Review of the tribe Amorphopini ( Orthoptera : Tetrigidae : Metrodorinae ) : Pygmy moss-lichen tetrigids from the Amazon rainforest

The tribe Amorphopini Günther, 1939 is reviewed. It consists of two genera: Amorphopus Seville, 1838 and Eomorphopus Hankock, 1907 with three Neotropical species: Amorphopus notabilis Serville, 1838, Eomorphopus antennatus (Bolívar, 1887), and Eomorphopus granulatus Hancock, 1907. Two species are transferred from Amorphopus to the genera Metrodora Bolívar, 1887 and Crimisus Bolívar, 1887, and two new combinations are proposed: Metrodora gibbosula (Walker, 1871), comb. nov. and Crimisus humeralis (Walker, 1871), comb. nov. New synonyms are proposed: Amorphopus notabilis Serville, 1838 = Amorphopus griseus Bolívar, 1887, syn. nov.; Metrodora gibbosula (Walker, 1871) = Platytettix reticulatus Hancock, 1906, syn. nov.; and Crimisus humeralis (Walker, 1871) = Allotettix bolivianus Brunner, 1913, syn. nov. Neotypes of Amorphopus notabilis and Eomorphopus antennatus as well as the lectotype of E. granulatus are designated. The description of Amorphopus testudo Saussure, 1861 is based on an immature specimen and we considered it as nomen dubius and the type depository of Eomorphopus purpurascens is unknown so we considered it, too, as nomen dubius. The tribe Amorphopini and all included taxa were redescribed and illustrated. A key to the genera and species is provided. Data on distribution, behavior, camouflage with lichens, polychromy, as well as ecological aspects of the species are reported.

In the present study, we review the tribe Amorphopini and its species, study the status of the genera and species and their ecological associations and behaviors, and provide an updated identification key. Additionally, we also present updated distribution maps for all known Amorphopini species. This paper is part of the cooperative study of Neotropical Tetrigidae led by Daniela Santos Martins Silva and Oscar J. Cadena-Castañeda.

Material and methods
Specimen preparation.-The studied specimens were deposited in the following institutions: Colección de Artrópodos y otros Invertebrados de la Universidad Distrital Francisco José de Caldas, Bogotá, Colombia (CAUD), Academy of Natural Sciences, Philadelphia, Pennsylvania, USA (ANSP), Naturhistoriska Riksmuseet, Sweden, Stockholm ( Specimen photos were taken with a Leica DFC295 attached to a stereomicroscope M205. The photographs of ANSP types were taken in a photo lightbox with a Canon EOS T3i digital camera equipped with a EF 100mm f/2.8 L macro lens. Photographs of living specimens were taken using a Nikon D7100 digital camera, with a 60 mm 2: 8 lens. The illustrations were made using Adobe Illustrator CS6 and Adobe Photoshop CS6. Terminology and measurements follow Devriese (1996) and Tumbrinck (2014). The measures that most discriminated Amorphopini species were the following: Body length from the tip of the fastigium projection to the posterior tip of the pronotum (CFP); pronotum length (PL); pronotum lateral lobes maximal width (PLB); fore femur length (FF); fore tibia length (FL); middle femur length (MFL); middle tibia length (MTL); hind femur length (HL); hind femur maximal width (HW); and hind tibia length (HL).
Maps and distribution data.-Maps were drawn with Simplemappr (Shorthouse 2010). Data included in the maps were collected from the studied specimens and from visits to the different collections previously mentioned, and maps are intended to correct erroneous or doubtful records in the literature. Distribution data of photographed specimens were also recorded and identifications could be reliably made from photographs.
Comments.-Amorphopini was erected as a tribe by Cadena-Castañeda and Cardona-Granda (2015) (Amédégnato and Devriese 2008). In addition to the previously mentioned characters, Amorphopini differs from the tribes established to date in Metrodorinae by lacking a prolonged vertex (which is common in Clinophaestini, Cleotrastini sensu Storozhenko 2016, and Miriatrini sensu Cadena-Castañeda and Cardona-Granda 2015), and by having filiform antennae. Clinophaestini and some Ophiotettigini, have widened antennal segments.
Platythorus is monotypic with only one female type, Platythorus camurus Morse, 1900, and occurs in Nicaragua and Costa Rica (Bruner et al. 1900(Bruner et al. -1909. This genus is easily distinguished from other Amorphopini by the lack of tegmina and wings and the middle femur that is not strongly expanded. This genus has morphology rather different from Amorphopini and is placed out of Amorphopini, as a Metrodorinae genus without tribal placement. Distribution.-The Amorphopini species, as well as other species in South America, exhibit a very peculiar geographical distribution (see Silva et al. 2017, Cadena-Castañeda et al. 2019). There is a large area in the north region of South America (mainly Amazon Forest) where these genera are not known to occur (Figs 12-14). In addition, there is only one record for an Eomorphopus species that probably refers to the Atlantic Forest of Bahia State (Brazil), but Günther (1939) did not provide an exact location. Eomorphopus probably does occur in those areas, but its species haven't been sampled or identified due to limited zoological expeditions and taxonomic effort focused on tiny litter insects.
Description.-Head. Not protruding from the body; face very distinctly oblique (Fig. 1B, C); antennae filiform with 15 segments, inserted below the eyes; vertex anteriorly truncated and equal in width to one of the eyes; frontal costa with a wide scutellum between the lower part of the eyes, slightly compressed-elevated, sinuate below; eyes globose, not prominent; posterior ocelli placed between the inferior part of the eyes (Fig. 1B). Thorax. Meso-pleura expanding to the sides and covering the coxae in dorsal view. Pronotum. Macropronotal and strongly depressed dorso-ventrally. Lateral view. Median carina slightly undulated on prozona and extended to pronotal disc apex, prozonal carina and humero-apical carina visible, reaching the sulci; tegminal and ventral sinus present; length of the infrascapular area mid-sized covering to first abdominal tergite; humeral angles obtuse (Fig. 1A). Dorsal view. anterior and posterior margins truncated, also the first one undulated; prozonal carina visible; lateral lobes of pronotum ampliate and projected sideways, with the margins undulated and with a blunt spine (Fig. 1D).
Wings. Tegmina and hind wings developed; tegmina ovoid, hind wings as long as the pronotum apex, opaque with the apical veins between the C and Sc yellowish. Legs. Fore and middle femora rectangular, longer than wide and with margins undulated (Fig. 1E, F), fore and middle tibiae narrow and short. Hind femur with the pre-genicular tooth slightly developed, small foliose plate present between the ventro and dorso-external carinae (Fig. 1D), hind tibia narrow and with few spines on the meso-distal portion. Abdomen. Narrow and slim, subgenital plate with the distal edge wavy with a rounded prolongation in the middle (Fig. 1G); ovipositor with narrow valves and with denticulations of moderate size (Fig. 1H).
Male. Similar to the female, except for the post-abdomen characters ( Fig. 2A-F). Subgenital plate moderately prolonged, with the dorsal edge straight and the apex rounded ( Fig. 2G), conical and robust cerci (Fig. 2H).
Coloration. Predominantly white with scattered gray spots. Face and ventral surface of the body black with scattered whitish bands; pronotal disc from the level of the third pair of coxae with gray stripes, which extend and alternate towards the posterior area of the pronotum; fore femur white, fore tibia black with a white ring in the mesal region; femur and mid tibia, as well as the basal half of the hind femur, light pink, distal half of the hind femur white with gray stripes in similar appearance to the pronotal disc (Fig. 3).
Variations.-The margin undulations of the fore and mid femora may be more conspicuous in some specimens and the lateral lobes with the posterior angles may have sinuato-dentate or serrato-crenate margins. Comments.-Currently A. notabilis has two synonyms: Tetrix cnemidotus Burmeister, 1838 and Amorphopus caiman Saussure, 1861, both synonymized by Günther (1939). A. testudo Saussure, 1861 is an immature specimen (Günther 1939) and currently the type depository is unknown (Hollier 2013); this specimen could possibly be an immature of A. notabilis, but we kept it as nomen dubius. Bruner (1910) separated A. griseus Bolívar, 1887, A. notabilis Serville, 1838, A. cnemidotus (Burmeister, 1838), and A. caiman by the size of the females and the coloration of the specimens. The size and coloration in this species may vary, depending on the area, availability of resources, and camouflage strategies (Cadena-Castañeda 2011a, b, 2013a, b, c). Moreover, colors of specimens preserved in museums may vary by virtue of the preservation method used, such as storage in alcohol, which usually makes the specimens lose its color (Cadena-Castañeda 2012, Cadena-Castañeda and Páez 2013). By studying the type specimens, the synonymy of these species is confirmed, and we propose that Amorphopus griseus Bolívar, 1887 syn. nov., be considered as a new synonym under A. notabilis.

Measurements (in mm
To the two remaining species of the genus, the following nomenclatural acts are proposed: 1. A. gibbosulus Walker, 1871 is transferred to Metrodora Bolívar, 1887, and it is synonymized with Metrodora reticulata (Hancock, 1906) syn. nov. (originally described as Platytettix reticulatus Hancock, 1906) under Metrodora gibbosulus (Walker, 1871) comb. nov. This synonym is proposed by comparison of the type specimens of both species. It is observed that there is no variation in the shape of the fastigium of   the vertex, since both species have a broad frontal costa, similar to the species of the subfamily Cladonotinae. The pronotum has a curvature in the prozone that rises significantly; the apex of the pronotum is curved slightly upwards and the lateral lobes of the pronotum project towards the sides, with the inferior margin triangular in shape. Since these diagnostic characters are present in specimens of both species, they cannot be maintained as separate specific entities, much less belonging to different genera.
2. Similarly, A. humeralis (Walker, 1871) (=Tettix humeralis) is transferred to Crimisus Bolívar, 1887, and it is synonymized with Crimisus bolivianus (Bruner, 1913), syn. nov. (originally described as Allotettix bolivianus Bruner, 1913) under Crimisus humeralis (Walker, 1871), comb. nov. The type specimens of both species are females, but, unfortunately, the legs in the holotype of A. humeralis are missing, so the legs were not compared. Nevertheless, both species share the same characteristics: narrow frontal costa, lower margins of the pronotal lobes rounded, without projecting to the sides as in the previous case, subgenital plate triangular, with a small prolongation at the apex. The aforementioned characters are observed in the type specimens of both species, indicating that they belong to a single species. Since they do not have expanded anterior and middle femora, it is ruled out that they belong to the Amorphopini tribe, fitting better in the genus Crimisus.
The two species described by Walker (1871), A. gibbosulus and A. humeralis, were not studied again and were not included in the Orthoptera Species File until Dr. J. Tumbrinck photographed the specimens and updated the information. If historical authors like Hancock and Günther had access to those specimens, for example, certainly they would have considered them to be synonyms. The nomenclatural acts were carried out by comparing the type specimens and their photographs; A. gibbosulus and A. humeralis do not meet the diagnostic characteristics to be included in Amorphopus, but they are similar to Metrodora reticulata syn. nov. (now Metrodora gibbosulus) and Crimisus bolivianus syn. nov. (now Crimisus humeralis), respectively, in diagnostic structures such as pronotum structure, face, and terminalia shape.
Finally, the genus Amorphopus is kept monotypic and its known distribution is extended through the Amazonian slope, similarly to Pterochroza ocellata (Linnaeus, 1758), a species that was once considered several different species, but is now known to be a single, very variable species (Xiberras and Ducaud 2004).
A neotype specimen is designated as the carrier-name of the species and is supported by the following reasons (ICZN 1999 Art. 75): 1. The location of the only type specimen is unknown. It was deposited in NHRS, but Josef Tumbrinck visited that collection and did not find the type specimen (pers. comm.) "Some of the types of Serville are lost. Some of them are in Paris. But Josip Skejo did not find Amorphopus notabilis in Paris. So -today -the type is lost". The holotype female specimen has as type locality "Brazil, Para". This specimen could not be traced from its original description (Arts. 75.3.1., 75.3.4.), but the author provided figures, and when compared with the neotype specimen here designated, it agrees with the drawings by Serville (1838). 2. Not having specimens from the type locality, a female from a nearby and available locality of similar geological characteristics was designated (Arts. 75.3.5, 75.3.6; recommendation 75A ICZN). 3. A detailed description is written of the neotype that is in agreement with the general idea of the identity of this species, differentiating itself from other taxa, ensuring the recognition of the designated specimen, and conveying a consensus in identifications and wide distribution that characterizes the species, ensuring that most identifications from the past are correct (Arts. 75.3.2, 75.3.3, 75.3.5; recommendation 75B). 4. The neotype is deposited in CAUD, a collection of a recognized scientific institution, which maintains adequate facilities to preserve the types and makes them accessible for study (Art. 75.3.7).
Journal of orthoptera research 2020, 29 (1) Behavioral notes.-The Brazilian specimens were collected only in non-flooded ombrophilous forests (Terra Firme). In this environment they are usually found on the trunk and branches of fallen trees, where, due to their coloration and flattened body, they are easily confused with the tree's bark. Once physically stimulated, the specimens exhibited thanatosis behavior, where the individual remained immobile, leaving its femurs parallel to the body, with the lobes of the femora that mimic foliage lying alongside the body and the tibia folded against the femora. Thus, the body of the insect is very similar to a small fragment of bark, and it remains in this position for several minutes even on physical stimulation. Only after several minutes did the observed specimens leave the thanatosis behavior and move (D. Mello Mendes pers. obs.).
Comments.-For a long time, Eomorphopus species were described as Amorphopus, except for E. purpurascens, which was originally described as Acrydium purpurascens by Olivier (1791) and is still almost unknown, without photos and with scant morphological information. Additionally, some of the available morphological information on E. purpurascens is non-traditional, such as the description of the coloration used by Oliver (1791). Characteristics of this kind can be lost over time (e.g., wings with purplish coloration). Furthermore, the type species was not defined in the original description and the depository is unknown. The distribution is known only for Trinidad Island (Olivier 1791). For that reason, we propose as nomen dubius this species, and Eomorphopus only contains two valid species: E. granulosus and E. antennatus.
Behavioral notes.-The Brazilian specimens were collected in lowland floodplains in areas of the Solimões River and non-flooding ombrophilous forests (Terra Firme). They are commonly found in litter on the ground and occasionally on trunks of fallen trees. They are usually found in the same environment with other pygmy grasshoppers, such as Scaria (Cadena-Castañeda et al. 2019 Redescription (Female lectotype, Fig. 4).-Body surface granulated. Head. Lateral view (Fig. 4A, B): protuberant and slightly conical eyes with a flattened base; vertex and fastigium visible between eyes; antennal groove situated between lower margin of compound eyes; frontal costa elevated. Frontal view (Fig. 4D). Fastigium of vertex slightly conic; frontal costa bifurcation placed between compound eyes with narrow scutellum; fascial carinae between both superior ocelli; median ocelli placed between fascial carinae and frontal carina, but not touching on the base by frontal carina; antennal groove situated between lower margin of compound eyes and medial ocelli. Dorsal view (Fig. 4C). Vertex with distance between eyes as long as horizontal diameter of eyes; medial carina conspicuous and continuing towards frontal costa; area of fastigium to occiput granulated; occipital area visible and anterior margin of pronotum distant from the eyes. Pronotum. Macropronotal and flattened dorso-ventrally. Lateral view (Fig. 4A, B). Anterior margin of pronotum truncated and slightly elevated; median carina slightly undulated, prozonal carina and humero-apical carina visible and short, not reaching the sulci; extralateral carina inconspicuous; ventral sinus present; lateral lobe with anterior margin truncated and without spine; tegminal sinus present; length of infrascapular area shorter than length of fore tibiae; two deep sulci between prozona and humero-apical carina; paranota granulated and triangularly shaped; humero-apical carina continuous to external lateral carina and both parallel to median carina. Frontal view (Fig. 4D). Lateral lobes of pronotum projected and directed sideways. Dorsal view (Fig. 4C). Dorsum granulated; prozonal carina visible and short, not reaching the sulci; median carina continuous; humero-apical carina conspicuous; anterior and posterior margin of pronotum truncated; lateral lobe directed sideways. Sternomentum. The sternomentum could not be checked due to it being glued on card. Wings. (Fig. 4A,  B). Tegmina and hindwings visible; tegmina oval, sublanceolated shape; hindwings dark brown and surpassing pronotum apex. Legs. Fore legs (Fig. 4A, B, D). Fore femur flattened laterally, dorsal and ventral margins of femur carinated with three undulations in the dorsal margin and one in ventral margin; tibia as long as femur.
Male (paralectotype, Fig. 5).-Similar to female, except: Head. Frontal view (Fig. 5D). Fastigium straight. Pronotum. Lateral view (Fig.  5A, B). Humero-apical carina not continuous to external lateral carina. Measurements (in Hancock 1907). Total length of male body: 15 mm; pronotum: 13 mm; hind femur: 6 mm.  ANSP. Both specimens of the museum have labels, with the female labeled as "Type" and the male labeled as "Allotype"/"Paratype". As the author did not designate the holotype in the original description, we designated the female as the lectotype and, consequently, the male specimen became the paralectotype. We believe that this redescription will facilitate species recognition in the future. In his description, Hancock (1907) indicated that the body was subtly granulated and cinereous or fuscus-cinereous (ash-colored; gray tinged with blackish), see Smith (1906). Actually, this type has overall brownish-yellow and brown color. Description.-Female. This species is very similar to E. granulatus, but E. antennatus is larger. Furthermore, it is differentiated by the following characters: Body surface more granulated than E. granulatus (Fig. 8A). Eyes globose and prominent, fastigium visible between the eyes, median carina slightly developed and continuing towards frontal costa; area of fastigium to occiput abundantly granulated (Fig. 8B). Pronotum with rounded sculpturing on prozona, median carinae undulate at level of humeral sinus, length of infrascapular area as long as fore femur (Fig. 8C); prolongation of the pronotum constricting and resuming its thickness rapidly, close to the distal third, apex of the lateral lobe of the side projection triangular shaped and moderately sharp; anterior and posterior margin of pronotum truncated; lateral lobes directed sideways (Fig. 8D).   Fore femur flattened laterally, dorsal and ventral margins carinated with two or three undulations in the dorsal margin and one or two in ventral margin (Fig. 8E); middle femur shield like in shape, flattened laterally and strongly foliaceous (mid-femur notably wider than E. granulatus), dorsal and ventral margin slightly undulated; ventral margin expanded, with rounded teeth in the apex (Fig. 8F). Subgenital plate triangular shaped, slightly longer than wide, with a small mid triangular tooth (Fig. 8G).

Eomorphopus antennatus Bolívar, 1887
Male. Similar to the female, distinguished by the ambisexual characters ( Fig. 9A-F): subgenital plate prolonged, in ventral view triangular shaped and with rounded apex (Fig. 9G), cerci cylindrical, slightly reducing in thickness from the base to the apex (Fig. 9H).
Variations.-The main variations observed in this species are related to the coloration, that will be detailed later. Morphologically, the undulations of the middle and anterior femur may be more conspicuous in some individuals than others, although it was observed that they are more conspicuous in males than in females. Moreover, the undulations of the dorsal margin of the anterior femur can vary from two, three, or four, distorting the use of this character to separate the two species of Eomorphopus. (Bruner (1910) suggested that E. granulatus had three undulations and E. antennatus had two). Comments.-Eomorphopus antennatus was described by Bolívar (1887) as Amorphospus, and in 1907, Hancock reallocated this species to the new genus Eomorphopus. E. antennatus is very similar to E. granulatus but is distinguished by the biundulated fore femur dorsal margin vs. the triundulated fore femur dorsal margin in E. granulatus (Bruner 1910). E. antennatus has several records: Peru, Guyana, Venezuela, Ecuador, Suriname, Brazil, and Trinidad Island. Currently, the depository of the primary type is unknown (Cigliano et al. 2019) and there is a female from Alto Amazonas in Bolívar's Tetrigoidea collection, housed at the National Museum of Natural History, Madrid, Spain (MNCN) (Paris 1993(Paris -1994.

Measurements (in mm
A neotype specimen is designated as the carrier-name of the species and is supported by the following reasons (ICZN 1999) Art. 75) 1. The status of the only type specimen is lost. It was deposited in MNCN, but this specimen could not be traced from its original description (Arts. 75.3.1., 75.3.4.). 2. The type female specimen has as type locality Peru, Upper Amazonas, but not having specimens from the same locality, a female from a nearby and available locality of similar geological characteristics was designated (Arts. 75.3.5, 75.3.6; recommendation 75A ICZN). 3. A detailed description is written for the neotype that is in agreement with the general idea of the identity of this species, differentiating it from other taxa, ensuring the recognition of the designated specimen, and conveying a consensus in identifications and wide distribution that characterizes the species, ensuring that most identifications from the past are correct (Arts. 75.3.2, 75.3.3, 75.3.5; recommendation 75B). 4. The neotype is deposited in CAUD, a collection of a recognized scientific institution, which maintains adequate facilities to preserve the types and makes them accessible for study (Art. 75.3.7).

Amorphopini camouflage
The species of this tribe have the peculiarity of camouflaging themselves among lichens and bryophytes in humid environments of the Amazon (Cadena-Castañeda and Cardona-Granda 2015). When the Amorphopini feel threatened, they take positions to go unnoticed, placing themselves flattened on the substrate to ensure their camouflage with the environment. The front legs are extended towards the front and the middle and the rear legs remain next to the pronotum.
The most striking case is of A. notabilis. The individuals of this species exhibit a peculiar design that simulates the surface of trees or rocks covered by diverse lichen and bryophyte communities (Fig. 3). Its whitish coloration simulates foliose lichen (Parmeliacea and Lobariaceae) or scabby/crustacean lichen (Stereocaulaceae and Roccellaceae), and the reddish to pink coloration of the middle and half of the basal surface of the posterior femur resembles the scabby lichens of the family Arthoniaceae. The gray stripes and other greenish ones give the appearance of surrounding bryophytes mainly of the families Plagiochilacea and Leucobryaceae. They are usually observed covered by a green dust that consists of microalgae.

Polychromy in Amorphopini species
Color variation is more conspicuous in Eomorphopus species. The individuals of this genus are bluish black, yellowish with brown spots of different shades, light or dark brown (Fig. 7); parts of the body are light or dark brown, with or without stripes (Figs 10, 11). These color variations do not define geographic populations, can occur in specimens from the same locality, and the function of the color variation is still unknown but it may be linked to the microenvironments that individuals inhabit. In A. notabilis, the variations are very subtle and are restricted to the intensity of the gray stripes on the body and the reddish color of the middle and hind legs.