Research Article |
Corresponding author: Henrique M. Rodrigues ( hmrbio@gmail.com ) Academic editor: Dominic Evangelista
© 2017 Henrique M. Rodrigues, Julio Rivera, Neil Reid, Gavin J. Svenson.
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:
Rodrigues HR, Rivera J, Reid N, Svenson GJ (2017) An elusive Neotropical giant, Hondurantemna chespiritoi gen. n. & sp. n. (Antemninae, Mantidae): a new lineage of mantises exhibiting an ontogenetic change in cryptic strategy. ZooKeys 680: 73-104. https://doi.org/10.3897/zookeys.680.11162
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We present the description of a new genus and new species of praying mantis, Hondurantemna chespiritoi gen. n. & sp. n. This species of cryptic mantis, collected in National parks in Mexico and Honduras, remained unknown despite its considerable body size. Based on a phylogenetic analysis with molecular data and traditional morphological analysis, we place this new genus within Antemninae, a monotypic Mantidae subfamily. We update the subfamily concept for Antemninae and provide a key to the two genera. We describe the external morphology of immatures and adults of the new species as well as the genital complexes of both sexes and the ootheca of Antemna rapax. The observed morphological changes between immature and adult females suggests that the selection for an alternate strategy for crypsis is a response to size increase of the abdomen during development. Immatures exploit a stick/branch habitat based on their morphological appearance while adult females appear as a leaf to disguise the profile of the body.
Se presenta la descripción de un nuevo género y una nueva especie de mantis religiosa, Hondurantemna chespiritoi gen. n. & sp. n. Esta nueva especie de mantis críptica, colectada en ciertos parques nacionales de México y Honduras, había permanecido hasta ahora desconocida para la ciencia a pesar de su gran tamaño corporal. Utilizando un análisis filogenético con datos moleculares y junto con análisis tradicional de morfología, se logró clasificar a este nuevo género dentro de la subfamilia monotípica Antemninae que pertenece a la familia Mantidae. Como resultado se actualiza el concepto taxonómico de Antemninae y se presenta una clave para identificar los dos géneros atribuidos a esta subfamilia. Se describe la morfología externa de los juveniles y adultos de la nueva especie, así como el complejo genital de ambos sexos y la ooteca de Antemna rapax. La diferencia morfológica observada entre juveniles y adultos sugiere que existen fuerzas selectivas divergentes, posiblemente en respuesta al aumento del tamaño del abdomen durante el desarrollo, para así mantener su camuflaje a lo largo de su ciclo de vida. Sobre la base de su apariencia general, los juveniles utilizarían una estrategia críptica asemejando ramas, mientras que las hembras adultas asemejan hojas verdes para ocultar el contorno corporal.
Mantodea , Praying mantis, Dictyoptera , crypsis
Mantodea , mantis religiosa, Dictyoptera , crypsis
The taxonomy of Mantodea has been revised several times during the 20th century, leading to unstable family and subfamily arrangements (
Two enigmatic praying mantis specimens, one male and one female, were discovered in collections from the United States and France. Shared characteristics of the two specimens suggested they were conspecific, but they were incompatible with the descriptions of known Neotropical genera. Additional material collected in Honduras, including two adult females and nymphs of both sexes, confirmed the conspecificity of the specimens and provided the opportunity to study some morphological variation. Initial examination of other Neotropical taxa allied our unknown specimens with Antemna rapax Stål, 1877, the only representative of Antemninae. In both species, mid- and hindlegs present a posteroventral sub-apical lobe on the femora; males have a medial ocellar process; and the shape of the forewing of the females is similar, with an enlarged costal area, which is unusual for Neotropical species. No other Neotropical genus included with the Acanthopoideasensu
Ontogenetic studies on Mantodea are uncommon and most species are described based on adult specimens, while nymphs remain unknown or undescribed, with a few exceptions.
Morphological sexual dimorphism, frequently present in Mantodea species (
Herein, we leverage a molecular based phylogeny paired with traditional comparative morphology to place our unknown taxon among other Neotropical praying mantises. We 1) place our unknown taxon in a newly created genus allied with Antemna within Antemninae; 2) provide a diagnosis for the new genus and an extensive description of the new species, high-resolution images and morphological illustrations; and 3) describe morphological changes occurring through post-embryonic development with comments on the ecological significance and present the distribution for the new species.
We examined twenty specimens of the new taxon, one male genitalia and one ootheca of Antemna rapax. Specimens are accessioned in four collections: the Muséum National d’Histoire Naturelle (
We examined specimens using a Leica M80 stereomicroscope and measured them with a Leica M165C stereomicroscope fitted with an IC80 HD coaxial video camera and the live measurement mode of the Leica Application Suite (LAS). Measurements are given in millimeters and include: body length (measured from the frons to the apex of the abdomen); prozona length (measured from the anterior end of the prothorax to the sulcus above the supracoxal dilation); metazona length (measured from the sulcus above the supracoxal dilation to the posterior end of the prothorax); prothorax width (measured at the level of the supracoxal dilation); forewing length (measured from the point where the forewing articulates with the thorax to the tip); hindwing length (measured from the point where the hindwing articulates with the thorax to the tip); forecoxa length (measured from the articulation with the prothorax to the articulation with the trochanter); forecoxa width (measured at the widest point of the coxa); forefemur length (measured from the articulation with the trochanter to the articulation with the tibia); forefemur width (measured at the widest point of the femur); foretibia length (measured from the articulation with the femur to the articulation with the tarsus); mesofemur length (measured from the articulation with the trochanter to the articulation with the tibia); metafemur length (measured from the articulation with the trochanter to the articulation with the tibia). We calculated ratios useful for species identification (
We took high resolution photos with a Passport Storm© system (Visionary Digital™, 2012), which included a Stackshot z-stepper, a Canon 5D SLR, macro lenses (50mm, 100mm and MP-E 65mm), three Speedlight 580EX II flash units with initial image processing done on Adobe Lightroom 3.6. Z-stepper was controlled using Zerene stacker 1.04, and images stacked with P-Max protocol. Photos were edited using Adobe Photoshop CC to correct for background noise and to add scale bars. We created illustrations with Adobe Illustrator CC based on high-resolution photos of the structures. We constructed plates with Adobe Illustrator CC.
We conducted phylogenetic analyses to test the position of our new taxon using molecular data. The ingroup sample included taxa within Antemninae, Stagmatopterinae, Stagmomantinae, and Vatinae (Table
List of species used in the phylogenetic analyses with their families and subfamilies given.
Species | Family | Subfamily | MN Code | GenBank accession number – COI | GenBank accession number – H2A | GenBank accession number – H3 | GenBank accession number – ND4 |
---|---|---|---|---|---|---|---|
Mantoida sp. | Mantoididae | - | MN180 | FJ802822.1 | - | FJ806771.1 | FJ802586.1 |
Chaeteessa sp. | Chaeteessidae | - | MN482 | KR360623.1 | - | KR360691.1 | - |
Acanthops falcataria | Acanthopidae | Acanthopinae | MN112 | EF383861.1 | - | EF384117.1 | FJ802526.1 |
Macromantis nicaraguae | Mantidae | Photininae | MN144 | EF383873.1 | - | EF384129.1 | FJ802554.1 |
Cardioptera squalodon | Mantidae | Photininae | MN178 | EF383889.1 | - | EF384145.1 | FJ802584.1 |
Epaphrodita musarum | Acanthopidae* | Epaphroditinae | MN435 | KY783773 | - | KY783805 | KY783826 |
Hymenopus coronatus | Hymenopodidae | Hymenopodinae | MN010 | EF383800.1 | KR360626.1 | AY491334.1 | FJ802425.1 |
Choeradodis rhombicollis | Mantidae | Choeradodinae | MN016 | EF383805.1 | - | AY491340.1 | FJ802431.1 |
Rhombodera basalis | Mantidae | Mantinae | MN344 | FJ802913.1 | - | FJ806867.1 | FJ802738.1 |
Vates pectinicornis | Mantidae | Vatinae | MN014 | EF383803.1 | AY491338.1 | FJ802429.1 | |
Vates sp. | Mantidae | Vatinae | MN760 | - | - | KY783825 | - |
Zoolea orba | Mantidae | Vatinae | MN351 | KT732082.1 | - | KT732101.1 | - |
Oxyopsis 1 | Mantidae | Stagmatopterinae | MN294 | FJ802868.1 | - | FJ806822.1 | FJ802689.1 |
Oxyopsis 2 | Mantidae | Stagmatopterinae | MN734 | KY783777 | - | KY783808 | KY783828 |
Oxyopsis 3 | Mantidae | Stagmatopterinae | MN739 | KY783780 | - | KY783811 | KY783829 |
Oxyopsis 4 | Mantidae | Stagmatopterinae | MN743 | KY783784 | - | KY783815 | KY783832 |
Oxyopsis 5 | Mantidae | Stagmatopterinae | MN749 | - | - | - | KY783841 |
Parastagmatoptera sottilei 1 | Mantidae | Stagmatopterinae | MN740 | KY783781 | - | KY783812 | - |
Parastagmatoptera sottilei 2 | Mantidae | Stagmatopterinae | MN742 | KY783783 | KY783797 | KY783814 | KY783831 |
Parastagmatoptera flavoguttata 1 | Mantidae | Stagmatopterinae | MN741 | KY783782 | KY783796 | KY783813 | KY783830 |
Parastagmatoptera flavoguttata 2 | Mantidae | Stagmatopterinae | MN751 | KY783788 | KY783801 | KY783819 | KY783836 |
Parastagmatoptera vitreola 1 | Mantidae | Stagmatopterinae | MN731 | KY783775 | KY783794 | KY783806 | - |
Parastagmatoptera vitreola 2 | Mantidae | Stagmatopterinae | MN735 | KY783778 | - | KY783809 | - |
Stagmatoptera hyaloptera | Mantidae | Stagmatopterinae | MN733 | KY783776 | - | KY783807 | KY783827 |
Stagmatoptera septentrionalis | Mantidae | Stagmatopterinae | MN029 | FJ802763.1 | - | AY491353.1 | FJ802444.1 |
Stagmatoptera supplicaria 1 | Mantidae | Stagmatopterinae | MN117 | EF383863.1 | - | EF384119.1 | FJ802531.1 |
Stagmatoptera supplicaria 2 | Mantidae | Stagmatopterinae | MN736 | KY783779 | KY783795 | KY783810 | - |
Stagmatoptera supplicaria 3 | Mantidae | Stagmatopterinae | MN748 | KY783787 | KY783800 | KY783818 | KY783835 |
Stagmomantis 1 | Mantidae | Stagmomantinae | MN747 | - | KY783804 | KY783824 | - |
Stagmomantis 2 | Mantidae | Stagmomantinae | MN744 | KY783785 | KY783798 | KY783816 | KY783833 |
Stagmomantis 3 | Mantidae | Stagmomantinae | MN745 | KY783786 | KY783799 | KY783817 | KY783834 |
Stagmomantis 4 | Mantidae | Stagmomantinae | MN730 | KY783774 | KY783793 | - | - |
Stagmomantis 5 | Mantidae | Stagmomantinae | MN753 | KY783789 | KY783802 | KY783820 | KY783837 |
Antemna rapax | Mantidae | Antemninae | MN147 | EF383875.1 | - | EF384132.1 | FJ802557.1 |
Hondurantemna chespiritoi gen. n. & sp. n. 1 | Mantidae | Antemninae | MN757 | KY783790 | - | KY783821 | KY783838 |
Hondurantemna chespiritoi gen. n. & sp. n. 2 | Mantidae | Antemninae | MN758 | KY783791 | - | KY783822 | KY783839 |
Hondurantemna chespiritoi gen. n. & sp. n. 3 | Mantidae | Antemninae | MN759 | KY783792 | KY783803 | KY783823 | KY783840 |
The results of BI and ML analyses were largely congruent and generally well supported (Fig.
Bayesian Inference (BI) tree with bootstrap values from the Maximum-likelihood and posterior probabilities values higher than 70 shown. Star represent clades with maximum support in both analyses, dash represents support lower than 70 in one of the analyses and asterisk represents a clade recovered only in the BI analysis. Hondurantemna chespiritoi n.gen. n. sp. is highlighted in red.
The phylogenetic analyses recovered the new taxon as closely related to Antemna rapax (Fig.
Antemna Stål, 1877.
Males have a medial ocellar process that originates posteriorly to the ocelli but anterior to the postfrontal sulcus. The dorsal margin of the forefemora at least partially produced, forming a lamellar projection. Forefemora with four discoidal spines. Meso- and metathoracic legs bearing a posteroventral sub-apical lobe originating from an expansion of the keel running along the margin of the femur. Abdomen of the females swollen, almost as wide as long.
1 | Five posteroventral forefemoral spines. Dorsal expansion of forefemur extending to femoral apex (Fig. |
Hondurantemna gen. n. |
– | Four posteroventral forefemoral spines. Dorsal expansion of forefemur ending abruptly before femoral apex (Fig. |
Antemna |
Hondurantemna chespiritoi sp. n. by monotypy
Rounded compound eyes, nymphs and adult males have a medial ocellar process, subadult and adult females without the process. Forelegs with five posteroventral spines and four discoidal spines. Mid- and hindlegs with a single small lobe near the apex of the femur. Male’s forewings are hyaline with green crossveins, forewings of females with a spot close to the center of the discoidal area.
The generic epithet combines the words Honduras, country were the majority of specimens we studied were collected, and Antemna, in reference to the morphological similarities of both Antemninae genera.
Holotype. 1 ♂ Mexico, Chiapas, Municipio de La Trinitaria, Lagunas de Monte Bello National Park, bellow Dos Lagos on rd. to Santa Elena, 1219m, 14.x.1981, D.E. & P.M. Breedlove (
Male: Medium sized. General coloration light brown with dark brown spots (Fig.
Head (Fig.
Thorax (Fig.
Prothoracic legs: Forecoxae (Fig.
Wings: Forewings reaching the apex of the abdomen, costal area with a sinuous margin, reticulate veins, opaque green; discoidal area mostly hyaline, with an anterior area smoky green and all the veins and crossveins opaque green. Hindwings shorter than the forewings, not reaching the apex of the abdomen; hyaline with brown-red veins and crossveins (Fig.
Meso- and metathoracic legs: Coxa with two strong keels, one anterodorsal and the other posterodorsal. Trochanter with a notch on apical ventral margin, bearing a spine on the articulation with the femora (Fig.
Abdomen: With black spots on the sides of tergites II–V and VII–IX, and a black stripe on tergites VI–VII. Slightly dorsoventrally compressed, with apical lobes on sternites IV–VI, more developed on segments V and VI, the lobes flat against the body (Fig.
Genitalia: Left phallomere – Sclerite L4B roughly rectangular, longer than wide, left margin projected anteriorly; apofisi falloide (afa) with the anterior part bearing small spines and extremely elongate, projecting dorso-posteriorly, posterior part also elongated, curved towards the left, tapering distally and bearing small spines at the apex; lobo membranoso (loa) elongate, without projections, glabrous; processo apical (paa) elongate, slightly flattened, curved 30° to the left, apex curved anteriorly; sclerite L4A roughly circular, without projections other than the processo distal (pda); pda elongate, curved to the right, uniformly broad, tapering at the distal third, ending in a strongly sclerotized spine (Fig.
Female: Medium to large sized. General coloration light green without any spots (Fig.
Head (Fig.
Thorax (Fig.
Prothoracic legs: Forecoxae (Fig.
Wings: Forewings opaque green, costal area almost as wide as the discoidal area, the apex constricted, making the tegmina follow the abdomen contour, with 7–10 branches of the sub-costa vein, crossveins with a reticulate appearance; spot in the center of the discoidal area, composed of an anterior small crescent-shaped brown portion and a posterior round white portion; anal area smoky green. Hindwings as long as the tegmina, reaching the apex of the abdomen, apex of the discoidal area well developed, opaque green, the remainder of the hindwing hyaline (Fig.
Meso- and metathoracic legs: Femora with three keels, one runs along the posteroventral margin and originates one single subapical lobe (Fig.
Abdomen: Without black spots. Slightly dorsoventrally compressed, without apical lobes on sternites. Cerci elongated, cercomeres cylindrical, except the last one, which is conical.
Genitalia: Gonoplacs (gl) simple, bearing setae along the dorsal margin and the base, apex bearing a ventral projection. Gonapophysis IX (gp) mostly membranous, with two sclerotized ribbons, one elongate and tapering towards the apex of gp, the other shorter and occupying a medial projection of gp, this projection being rounded; gl and gp of almost the same length. Gonapophysis VIII (ga) bearing setae on the base, on the ventral surface and on the apex, a dorsal groove spanning the two basal thirds, ending in a pointed projection, the apex enlarged ventrally. Basivalvula (bv) with the lateral surface smooth, bearing a central depression, the medial surface rugose, with two projections, one central directed medially, the other more posterior, directed to the base of the ga. Interbasivalvula (ib) well sclerotized, rugose and shaped like a sectioned rhombus. Laterosternal shelves (ls) weakly sclerotized, roughly rhomboid, with short rounded posterior projections (Fig.
Nymphs (unless specified, description applies to male and female nymphs of all instars): General coloration varies from entirely light brown to light brown mottled with dark brown.
Head: Vertex higher than imaginary line connecting dorsal margin of the compound eyes, without lateral keels and a central depression but with the medial ocellar process. In female nymphs, the process becomes increasingly smaller during development, being absent on the instar before the final molt (Fig.
Dorsolateral view of the head of female nymphs of Hondurantemna chespiritoi gen. n. sp. n. Black arrows point the medial ocellar process that degenerates during ontogenetic development, grey arrow points the region where the process stood. A early instar nymph B mid instar nymph C late instar nymph. Scale bars = 1mm.
Thorax: The first ventral cervical sclerite may be split in two. Metathoracic hearing organ underdeveloped.
Prothoracic legs: Forecoxae light brown except for the lower apical lobe, which is dark brown. Dorsal margin bearing five to six large spines. Forefemora varying, light brown with three dark brown spots on the dorsal area of the anterior surface to dark brown with light brown spots; F=4DS/15AvS/5PvS; males without crenulation between posteroventral spines, females with crenulation; discoidal spines black on the anterior surface, the first spine presenting a dark spot on its base; the first anteroventral spine black, a dark spot on the anterior surface above the first two to four spines; femoral brush extending from the 12th anteroventral spine to the last, a dark spot may be present under the femoral brush. T=13–14AvS/12–14PvS. Foretarsi with an anterior-basal dark brown spot on the first tarsomere and dark brown anterior-apical spots on all tarsomeres.
Meso- and metathoracic legs: Femora with three keels, one runs along the posteroventral margin and originates one single subapical lobe, the second runs along the dorsoposterior margin and the third, less marked, runs along the dorsoanterior margin, the keels on the youngest female nymphs are expanded into shelves (Fig.
Abdomen: Without black spots or bands on the tergites. Not dorsoventrally compressed, on males apical lobes present on sternites IV–VI, lobe on segment V more developed, the lobes pointing down instead of being held against the body (Fig.
The Lagunas de Montebello National Park, Mexico, from which the holotype was collected, is ca. 6,500 hectares located on the high plains of Chiapas, with an altitude between 1,200 and 1,800 meters above sea level (UNESCO: Lagunas de Montebello http://www.unesco.org/mabdb/br/brdir/directory/biores.asp?mode=gen&code=MEX+37). The predominant vegetation is Central American pine-oak forest over a highly rugged terrain. The Sierra del Merendón, from which the allotype and paratypes were collected, is a mountain range extending from northwest Honduras into southeast Guatemala bordered by the Lempa and Motagua River valleys. The size of the region and its typographical complexity supports four principal forest ecotypes; 1) tropical lowland dry forest, 2) tropical moist forest, 3) montane cloud forest (above 1,200m) and 4) the Bosque Enano or ‘dwarf forest’ occurring at the highest elevations (above 2,000m). The Parque Nacional Cusuco, surrounding Montaña San Ildefonso (also known as Cerro Jilinco), from which the paratypes were collected, is located within the Sierra del Merendón, and is a protected area of 23,440 hectares (
A name in the genitive case, this species is named after “Chespirito”, the screen name of famous late Mexican TV comedian Roberto Gomez Bolaños. Chespirito created and portrayed several characters cherished across Latin America, including “El Chavo del Ocho” and “El Chapulín Colorado”, the latter a sort of superhero whose outfit was inspired by grasshoppers or “chapulines”.
Genitalia: Left phallomere – Sclerite L4B roughly oval, much longer than wide, left margin projected anteriorly; afa with the anterior part smooth and short, posterior part elongated, curved towards the right, clubbed and bearing spines at the apex; loa elongate, without projections, glabrous; paa elongate, slightly flattened, curved 30° to the left, apex curved anteriorly; sclerite L4A elongate, without projections other than the pda; pda elongate, curved to the right, uniformly broad, tapering at the apex, ending in a sclerotized spine (Fig.
Egg case: somewhat barrel-like, laterally compressed, posteroventral end encircling substrate to which it is attached, ventral surface away from, and forming an angle with the substrate. External wall russet brown in color and rough in appearance. External coating in the form of a whitish layer of frothy material. The coating extends over the emergence area and adjacent dorsal surface of egg case. Exhibiting 40–44 egg chambers whose boundaries are clearly visible as sigmoidal markings along the dorsolateral surface the egg case (external coating might conceal this feature in some specimens), and with as many emergence openings as egg cambers, aligned to form two parallel rows along the dorsal margin. Some emergence openings can be seen on a long, relatively straight, and upwardly projected, distal process (Fig.
Male genitalia: Costa Rica, Puntarenas, P. N. Piedras Blancas, Esquinas Lodge (NW – Golfito), 15.v.1996, D. Brzoska, GSMC005332, GD0097 (
Our molecular phylogenetic analyses confirmed our morphology based hypothesis of a unique taxon, Hondurantemna chespiritoi, being placed within the subfamily Antemninae. Our analysis also recovered Antemninae and Stagmomantinae as closely related, with the latter recovered as paraphyletic. This result suggests that current classification does not represent natural lineages, a pattern that repeats across various major lineages within Mantodea (
There are two non-exclusive explanations for differing morphologies in immatures and adults. Adaptive responses to changes in habitat and resource (i.e. prey) use during postembryonic development, e.g. Acontista (
Nymphs of both sexes and adult males of Hondurantemna chespiritoi exhibit cryptic features to resemble small twigs. These include brown coloration, presence of a medial ocellar process (Figs
The ontogenetic changes of Hondurantemna chespiritoi brings to question the identity of nymphs described by
Hondurantemna chespiritoi is exemplary of large, undiscovered insect diversity yet to be documented. Although H. chespiritoi has fascinating post-embryonic changes that indicate distinct selective pressures acting on both sexes, the pattern may be more common than we realize, considering the lack of information on nymphal biology. This study shows the importance of describing all life stages and both sexes whenever possible, to prevent misidentification of conspecific specimens and bring to light the natural history of the species.
We thank Mr Roger Roy and Dr Philippe Grandcolas from the Muséum National d’Histoire Naturelle and Dr Brian Fisher and Dr Norm Penny from the California Academy of Sciences for the loan of the material. Dr. Jason Weintraub for allowing JR to access the Antemna rapax ootheca and Rick Wherley for imaging it. Operation Wallacea Ltd organized the field expedition to Honduras. Permits for collections in El Parque Nacional Cusuco and export permits were provided by the Instituto Nacional de Conservación y Desarrollo Forestal facilitated by Roberto Downing. We thank Dr Merlijn Jocque, Royal Belgian Institute of Natural Sciences, Aquatic & Terrestrial Ecology (ATECO), Belgium, for support in acquiring immature and adult specimens used to describe the post-embryonic development and to carry out the molecular analyses. We also thank Dr Nicole Gunter and Marlene Harmon for their help with the DNA extraction and PCR, and to Andrew Snyder and Ethan Staats for kindly allowing us to reproduce their photograph of living specimens taken at Cusuco National Park, Honduras. HMR thanks CNPq for the funding through the Brazilian program “Ciências sem Fronteiras”, process number 2007002014-6. This project was supported, in part, by the National Science Foundation under the grant DEB-1216309 to GJS. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation or the Cleveland Museum of Natural History. No conflict of interests exist.