Corresponding author: Claudia Hemp ( firstname.lastname@example.org )
Academic editor: Susanne Randolf
© 2016 Claudia Hemp, Klaus-Gerhard Heller, Elzbieta Warchalowska-Sliwa, Andreas Hemp.
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: Hemp C, Heller K, Warchalowska-Sliwa E, Hemp A (2016) Spotted males, uniform females and the lowest chromosome number in Tettigoniids recorded: Review of the genus Gonatoxia Karsch (Orthoptera, Phaneropterinae). Deutsche Entomologische Zeitschrift 63(2): 271-286. https://doi.org/10.3897/dez.63.10799
The genus Gonatoxia Karsch, which was synonymized with Dapanera Karsch by
Taxonomy, new species, biogeography, acoustics, biology, chromosomes, speciation, bioindication
Lowland and coastal forests in East Africa are diminishing rapidly although their importance as hotspots of biodiversity and endemism are acknowledged (
Until recently species of the genus Gonatoxia were poorly collected and little or no data were available on their biology, habitat or chromosomes.
Measurements. The total body length refers to the body length of the insect without tegmina. In females the ovipositor is not included in the body length, its length is taken from the tip to the base of the subgenital plate not considering the curvature. Length of tegmina are taken from above.
Depositories. NHML: British Museum, Natural History, London, U.K.
Acoustics. Songs were recorded in the laboratory using a digital bat detector (Pettersson D1000X) with sampling rates between 100 and 192 kHz and, additionally, a Sony ECM-121 microphone (frequency response relatively flat up to 30 kHz; own tests) connected to a personal computer through an external soundcard (Transit USB, “M-Audio”; 64-kHz sampling rate).
Specimens recorded. Gonatoxia helleri sp. n./Hemp 2016: Tanzania, Udzungwa Mts., 6 males (3 collected in the field, 3 reared from nymphs), Tanzania, Uluguru Mts, 4 males, Tanzania, Nilo forest reserve, 2 males. Gonatoxia maculata
Song measurements and sonograms were obtained using AMADEUS II and AMADEUS Pro (Martin Hairer; http://www.hairersoft.com). Oscillograms of the songs were prepared using TURBOLAB (Bressner Technology, Germany). All recordings were made at temperatures between 20 and 27 °C. The singers were caged in plastic tubes, wire mesh cages or gauze cages with microphone fixed or hand held at distances between 5 and 60 cm. Data are presented as mean ± standard deviation.
Terminology. Syllable: sound produced during one cycle of movements (opening and closing of the tegmina), in Gonatoxia equivalent to a pulse; echeme: first order assemblage of syllables; pulse: undivided train of sound waves increasing in amplitude at the beginning and containing many similarly sized wave maxima and minima (cricket-like song structure; example see Fig.
Chromosomes. G. maculata (еleven males and one female), G. immaculata (two males and two females), G. furcata sp. n. (one male) and G. helleri sp. n. (twelve males and seven females) were used for classical cytotaxonomic analyses. Chromosome preparation was obtained from adult gonads and gastric caeca. Testes, ovaries and gastric caeca were excised, incubated in a hypotonic solution (0.9% sodium citrate), fixed in ethanol - acetic acid (3:1, v/v) and stored at 2 °C until use. The fixed material was squashed in 45% acetic acid. Cover slips were removed by the dry ice procedure and then preparations were air dried. Constitutive heterochromatin was revealed by the technique as described by
Until recently little material was available in museum collections from the two known species of Gonatoxia. Now specimens of G. maculata were collected on Mt Kilimanjaro (
Habitus of Gonatoxia species. A, B. Male (A) and female (B) of G. maculata, Rau forest Kilimanjaro. Male with maculae on tegmina, female (B) showing the bright yellow tergites of abdomen, typical for all Gonatoxia species. C. Female G. immaculata, Kazimzumbwi Forest Reserve, Kisarawe near Dar es Salaam D. Female G. furcata sp. n., lowland forest Udzungwa Mountains, Morogoro District, Tanzania.
Аll Tanzania, 1 male, Mt Kilimanjaro, southern slopes, Msaranga valley, submontane riverine forest relicts, 1300 m, April 2011; 4 females, Mt Kilimanjaro, western slopes, Sanja Juu, 1300 m, savanna woodland May 2013; 3 males, 3 females, Mt Kilimanjaro, southern slopes, Rau forest near Moshi, lowland wet forest, 800 m, March, July, August, December 2014 and July 2015; 3 males, 4 females, North Pare Mountains, southern slopes, Lembeni, dry deciduous woodland, 1250 m, March, May, August 2013, May, November 2014 and July 2015; 1 female, Mt Kilimanjaro, southern slopes, Mabungu Hill, savanna woodland, 910 m, December 2013; 2 females, Mt Kilimanjaro, eastern slopes, Kirua, submontane savanna woodland 1300 m, July 2014; 1 female, Mt Kilimanjaro, eastern slopes, Holili, savanna woodland, 1300 m, June 2013 (collection C. Hemp).
1 male, Somalia, Afgoi, Feb-March 1978, coll. A. Simonetta, B.M. 1979-543; 1 male, Kenya, Mombasa, coll. W. L. Sclater, 1911-7. Depository NHML.
Males are characterized by a median deeply incised subgenital plate. The styli are long and slender and about 1.5 times longer than the median incision (Fig.
Morphological details of male Gonatoxia species. A–C. G. maculata, apex, semilateral view (A), dorsal view on cerci and apex (B), subgenital plate (C) D–F. G. immaculata, dorsal view on apex (D), right cercus (E), subgenital plate (F) G–I. G. furcata sp. n., semilateral view on apex (G), left cercus (H) and subgenital plate (I).
Stridulatory files of male G. maculata (A), G. immaculata (B) and G. helleri sp. n. (C). The arrow points a the discontinuity (elevation midway) typical for G. helleri sp. n. Scale bar 0.5 mm.
Pronotum and mirror area of male G. maculata (A, B) and male G. helleri sp. n. (C, D). Differences are small, the mirror of G. helleri sp. n. being more shiny and translucent. Scale bars 5 mm.
General habitus and colour. Predominantly green with broad oval tegmina and strongly up-curved ovipositor. Venation of tegmina often light green and often with tiny white dots scattered over tegmina, thus resembling a leaf perfectly. Whitish dots also on pronotum and legs. A pair of yellowish to whitish lines often present starting in upper part of compound eye and running over head and pronotum. Abdominal tergite bright yellow (2 B), tarsi whitish. Head and antennae. Antennae thin and whitish, surpassing tegmina. Eyes round, except for yellowish-whitish upper part green or brown-green. Thorax. Pronotal disc flat, longer posteriorly than pronotal lobes which are evenly rounded at lower part, with acute edge at insertion of tegmina and wings. Tegmina broad with leaf-like pattern of veins, truncate at tips, alae surpassing tegmina. Alae hyaline except for tips which are of same green colour than tegmina. Stridulatory teeth on the right tegmen for female response to male calling song as in Fig.
Right tegmen with stridulatory veins of female Gonatoxia species A. G. maculata B G. immaculata C G. helleri sp. n. D G. furcata sp. n. Scale bars 5 mm.
Lateral view on ovipositor of female Gonatoxia species. Note bowl-like structures laterally (arrows) A. G. maculata B. G. immaculata C. G. furcata sp. n. D. G. helleri sp. n. Scale bars 1 mm.
Bowl-like structures lateral at base of ovipositors of female Gonatoxia species. A. G. maculata B. G. helleri sp. n. C. G. immaculata D. G. furcata sp. n. Scale bars 1 mm.
Subgenital plates of female Gonatoxia species. A. G. maculata B. G. immaculata C. G. helleri sp. n. D. G. furcata sp. n.
Nymphs similar to adults (Fig.
Females (n = 5): Total length of body: 21.5–28.8; median length of pronotum: 6.1–6.3; length of hind femur: 26.2–27; length of tegmina: 41.8–44.7. Width of tegmina: 13.3–14.6; ovipositor: 5.3–5.8.
Since only data for the holotype male of G. maculata are available at present, we provide more measurement data.
Males (n = 8): Total length of body: 23–28 (holotype 30); median length of pronotum: 6.1–6.6 (holotype: 7); length of hind femur: 25–27 (holotype 25); length of tegmina: 41–43.7 (holotype 41); width of tegmina: 10.3–14 (holotype 11.5).
A pair from Kilimanjaro mated on the 19th of November 2014. Mating only took a couple of minutes. A spermatophore containing a two-parted spermatophylax was transferred to the female (Fig.
Pair of Gonatoxia maculata shortly after mating. Note the white spermatophore at the abdomen of the female.
In two matings (one male, two females; interval about two months) of culture-reared specimens the male weighed 1584 and 1590 mg and the females 1950 and 1830 mg (all before mating) and the two-parted spermatophores 214 and 169 mg (each value mean of male weight loss and female weight gain).
Savanna woodlands and deciduous dry forest up to submontane elevations.
Tanzania, Kenya, Somalia.
Female Holotype, Usambara,
Tanzania: 1 male, 4 females, Pwani Region, Kisarawe District, Kazimzumbwi Forest Reserve, 150 m, February and July 2015. 2 males, East Usambara Mountains, Nilo forest reserve, December 2015 and May 2016; 1 male, East Usambara Mountains, Sigi Trail, 450 m, lowland wet forest, November 2015 (Collection C. Hemp). 1 female, Kenya, Rabai, coll. A.F.J. Geydte Jan-Feb 1929 (NHML).
Color dark and shiny green, with few ivory to orange patches on tegmina; tergites of abdomen vivid yellow, venter whitish to light green; fore femora dorsally light brown, same colour as tarsi (Fig.
Gonatoxia immaculata male, East Usambara Mountains. Note the orange patches on the tegmina and the deep green shiny colour.
Similar as male in habitus and colour. Stridulatory veins as in Fig.
Nymphs similar to adults (Fig.
Females (n = 3): Total length of body: 23.8–25 (holotype: 27); median length of pronotum: 5.4–6.1 (holotype: 6); length of hind femur: 20–21.5 (holotype: 24); length of tegmina: 35.7–37.4 (holotype: 42). Width of tegmina: 12.1–12.6 (holotype: 14); ovipositor: 5–5.2 (holotype: 5).
Males (n = 2): Total length of body: 24–29; median length of pronotum: 6.2–6.7; length of hind femur: 21; length of tegmina: 36.2–42.3; width of tegmina: 11–13.5.
When first males of G. immaculata were collected it became clear that specimens coming from Kazimzumbwi Forest Reserve belonged to G. immaculata. Thus the specimens from the spirit collection of the Zoological Museum Copenhagen listed as G. maculata from Kazimzumbwi Forest Reserve in
Lowland wet forest to submontane wet forest.
Coastal Tanzania, East and West Usambara Mountains.
Tanzania, Morogoro District, Udzungwa Mountains, National Park Headquarters, Mangula Gate, 300 m, lowland wet forest, July 2015. Depository
Paratype female, same data as holotype but March 2015. Depository
3 females, same data as holotype, May and June 2016 (collection C Hemp). 1 male (in alcohol), Tanzania, Iringa Region, Mufindi District, Udzungwa Scarp Forest Reserve, 08°31.5’S 35°53.9’E, 750 m, March 1996, McKamey et al. leg., depository
Females of G. maculata, G. immaculata and G. furcata sp. n. are very similar. Differences are seen in the general coloration especially when specimens are alive. G. maculata and G. helleri sp. n. females are of lighter green colour while those of G. immaculata and especially G. furcata sp. n. are darker green and the tegmina shiny (Fig.
Males are distinguished when comparing the outer genitalic morphology. In G. maculata the cerci are evenly tapering to their apices, the tips wearing a short and straight serrated ridge (Fig.
Left wings of male G. maculata (A), G. helleri sp. n. (B), G. immaculata (C) and female G. furcata sp. n. (D). Morphological differences beteen G. maculata and G. helleri sp. n. are small. However, usually G. maculata (A) have more and larger maculae on the tegmina while G. helleri sp. n. (B) have fewer maculae that are smaller and longish and usually start where Rs branches off (right arrow). Also G. helleri sp. n. has a white borderd costal margin with veins branching off white and thickened (left arrow).
Color dark and shiny green, with few ivory patches on tegmina; tergites of abdomen vivid yellow, venter whitish to light green; fore femora dorsally light brown, same colour as tarsi, thus similar to G. immaculata. Head and antennae. Antennae thin, green, surpassing tegmina by about 1/3. Eyes round, green, with light stripe beginning in eyes, running over the head getting yellow along lateral edges of the pronotum. Thorax. Pronotal disc flat with sharp lateral edges, anterior margin v-shaped incurved, posterior margin of disc broadly rounded as described for genus (
Similar as male in habitus and colour (Fig.
Females (n=3). Total length of body: 26–27; median length of pronotum: 6.3–6.5; length of hind femur: 25–26.6; length of tegmina: 48–49; width of tegmina: 16; ovipositor: 5.5–6.
Males (n=1): Total length of body: 31.5; median length of pronotum: 6.9; length of hind femur: 25; length of tegmina: 43. Width of tegmina: 13.4.
from Latin: furca = fork because of the forked male cerci.
Lowland wet forest.
At present only known from the Udzungwa Mountains, Tanzania.
Tanzania, Uluguru Mountains, Morogoro District, forest above Morningside, February 2016. Depository
Paratype female, same data as holotype; depository
All Tanzania; 13 males, 17 females, same data as holotype, March and April 2016; 3 males, 1 female, East Usambara Mountains, Nilo forest reserve, February and May 2016; 1 male, East Usambara Mountains, Sigi Trail, lowland wet forest, 450 m, November 2015; 1 male, 4 females, West Usambara Mountains, Lutindi Mental Hospital, submontane forest, 1250 m, February 2015 and June 2016; 1, male, 1 female, West Usambara Mountains, Mazumbai forest reserve, 1600 m, March 2016; 7 males, 3 females, Udzungwa Mountains National Park, Mangula Gate, lowland wet forest, 300 m, March, July, September 2015, January, March and May 2016; 1 female, Kisarawe District, Kazimzumbwi Forest Reserve, February 2015 (collection C. Hemp).
1 male, Kenya?, Kibatuga, 20/10/51, B.M 1966–628; 1 female, East Africa 82/24, Tanzania, Korogwe-Msata Road, 103 km north of Msata, summit of kopj, 21 IX 1982, coll. N. Jago; 1 female, Tanzania, Kilosa. 10 IX 1926, coll. N. C. E. Miller, B.M. 1928–281; 1 female, Tanzania 63, B.M. 1950–96; 1 female, Tanzania, Lindi, Ndanda, 300 m , 5. III 1952, coll. Lindemann and Pavlitzki; 1 male, N Derema, coll. G. v. Son, B.M. 1969–331 (depository: NHML). The specimens from the collection of the NHML are not listed as paratypes since they were either females that are difficult to identify without males or males where the stridulatory file could not be studied.
G. helleri sp. n. is very similar to G. maculata. Both species have about the same size and colour and shape of tegmina and wings. However, G. helleri sp. n. usually have far less conspicuous maculae on the tegmina, being smaller and more longish and fewer in number. Mostly these maculae start about where the Rs vein branches off. Typical is also a dense net of white veins, especially in the costal area of the tegmen forming multiple small white dots. Also the costal margin is bordered white with veins branching off thick and very white in both sexes when alive (weakly expressed in the Udzungwa population of G. helleri sp. n.). The males of G. helleri sp. n. can also be distinguished from G. maculata by in the male cerci wearing a smaller sclerotized ridge or 1–4 single teeth clustered tightly together whereas G. maculata males wear a stouter and larger serrated ridge at the tips of the male cerci. Differences are also seen in the stridulatory file of the males. The stridulatory file of G. maculata evenly tapers in dent size from one side to the other (Fig.
Morphological details of male Gonatoxia helleri sp. n. A. Semilateral view on abdominal apex. Scale bar 1 mm B. Dorsal view on abdominal apex with sclerotized ridge of cercus. Scale bar 1 mm C. Subgenital plate. Scale bar 1 mm D. Stridulatory file. Scale bar 500 µm.
General habitus and colour. Predominantly green with oval tegmina and 2–4 small ivory patches on tegmina (Fig.
Similar to male in size but with more roundish tegmina and mostly without ivory patches on tegmina or 1–2 and very small ones, mostly where Rs branches off. Also with for this species typical costal margin bordered white with branching off veins thicker and white and net of white veins forming white dots. Stridulatory veins as in Fig.
(mg; n=1) Male 990. Female 1462 (culture-reared, 01.08.2015).
Females (n=6): Total length of body: 25.8–27.5; median length of pronotum: 6.5–6.8; length of hind femur: 26.5–28.6; length of tegmina: 44.0–45.9; width of tegmina: 14.8–14.4; ovipositor: 5.2–5.4.
Males (n=6): Total length of body: 23.5–26.4; median length of pronotum: 5.7–6.5; length of hind femur: 25–28; length of tegmina: 42.5–44.4; width of tegmina: 12.5–13.4.
Named after Klaus-Gerhard Heller.
Lowland wet to submontane forest.
Tanzania and very likely Kenya.
|1||Male cerci not scythe-shaped||2|
|–||Male cerci scythe-shaped (Fig.
||G. furcata sp. n.|
|2||Male subgenital plate deeply medially incised, styli long and slender, about 1.5 times as long as incision (Fig.
|–||Male subgenital plate not deeply medially incised, styli not longer than incision, broader and compressed||3|
|3||Cerci with short straight sclerotized ridge at tips (Fig.
||G. helleri sp. n.|
|–||Apices of male cerci inwardly curved and with long sclerotized serrated ridge (Fig.
Morphology of stridulatory organs: In the male, the slightly curved stridulatory file (Fig.
The females bear one distinct row of spines on each of several veins on the upper side of the right tegmen (Fig.
Inter-tooth spacing in stridulatory files of male Gonatoxia species (most intervals between small teeth at the anal end not measured).
Spectral composition of song: The frequency spectra of the male songs were relatively narrow-banded in all four species studied (for example see Fig.
Oscillograms of single syllables of the male calling song and corresponding spectral composition (power spectra).
Song pattern. The calling songs of all studied species consisted of short (1–4 ms), resonant syllables (Fig.
Comparison of the chromosomes of four Gonatoxia species revealed differences between their karyotypes, including the number of chromosomes (2n), the morphology of the chromosomes, the fundamental number of chromosome arms (FN) and C-banding patterns. All analyzed species show the same sex determining system: X0 (male) and XX (female) as well as the acrocentric X chromosome which is the largest element of the set.
The standard karyotypes of G. maculata and G. immaculata were characterized by a chromosome number of 2n = 29 (males) and 30 (females). All chromosomes were acrocentric, consisting of three long, four medium and seven short pairs (Fig.
The study of spermatogonial, oogonial and somatic gastric caeca mitotic metaphase of G. helleri sp. n. showed in most cells 7 chromosomes, FN = 10, 11 in the male (Fig.
C-banded mitotic metaphase of male complement of G. maculata (A), female G. immaculata (B), male G. furcata sp. n. (C) as well as both male (D, F, G) and female (E) of G. helleri sp. n. Arrows indicate biarmed chromosomes in G. furcata sp. n. (C). In G. helleri sp. n. the long polymorphic pair 2 shows three main karyomorphs in which homologous chromosomes differ in their morphology: both meta- or submetacentric (D, E), meta/submetacentric : acrocentric (F) and both acrocentric (G). X, sex chromosome. Scale bar = 10 µm.
Four species of Gonatoxia are known at present. However, further specimens stored in the entomological collection of the Natural History Museum in Vienna probably belong to new species of Gonatoxia. One male is labelled “Zanzibar”, collected by A. Horn, showing cerci with only single sclerotized dents at their tips and an unlobed subgenital plate with short styli. Until further material gets available we decided not to describe this new species.
Another male specimen identified as “Arantia spinulosa” collected by A. Horn also belongs to Gonatoxia. This specimen is labelled “MKaffa”, could thus come from Ethiopia. It is larger than G. maculata which it resembles in terms of male cerci, tegmina shape and maculation (Fig.
Comparison of G. maculata male from Mt Kilimanjaro with specimen in the collection of Vienna labeled Arantia spinulosa.
Further two specimens in Vienna were also studied, collected by Reimer labelled “DO Afrika” thus coming from Tanzania. Since the exact locality is unclear and the cerci could not be studied in detail without damaging the very old specimens a diagnosis to which species they belong is uncertain. One of the two males, however, could belong to G. immaculata since the subgenital plate agrees with males collected from the East Usambara Mountains and Kazimzumbwi Forest Reserve, the other to G. maculata. For the distribution of Gonatoxia species in East Africa see Fig.
Map of East Africa with distribution of Gonatoxia species. G. maculata in Somalia is not indicated since locality information is insufficient.
Studying a larger series of Gonatoxia specimens newly collected in Tanzania and from the entomological collections of Vienna and London showed that Gonatoxia is a very uniform genus and well separated from Dapanera which it superficially resembles. However, molecular studies on Dapanera and Gonatoxia are necessary to deepen our understanding about generic relationships, also on tribal level within Holochlorini.
The calling song of all four species of Gonatoxia consists of very short, cricket-like, resonant syllables, separated by large silent intervals, similar as in the genus Parapyrrhicia Brunner von Wattenwyl (
However, the structure of the stridulatory file of Gonatoxia differs somewhat from that of Parapyrrhicia. The distribution of the inter-tooth intervals is similar, but from the anal end onwards the file runs on a slightly elevated bulge and the teeth are larger. In the larger teeth it is clearly visible that the steep side of the asymmetric teeth are directed to the anal side (Fig.
The four species examined in this study revealed a remarkable variability in chromosome numbers and morphology. Patterns of chromosome evolution in this genus are very interesting and differ from the ancestral/model karyotype (2n = 31 in the male with acrocentric chromosomes) found in most tettigoniids (e.g.
Gonatoxia species were rarely collected, partly because they are nocturnal species, well camouflaged in the tree layer of forests and seasonal. But they are rarely collected partly also because they occur in habitats that are vanishing rapidly and also never had a large extension formerly. Gonatoxia maculata was only caught in deciduous dry forests and a vegetation type which was called “Obstgartensteppe” = orchard steppe by the Germans, since the trees are scattered and resemble superficially fruit trees planted in an orchard. Both vegetation types are rapidly vanishing in East Africa. The North and South Pare Mountains for example still harbour deciduous dry forests especially at their northern slopes. However, a rapidly increasing human population impact these forests by cutting, burning and using also steepest slopes as range land for life stock these days. The same holds true for the vegetation type “Obstgartensteppe” which is almost lost e.g. on Mt Kilimanjaro. Thus the presence of species such as Gonatoxia maculata serve as information about the vegetation types they are bound to, and therefore this species can be used as a bioindicator. The same was suggested for Tropidonotacris grandis occurring in same habitat types as G. maculata (
Species such as Gonatoxia, Parapyrrhicia and Tropidonotacris may be used as bioindicators allowing to follow land cover changes over time since early collections reach back as far as the 18th century. Thus the evaluation of old collections are precious archives providing multiple data to e.g. model scenarios of how land cover changed over time and to identify areas which once harboured habitats rich in biodiversity, e.g. for restauration programmes. Thus even few specimens of certain species as shown above for the Vienna collection holding a couple of specimens of different Gonatoxia species provides insight of the vegetation covering the area more than 100 years ago.
Part of this research received support from the Synthesys Project (http://www.synthesys.info/) financed by the European Community Research Infrastructure Action under the FP6 “Structuring the European Research Area Programme”, enabling us to visit collections in London, Vienna and Copenhagen. We gratefully acknowledge grants by the Deutsche Forschungsgemeinschaft and the Tanzanian Commission for Science and Technology (COSTECH) as well as the Tanzania Wildlife Research Institute (TAWIRI) for permitting research. Many thanks to Susanne Randolf, Sigfrid Ingrisch and Bruno Massa for improving the manuscript.