Pronotum (excluding anterior zone tapering to head) almost quadrate or slightly longer than broad (Figs |
6 |
5 | Pronotum (excluding anterior tapering region) more than 1.5 times longer than broad. Virga straight, very short, almost half as long as penis lobe | Cylindrogaster velox |
– | Pronotum (excluding anterior tapering region) less than 1.5 times longer than broad. Virga sinuated, relatively long (Fig. |
Cylindrogaster thoracicus |
6 | Virga simple, straight, almost as long as penis lobe (Fig. |
Cylindrogaster gracilis |
– | Virga very short, almost half as long as penis lobe, but weakly sinuated (Figs |
Cylindrogaster cavernicola Kamimura, sp. n. |
The species epithet refers to the cave-dwelling habit of this new species, although it is presently unknown whether it is a troglobite.
Rio Grande do Norte, Brazil.
The specimen of Cylindrogaster cavernicola Kamimura, sp. n. was collected near the entrance of a cave associated with limestone rocks from the Jandaíra formation (Upper Cretaceous) in northern Rio Grande do Norte state. The caves in this region are predominantly shallow, most of which present several connections with the epigean environment (usually vertical cracks in the limestone outcrops). Accordingly, many caves in the area are strongly influenced by the external environment. Even so, given the extremely dry external environment, the caves represent a more suitable habitat for many animal species, presenting more stable temperatures and higher humidity than the epigean habitat. Furthermore, although the macro-caves are more influenced by the epigean environment, they are connected to huge systems of meso-caves, comprising small passages that are much more stable.
1 ♀, Gruta Túneis, Lagoa Santa, Minas Gerais, 10.x.2011, Ferreira, RL leg. (ISLA 43365).
The female specimen was collected near the entrance of a cave of the Sumidouro state park, located in Lagoa Santa, Minas Gerais state. Numerous nymphs presumably belonging to this species were observed throughout the years, especially on the cave walls in areas close to entrances, in the limestone caves of this region. Therefore, it is possible that this species uses the caves as a protected habitat during its development, but leaves the caves when reaching adulthood. They probably prey upon small invertebrates that are found on the walls near the entrances.
In this study, two adult females of Cylindrogaster were examined. Based on differences in body size and genital structures (see below), these two females are not conspecific. The characteristics for species diagnosis have not been established for female Cylindrogaster spp. In addition, because the collection localities of both female samples (from Minas Gerais and Pará states, respectively) are quite far from the type locality of C. cavernicola sp. n. (Rio Grande do Norte state), these female samples are tentatively treated as Cylindrogaster sp. 1 (Figs
12–17 Cylindrogaster sp. 1 (female): habitus (12), spiny ridges (indicated by the blue arrowheads) on the mesothorax (13), wing base of the left hindwing (14), and genital regions (15–17) 18–21 Cylindrogaster sp. 2 (female): habitus (18), spiny ridges (indicated by the blue arrowheads) on the mesothorax (19), fustis of the left hindwing (20), and genital regions (21) 22 Cylindrogaster sp. (nymph): detail of cercus. Scale bars 3 mm for Figs 12, 18; 0.5 mm for Figs 13–15, 19–22; 200 μm for Figs 16, 17.
Wing and female genital structures have not been reported for any members of Cylindrogaster. The female genital region of Cylindrogaster sp.1 is characterized by having shorter gonapophysis VIII (gp8) than gonapophysis IX (gp9), which was slightly shorter than the finger-like gonoplac IX (gl9) (Figs
The spermatheca of Cylindrogaster sp. 1 consisted of long thin tubes (Fig.
According to Hass and Kukalová-Peck (2001), Diplatyidae (Diplatys) and Haplodiplatyidae (Haplodiplatys) are separated from other members of the infraorder Protodermaptera by the presence of (1) a narrow, slender, and elongated fustis head, (2) a long and slender costal area, (3) a concave and strongly three-dimensional anojugal arm (FAJ: anojugal fulcalare), (4) the distal end of CuA3+4 (cubitus anterior 3 and 4) lying between the 8th and 9th branches of AP1+2 (anal posterior 1 and 2), and (5) two proximal branches of AP1+2 diverging close together. The characteristics unique to Diplatyidae and Haplodiplatyidae (1–3) were observed in Cylindrogaster sp. 1 (Fig.
The genus Haplodiplatys (Haplodiplatyidae) is characterized by multiple plesiomorphic features, including laterally symmetrical tegmina and absence of a spiny ridge (a component of the tegmina-locking device) on the dorsal side of the mesothorax (Hass and Kukalová-Peck 2001). The female sample of Cylindrogaster sp. 1, however, possessed well-developed spiny ridges (Fig.
1 ♀, Cave N5SM1-017, Parauapebas, Pará, 17.ii.2011, CARSTE leg. (ISLA 15558).
The specimen was found in the cave N5SM1-017 (also known as GEM-1190 cave). This cave consists of a shallow iron ore cave (14 m horizontal projection), located in Carajás region (Pará state, Brazil). The surrounding vegetation is composed of Amazon forest with a dense canopy. The cave has only one wide and shaded entrance, with the presence of vegetation (lichens, moss, and ferns). Furthermore, it does not present an aphotic zone, being lightened throughout its whole extension. The litter is abundant near the entrance zone and sparse in the rest of the cavity. Several caves were sampled in this region, and as a single specimen was found, it is likely that this species is accidental or seeks only temporarily shelter in caves.
The genital structures of this species are essentially similar to those of Cylindrogaster sp. 1, but the spermatheca was missing likely due to incorrect dissection. Cylindrogaster sp. 2 differs from Cylindrogaster sp. 1 in having triangular shaped gl9 (Fig.
1 nymph, Cavidade RF 86, Barão de Cocais, Minas Gerais, 9.ii.2015, ATIVO AMBIENTAL leg. (ISLA 15507) – 1 nymph, Cavidade CBT_09, Barão de Cocais, Minas Gerais, 19.i.2015, ATIVO AMBIENTAL leg. (ISLA 15508) – 1 nymph, S11D, S11D-0003, Serra / Sul, Canaã dos Carajás, Pará, 16.xii.2014, CARSTE leg. (ISLA 17201) – 1 nymph, Gruta da Lapinha, Lagoa Santa, Minas Gerais, 7.vii.2011, Ferreira, RL leg. (ISLA 21083) – 3 nymphs, Cave GEM-1194, Parauapebas, Pará, 23.ii.2011, CARSTE leg. (ISLA 21087) – 1 nymph, CAPA 03, Itabirito, Minas Gerais, 11.xi.2013, SPELAYON leg. (ISLA 21088) – 1 nymph, Cave Mll GEM-1705, Parauapebas, Pará, 13.iv.2011, CARSTE leg. (ISLA 21091) – 2 nymphs, Cave Mll GEM-1738, Parauapebas, Pará, 3.xi.2011, CARSTE leg. (ISLA 21092) – 1 nymph, Cave Mll GEM-1694, Parauapebas, Pará, 20.iii.2011, CARSTE leg. (ISLA 21095) – 4 nymphs, Didi Vieira cave, Afonso Cláudio, Espírito Santo, 23.iii.2005, Souza MS et al. leg. (ISLA 21098) – 1 nymph, Sitio Paraíso cave, Ecoporanga, Espírito Santo, 22.vii.2004, Souza MS et al. leg. (ISLA 21099) – 2 nymphs, Gruta do Roxo, Novo Oriente de Minas, Minas Gerais, 20.vii.2002, Souza MS et al. leg. (ISLA 21100) – 1 nymph, SEP-0407 (Geraldo Gusso), Felipe Guerra, Rio Grande do Norte, 2.x.2010, Ferreira, RL leg. (ISLA 21102) – 1 nymph, Lapa de Urtiga, Vazante, Minas Gerais, 16.ix.2010, Ferreira, RL leg. (ISLA 2735).
Remarks. A total of 21 nymphs of Cylindrogaster were examined. Nymphal cerci were frequently lost in these specimens, but when present, they were always segmented instead of unsegmented forceps of adults (Fig.
Species diagnosis has not been established for nymphal samples of Cylindrogaster spp.
3 ♂♂, 6 ♀♀, 7 nymphs, Gruta dos Farias cave, Barbalhas, Ceará, 30.iv.2007, Ferreira, RL leg. (ISLA 15565) – 1 nymph, Cave GEM-1623, Parauapebas, Pará, 16.iii.2011, CARSTE leg. (ISLA 21085) – 1 nymph, Gruta Ecos cave, Cocalzinho de Goiás, Goiás, 4.iv.2006, CECAV leg. (ISLA 21096).
While most earwigs found in Brazilian caves seem to be accidental, this species was present as a large population within Gruta dos Farias cave, a sandstone cave located in Barbalhas municipality (Ceará state, Brazil). Many adults and nymphs were observed only in guano piles in deeper areas of the cave, which has a stream trespassing its entire conduit, strongly suggesting that the population is troglophilic. They are likely feeding on bat guano or preying upon small invertebrates.
All adult specimens examined in this study had fully developed tegmina, but lacked hind wings. Four species of Euborellia from the Neotropical region, E. boliviana Brindle, 1971, E. ambigua (Borelli, 1906), E. caraibea Hebard, 1921, and E. janeirensis, also have such characteristics. Among these species, E. janeirensis is distinguished from the others by the presence of well-developed lateral longitudinal ridges on the male abdominal tergites VI and IX, and one or more white/yellow distal antennal segments (
23–26 Euborellia janeirensis (male): habitus (23), penultimate sternite + manubrium (24), and genitalia (25, 26) 27–28 Euborellia janeirensis (female): habitus (27), and spermatheca (28) 29–32 Euborellia brasiliensis (male): habitus (29), penultimate sternite + manubrium (30), and genitalia (31, 32) 33Anisolabididae gen. sp. 1 (female): habitus 34Anisolabididae gen. sp. 2 (nymph): habitus 35Anisolabididae gen. sp. 3 (nymph) habitus. Scale bars 3 mm for Figs 23–25, 27, 29, 30, 33–35; 0.5 mm for Figs 26, 28, 31; 100 μm for Fig. 32.
Taxonomists generally examine only the terminal region of the male genital organs. The male genitalia of E. janeirensis were approximately 22 mm in length, and more than twice the body length with forceps (Fig.
Males of Euborellia spp. directly insert the elongated virga into the female spermatheca during copulation (
Brazil, Argentina, Paraguay, and Venezuela.
2 ♂♂, 2 nymphs, Gruta dos Coelhos cave, Lima Duarte, Minas Gerais, 11.vii.2005, Ferreira, RL leg. (ISLA 15564).
This species was found in deeper areas (aphotic zones) of Gruta dos Coelhos and Gruta do Pião caves, both associated with quartzite rocks and located in the Ibitipoca state park (Lima Duarte municipality, Minas Gerais state, Brazil). In the latter cave, several individuals were found walking near root masses, probably searching for prey. There are several caves in the area, and at least three distinct inventories of cave fauna were performed over the last 10 years. However, this species was only found in two caves, suggesting that, although probably not accidental, their association with subterranean habitats is uncommon.
This apterous anisolabidid species from Brazil (Fig.
Currently Heterolabis Borelli, 1912 is considered a synonym of Euborellia, and the species previously considered as members of Heterolabis is as follows:
1. Euborellia brasiliensis (Borelli, 1912):
Synonym: Heterolabis brasiliensis Borelli, 1912
2. Euborellia srivastavai Sakai, 1987
Synonyms: Heterolabis punctata Srivastava, 1978; Epilabis harlequin Steinmann, 1989 (junior objective synonym); Euborellia mindanoensis Srivastava, 1999 (junior objective synonym).
The generic name Heterolabis Borelli, 1912 is an invalid homonym of Heterolabis Kriechbaumer, 1889 (Ichneumonidae).
Brazil.
1 ♀, cave SERP 0100, Conceição do Mato Dentro, Minas Gerais, 26.v.2014, SPELAYON leg. (ISLA 15557).
Unknown.
The tegmina and wings were fully developed (Fig.
2 nymphs, Gruta Ecos cave, Cocalzinho de Goiás, Goiás, 4.iv.2006, CECAV leg. (ISLA 21097) – 1 nymph, Cave GEM-1710, Parauapebas, Pará, 14.iii.2011, CARSTE leg. (ISLA 21086) – 1 nymph, cave SERP 0100, Conceição do Mato Dentro, Minas Gerais, 26.v.2014, SPELAYON leg. (ISLA 21082).
Unknown.
Four nymphs, with well-developed wing primordia and some whitish antennal segments, were examined. Being recorded from Goiás, Pará, and Minas Gerais states, this species is possibly distributed widely in Brazil. Otherwise, several species may be mixed in this tentative species.
1 nymph, cave RF 103, Barão de Cocais, Minas Gerais, 16.i.2015, ATIVO AMBIENTAL leg. (ISLA 15505).
Unknown.
Only one young nymphal specimen was collected. This species is characterized by a brownish stripe straddling the long axis of the compound eye.
1 nymph, Cave Mll GEM 1712, Parauapebas, Pará, 30.x.2011, CARSTE leg. (ISLA 21093).
Unknown.
This species is tentatively assigned to the family Spongiphoridae. Only one young nymph, which lacked the post-abdomen including the forceps, was examined. The antennae are characteristically stout.
(= Paralabella Steinmann, 1990; see Kevan and Vickery 1997)
2 ♂♂, 9 ♀♀, 8 nymphs, Cave N5SM2-099 (= GEM-1799 cave), Parauapebas, Pará, 5.v.2011, CARSTE leg. (ISLA 15563) – 1 ♀, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 31.x.2010, CARSTE leg. (ISLA 15562) – 3♀, Cave N5SM2-099 (= GEM-1799 cave), Parauapebas, Pará, 31.x.2010, CARSTE leg. (ISLA 15560) – 1 ♂, 2 ♀♀, 8 nymphs, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 5.v.2011, CARSTE leg. (ISLA 15561) – 1 nymph, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 31.x.2010, CARSTE leg. (ISLA 21084) – 1 nymph, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 5.v.2011, CARSTE leg. (ISLA 21089) – 1 nymph, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 5.v.2011, CARSTE leg. (ISLA 21090) – 3 nymphs, Cave N5SM2-019 (= GEM-1739 cave), Parauapebas, Pará, 31.x.2010, CARSTE leg. (ISLA 21094).
Many specimens of P. dorsalis were found in two iron ore caves (N5SM2-019 cave – synonym of GEM-1739 cave, and N5SM2-099 cave – synonym of GEM-1799 cave), both located in Carajás region (Pará state). These caves occur in an iron ore plateau surrounded by the Amazon forest. However, they are in an area of metallophilic savannah, a vegetation type usually found at the top of plateaus. The caves are considerably large (> 100 m in horizontal projection) compared to other caves in the area. Although many caves were sampled in the plateau (at least 100 caves), this species was found in only these two caves, which contain huge colonies of the insectivorous bat genus Pteronotus (Pteronotus gymnonotus Wagner, 1843, in the N5SM2-019 cave and Pteronotus parnellii (Gray, 1843) in the N5SM2-099 cave). These colonies produce large guano piles, where several individuals of P. dorsalis were observed. The populations of P. dorsalis, which include both adults and nymphs, were observed in both dry and rainy seasons in the two caves, strongly suggesting that they are troglophilic.
The external morphologies and genital structures of male and female specimens were examined (Figs
36–38 Paralabellula dorsalis (male): habitus (36), forceps (dorsolateral view) (37), and genitalia (38) 39–41 Paralabellula dorsalis (female): habitus (39), spermatheca and spiny area in the genitalia (40, 41). Repaired wound patches are indicated by the red arrowheads in Figs
Based on samples collected from Costa Rica,
Using specimens fixed during copulation,
West Indies, Mexico, Costa Rica, Panama and northern South America (including Brazil).
1 ♀, Gruta do Vento cave, Pains, Minas Gerais, 12.x.2000, R. L. Ferreira leg. (ISLA 495) – 1 ♀, Gruta Zé Geraldão cave, Pains, Minas Gerais, 10.iii.2009, R. A. Zampaulo leg. (ISLA 534).
Doru luteipes is an extremely common species in Brazil (
Only female samples of Doru, which are difficult to identify to the species level, were collected in this study. The external morphologies (Fig.
Colombia, Surinam, Brazil, Peru, Bolivia, and Argentina.
Of the five taxa identified to the species level in this study, E. brasiliensis and D. luteipes may be accidental inhabitants of caves, while E. janeirensis and P. dorsalis likely maintain permanent cave populations, but being also found in various non-cave habitats (troglophiles).
At present the association to cave habitats is unknown for C. cavernicola sp. n. The species does not present any obvious troglomorphic traits. However, subterranean species do not always possess obvious troglomorphic traits, especially when associated with shallow subterranean habitats.
The association of Dermaptera with bat guano in caves has been reported for some species around the world: large populations of Arixenia esau Jordan, 1909 associated with bat guano piles in Niah caves, Sarawak (
In the present study, the wing and female genital structures are described for Cylindrogaster spp. for the first time. Well-developed ovipositor components [gonoplacs (= coxal lobes) and gonapophyses of the 8th and 9th abdominal segments (gl8, gl9, gp8, and gp9, respectively)] are considered plesiomorphic in Dermaptera (
In conclusion, multiple genital and wing traits (see “Remarks” of Cylindrogaster sp. 1 and Cylindrogaster sp. 2), as well as segmented nymphal cerci, suggested a close relationship between Cylindrogastrinae and Diplatyinae (or Diplatyidaesensu stricto). These two groups in the Protodermaptera also had depressed femora with lamelliform edges, an arolium between the claws, and short antennae with fewer than 25 segments (
The subfamily Cylindrogastrinae was originally erected in the family Pygidicranidae (
We are grateful to the team of the Center of Studies in Subterranean Biology from the Federal University of Lavras (CEBS/UFLA) for their efforts in sampling earwigs in Brazilian caves. We also thank Kazunori Yoshizawa, Shigehiko Shiyake, and Dmitri V. Logunov for their help with specimen examination, Kyohei Watanabe for advice on the present status of the genus Heterolabis (Ichneumonidae), and Petr Kočárek, Christophe Girod, and Masaru Nishikawa for useful comments on a previous version of the manuscript. This study was partly supported by JSPS research grants (Kakenhi Nos. 15H04409 [head, Kazunori Yoshizawa] and 15K07133) to YK and CNPq grant (n.304682/2014-4 from the Conselho Nacional de Desenvolvimento Científico e Tecnológico) to RLF.