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A Second New Species of Ice Crawlers from China (Insecta: Grylloblattodea), with Thorax Evolution and the Prediction of Potential Distribution

  • Ming Bai,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Karl Jarvis,

    Affiliation Northern Arizona University, Flagstaff, Arizona, United States of America

  • Shu-Yong Wang,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Ke-Qing Song,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Yan-Ping Wang,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Zhi-Liang Wang,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Wen-Zhu Li,

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

  • Wei Wang,

    Affiliation Foreign Economic Cooperation Office, Ministry of Environmental Protection, Beijing, People's Republic of China

  • Xing-Ke Yang

    yangxk@ioz.ac.cn

    Affiliation Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, People's Republic of China

A Second New Species of Ice Crawlers from China (Insecta: Grylloblattodea), with Thorax Evolution and the Prediction of Potential Distribution

  • Ming Bai, 
  • Karl Jarvis, 
  • Shu-Yong Wang, 
  • Ke-Qing Song, 
  • Yan-Ping Wang, 
  • Zhi-Liang Wang, 
  • Wen-Zhu Li, 
  • Wei Wang, 
  • Xing-Ke Yang
PLOS
x

Abstract

Modern grylloblattids are one of the least diverse of the modern insect orders. The thorax changes in morphology might be associated with the changes of the function of the forelegs, wing loss, changes in behavior and adaptation to habitat. As temperature is the main barrier for migration of modern grylloblattids, the range of each species is extremely limited. The potential distribution areas of grylloblattids remain unclear. A second new species of ice crawlers (Insecta: Grylloblattodea), Grylloblattella cheni Bai, Wang et Yang sp. nov., is described from China. The distribution map and key to species of Grylloblattella are given. A comparison of the thorax of extant and extinct Grylloblattodea is presented, with an emphasis on the pronotum using geometric morphometric analysis, which may reflect thorax adaptation and the evolution of Grylloblattodea. Potential global distribution of grylloblattids is inferred. Highly diversified pronota of extinct Grylloblattodea may reflect diverse habitats and niches. The relatively homogeneous pronota of modern grylloblattids might be explained by two hypotheses: synapomorphy or convergent evolution. Most fossils of Grylloblattodea contain an obviously longer meso- and metathorax than prothorax. The length of the meso- and metathorax of modern grylloblattids is normally shorter than the prothorax. This may be associated with the wing loss, which is accompanied by muscle reduction and changes to the thoracic skeleton system. Threats to grylloblattids and several conservation comments are also provided.

Introduction

Modern grylloblattids (also known as ice bugs, ice crawlers, and rock crawlers), all occur northward of ∼35° latitude in cool-temperate areas of the United States, Canada, Russia, Japan, Korea and China, and they are restricted to cold and extreme habitats that are difficult to access. They are one of the least diverse of the modern insect orders, consisting of 29 species, including a new species described below. All of the known extant species, which belong to the family Grylloblattidae and 5 genera, Galloisiana, Grylloblattina, Grylloblattella, Namkungia and Grylloblatta. Ice crawlers can be considered as “living fossils” with presently relict distributions [1], [2]. Grylloblattids are generally found on north-facing talus slopes, snow patches near forest at high elevations (1500–3000 m), in caves with permanent ice at low elevations (300–1000 m) [3], [4], and some Grylloblattina are from 5 m–300 m, much lower than most other grylloblattids [5]. They live on and in soil, in caves, and beneath stones and in crevices of mountainous regions. They are principally carrion feeders on other insects, though they will consume plant material, fungus, and detritus [6].

Grylloblattids are extremely rare in China. Mr. Shu-Yong Wang collected the first grylloblattid from China, which was one male Galloisiana sinensis Wang, 1987 [7] specimen from Mt. Changbaishan, Jilin in 1986. Over 20 years later, Mr. Ke-Qing Song collected the second grylloblattid from China, which is one female Grylloblattella cheni sp. nov. in Akekule Lake (White Lake), Xinjiang, China. The inclusion of this species to Grylloblattella expands the genus to 3 species, the other two species being found in western to central Siberia, Russia: G. pravdini in the Altai Mountains and G. sayanensis in the Sayan Mountains (Fig. 1C).

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Figure 1. Grylloblattella cheni Bai, Wang et Yang sp. nov.

(A) Female. (B) Habitat. (C) Type localities of all known three species of Grylloblattella.

https://doi.org/10.1371/journal.pone.0012850.g001

Modern grylloblattids are 14–34 mm long, wingless, pale, and either nocturnal or cavernicolous. Adults have long cerci with 5–10 segments, and females have a sword-shaped ovipositor similar in shape to that of katydids (Orthoptera: Tettigoniidae). The single extant family can be contrasted with 46 families described from the fossil record, which extend to the Late Carboniferous [8], [9], [10]. The morphology of grylloblattodeans was stable with only minor changes during the ∼300 Million years of evolution, except thorax variations, which are the most significant difference between extant and extinct members of Grylloblattodea. The thorax, which contains the muscles of the legs and wings, had changed in some degree during the evolution of Grylloblattodea. This might be associated with the changes of the function of the forelegs, wing loss, changes in behavior and adaptation to habitat. Here we present a comparison of the thorax of extant and extinct Grylloblattodea, with an emphasis on the pronotum using geometric morphometric analysis, which may reflect thorax adaptation and the evolution of Grylloblattodea.

Few entomologists have ever collected these unique insects, and little is known about their life history and biology. However, the potential distribution areas of the world are relative broad according our prediction in this study. Industrial development, human activities and global warming may threaten unknown and undiscovered grylloblattids. Several conservation comments are also provided.

Results

Taxonomy

Genus Grylloblattella Storozhenko, 1988 [11]

Diagnosis: Grylloblattella can be distinguished from other genus in Grylloblattidae as follows: eyes black; antennae 27–38-segmented, epicranial suture not reaching the circumantennal suture; lacinia with one or two teeth; posterior margin of pronotum incurved, without marginal area; tarsal pulvilli visible; cerci 9–10-segmented; supra-anal plate of male symmetrical, project on the posterior margin with broadly rounded or truncate tip.

Grylloblattella cheni Bai, Wang et Yang sp. nov. (Figs 1A, 2A–I)

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Figure 2. Grylloblattella cheni Bai, Wang et Yang sp. nov., female.

(A) Habitus, lateral view. (B) Head, dorsal view. (C) Pronotum, dorsal view. (D) Cervical sclerites and eusterna of prothorax, ventral view. (E) Ovipositor, lateral view. (F) Ovipositor, dorsal view. (G) Basal antennomeres, left. (H) Lacinia with two preapical teeth, left. (I) Cercus, left.

https://doi.org/10.1371/journal.pone.0012850.g002

urn:lsid:zoobank.org:act:E0375431-6D0E-4949-B0A0-EA99A5927104

Holotype: Female, CHINA, Xinjiang Province, Buerjin County, Kanas Nature Reserve, 8 km west to Akekule Lake (White Lake), north of Kanas Lake, south-east of Mt. Youyifeng (Friendship Peak), N49.04173°, E87.49166°, 1750 m, raining, 2009-VII-24; collected by Ke-Qing SONG; deposited in the collection of the Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, People's Republic of China.

Etymology: This species is named in honor of Prof. Sicien Chen (Shixiang Chen), Fellow of Chinese Academy of Sciences, former PI for the Group of Morphology and Evolution of Coleoptera, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. Prof. Chen was the founder and former director of the Institute of Zoology, Chinese Academy of Sciences, and he made great contributions to entomological research of China.

Diagnosis: This new species can be attribute to Grylloblattella as follows: eyes black, epicranial suture not reaching the circumantennal suture, posterior margin of pronotum incurved, and tarsal pulvilli visible. Additionally, it can be distinguished from other species in Grylloblattidae as follows: antennae 38-segmented, cervical sclerites with five setae on each of the two lateral margins, lacinia with two teeth, and cerci 10-segmented. The key to species of Grylloblattella is given (Table 1).

Description: Female (holotype). Total body length 14.0 mm (measured from anterior margin of labrum to posterior margin of 10th abdominal segment) (Fig. 2A). Body colored heavy orange-brown on head and thorax, lighter in color on abdominal segments, and covered with numerous short hairs (Fig. 1A).

Head attached obliquely to pronotum (Fig. 2B). Cranium wider than long (length 2.2 mm, width 2.8 mm), with six setae on each lateral margin, two setae around the antennal socket, two setae near eye, three on the posterior of each side and no seta on the middle; epicranial suture distinctly Y-shaped, not reaching the circumantennal suture, and a pair of parietal sutures extending from the occipital foramen over to the vertex. Clypeus 2.8 times wider than long, projected on its anterior middle, with distinct clypeal suture. Lacinia with two teeth (Fig. 2H). Eyes black, elongated oval in shape (Fig. 2B). Antennae filiform, composed of 38 antennomeres, the 3rd segment 1.5 times as long as the 2nd (Fig. 2G).

Pronotum 1.1 times as long as wide, slightly concave in the posterior part, with a long median suture, some hairs on the anterior and lateral margins (Fig. 2C). Mesonotum slightly concave in the posterior part, with a long median suture. Metanotum with two setae on its mid-lateral side and two longitudinal short sutures in its anterior part.

Cervical sclerites about 1.3 times as long as wide, triangular, elongated anteriorly, with five setae on each of the two lateral margins and small setae on its posterior part (Fig. 2D). Basisternum of the prothorax 1.2 times as long as wide, triangular, expanded in the anterior part, with many scattered hairs. Katepisterna of the prothorax inclined, triangular in shape, situated near the posterior part of the cervical sclerite. Trochantin of the prothorax crescent shaped, with two setae on its distal part.

Legs elongate. Coxa with scattered setae and distinct ribs on the ventral part. Profemur with one row of setae on inner margin of ventral side, no seta on lateral side of profemur; meso- and metafemur with many scattered setae. Protibia with setae on ventral side and seta on lateral side; meso- and metatibia with many scattered setae; two large spines on the apical part of all tibia. Two setae each on the apical part of the 2nd and 3rd tarsi, white pulvilli and many long hairs on all tarsi, and two strong tarsal claws without teeth. Protarsus relative length of each segment (base to apex) 13∶8∶7∶6∶11. Mesotarsus relative length of each segment (base to apex) 16∶11∶7∶5∶10. Metatarsus relative length of each segment (base to apex) 19∶11∶8∶4∶10.

Abdominal tergites with lateral margin flexed to the posterior, 10-segmented, with one seta each on the posterior margin of the 1st to 8th tergites, one seta each on the mid-lateral side of the 2nd to 7th tergites. Abdominal sternites with lateral margin flexed to the posterior, without setae.

Cercomeres ten (length 7.2 mm), cylindrical, with one ring pattern of setae on the distal part of all cercomeres except the first and terminal one (Fig. 2I). Relative length of each segment (base to apex) 3∶3∶5∶8∶10∶12∶14∶16∶15∶10. 1st cercomere without seta; 2nd cercomere with 2 setae; 3rd cercomere with four setae; 4th cercomere with five setae; 5th cercomere with four setae; 6th and 7th cercomere with four setae each; 8th and 9th cercomere with three setae; 10th cercomere with one seta.

Ovipositor situated in the ventral part of the 8th and 9th abdominal segments, symmetrical, not attaining the distal end of the 6th cercomere; gonoplac (4.1 mm) longer than the others, with numerous setae on the dorsal part; gonangulum situated between the 8th sternite and 1st gonapophysis, asymmetrical “/ \”-shaped, slightly pointed; 1st gonapophysis (length 3.7 mm) slightly curved medially, with numerous bent hairs on the lower posterior part, adjoining gonangulum, and vertically emarginated mid-anterior part (Figs 2E–F).

Biological Notes: The species is known only from primary boreal coniferous forest (taiga), near Lake or river (Fig. 1B). The specimen collected was found under the bark of fallen dead tree, which near snow line (about 2 km away) in summer and could be covered by over 1 meter deep snow in winter. The temperature of type locality is from 0∼10°C in summer and −30∼0°C in winter.

Geographic Distribution: This species is known from the type locality near Akekule Lake (White Lake) and north of Kanas Lake, Kanas Nature Reserve, Buerjin County, Xinjiang Province, China (Fig. 1C).

Variations of pronotum morphology in Grylloblattodea

Geometric morphometrics can be used to determine shape differences, and the resulting phenograms from Procrustes distances can effectively indicate phenetic relationships, summarizing overall patterns of similarity [14]. Compared with other characters, the pronotum shows relatively high diversity in Grylloblattodea. We performed a morphometric analysis of the pronotum morphology of extant and extinct Grylloblattodea. This morphometric analysis allowed us to evaluate the similarity of the fossil pronotum to contemporary pronotum.

There were 50 equidistant semilandmarks chosen on the outline of the pronotum (tps-DIG 2.05, curve). The consensus configuration for each genus was determined and the images of each species of the genus ‘unwarped’ so that the semilandmarks coincided with their positions in the consensus configuration. All the species in a single genus were then superimposed onto one another. Analyses of the data set using tps-SMALL indicated that an excellent correlation between the tangent and the shape space existed (Fig. 3A). The correlation (uncentred) between the tangent space, Y, regressed onto Procrustes distance (geodesic distances in radians) was 0.999993. There was little doubt on the basis of the result from tps-SMALL, which supported the hypothesis that genus within a taxon such as a family can be analyzed by geometric morphometric methods since the results from the statistical test performed by tps-SMALL proved the acceptability of the data set for further statistical analysis [14].

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Figure 3. Pronotum shape variation test and shape differences of 13 grylloblattids genera.

(A) Shape variation test tps-SMALL 1.2. (B) Ordination of the 13 grylloblattids genera means along the three canonical varieties axes based on the Procrustes distance matrix. (1) Blattogryllulus; (2) Parasheimia; (3) Plesioblattogryllus; (4) Sojanorapbidia; (5) Sylvamicropteron; (6) Sylvonympha; (7) Tataronympha; (8) Tillyardembia; (9) Galloisiana; (10) Grylloblatta; (11) Grylloblattella; (12) Grylloblattina; (13) Namkungia. Green circle includes the extant 5 grylloblattids genera.

https://doi.org/10.1371/journal.pone.0012850.g003

The first two relative warps of the semilandmarks accounted for 81.85% of the variation among the genera. These were computed by a singular-value decomposition of the weight matrix [15]. The first two relative warps were plotted to indicate variation along the two axes (Fig. 4A). The shape changes of different genera implied by variation along the first two relative warp axes and shape changes were shown as deformations of the GLS reference, using thin-plate splines (Fig. 4A). The spline of each genus showed the deformation of the semilandmarks in comparison to that of the reference. The five modern genera are in the First Quadrant and other eight fossil genera are in the other Quadrants.

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Figure 4. Pronotum shape differences of 13 grylloblattids genera.

(A) Relative warps computed from the data set, plotted against one another to indicate positions of the relationships among genera relative to one another and to the reference configuration (situated at the origin). The shape changes of different families implied by variation along the first two relative warp axes. Shape changes are shown as deformations of the GLS reference, using thin-plate splines. (B) Phenetic tree (UPGMA), the trees compiled using NTSYS-pc based on Procrustes distances among the genera.

https://doi.org/10.1371/journal.pone.0012850.g004

The 13 grylloblattodean genera means were plotted along the three canonical varieties axes based on the Procrustes distance matrix (Fig. 3B). UPGMA phenogram [16] of the pronotum of the 13 studied genera based on Procrustes distance matrix are presented in Figure 4B. The results indicate a good correlation between the scatter plots (Figs 3B, 4A) and the phenograms (produced from the Procrustes distances) (Fig. 4B). Genera clustering together in the phenograms are closely situated on the scatter plot of the first two relative warps.

Discussion

Phylogenetic relationships among fossil and extant grylloblattodeans

The relationships between grylloblattodean fossil taxa and the modern grylloblattids remain unclear because most fossils are based on isolated wings or have poorly preserved body features. Wheeler et al. [17] proposed that the modern Grylloblattidae were the sister group of the Dermaptera, being together the sister group of (Phasmida + Orthoptera), and that the (Plecoptera + Embioptera) were not directly related to this clade. Beutel and Gorb [18] claimed that the Grylloblattidae were the sister group of the clade {Phasmatodea + [Mantodea + (Isoptera + Blattodea)]}. Grimaldi [19] considered that the extant and fossil ‘Grylloblattodea’ fell in an unresolved polytomy with the majority of the other ‘polyneopteran’ orders. Molecular phylogenies from Terry and Whiting [20] and Cameron, Barker and Whiting [21] indicated that Grylloblattodea could be the sister group of the recently discovered order Mantophasmatodea, and altogether could be the sister group of the Dictyoptera. Grimaldi and Engel [22] also considered that the Palaeozoic and Mesozoic alate ‘grylloblattids’ could represent a stem group of both apterous Grylloblattodea and Mantophasmatodea. Lastly, even if Rasnitsyn [23], [24] listed several similarities between Blattogryllus and the extant Grylloblattidae, the potential synapomorphies of this last group with the fossil ‘Grylloblattodea’ are not clear. We present possible relationships of all modern grylloblattids and eight extinct genera based on the morphology of pronotum, which is a highly diverse character in Grylloblattodea. This result suggests a new way to infer the phylogeny of fossil taxa and modern grylloblattids, which bridge the huge gap between extremely diverse extinct winged taxa and rare extant wingless grylloblattids.

Little is known of extant grylloblattid genus and species phylogeny. Storozhenko [25] proposed a phylogeny of four extant grylloblattid genera, Grylloblatta, Galloisiana, Grylloblattina, and Grylloblattella, based on an intuitive analysis of ten morphological and two habitat characters. A single character supports the monophyly of the Asian genera (presence of four to eight setae on the edges of the cervical sclerites, as opposed to none in Grylloblatta), rendering the Asian genera as sister group to Grylloblatta [25]. Among the Asian genera, Storozhenko places Grylloblattina as sister to Galloisiana+Grylloblattella, supported by the narrow elongated condition of the right coxopodite of abdominal segment IX of the male in Galloisiana and Grylloblattella rather than a short thickened one in Grylloblattella. Jarvis and Whiting [1] presents the first-ever formal phylogenetic hypothesis of modern grylloblattid genera and species based on molecular evidence. The topology confirms the monophyly of the three genera included in the analysis: Grylloblatta, Galloisiana, and Grylloblattina. The analysis indicates that the eastern Asian genus Galloisiana is sister to a monophyletic group of the east Siberian Grylloblattina and the North American Grylloblatta. Our result not only confirms the phylogenetic hypothesis of Grylloblatta, Galloisiana, and Grylloblattina from Jarvis and Whiting [1], but also presents the relationships of all known modern grylloblattid genera.

Thorax evolution in Grylloblattodea

The thorax must have evolved early in the phylogenetic history of the Hexapoda as a locomotor section of the body through the specialization of its appendages for quicker movement [26]. The evolution of thorax morphology may be correlated with movement functions involved in walking and flying.

Our results indicate that there was much higher diversity in the pronotum of fossil species than in modern grylloblattids. This may be due to the totally different habitats in extant and extinct species. The food habits of the early grylloblattodeans, such as pollen feeding, predation, etc., were very diverse, according to the fossil record. For example, Plesioblattogryllus magnificus from Middle Jurassic with the movable structures composed of the fore tarsal claws, the most apical tarsomeres, and very strong mandibles with a sharp pointed apical tooth is considered as an active hunter [27]. Winged members of Grylloblattodea might have lived in a relatively warm environment and a variety of habitat types in the Paleozoic and Mesozoic Era. Highly diversified pronota might reflect a diverse habitats and niches. Modern grylloblattids probably became adapted to live under rocks or hidden in moss from cold areas. The lack of pronotal variation in modern grylloblattids might be explained by two hypotheses: synapomorphy or convergent evolution. The first hypothesis proposes a single clade supported by the character of a nearly rectangular pronotum, which has survived after the extinction of other grylloblattodean taxa. The second hypothesis proposes that the pronotum of the ancestors of modern grylloblattids were different in shape. After the extinction of most grylloblattodeans, the remaining species lived in similar environments, which drove convergent evolution in pronotum shape.

Insects are the only invertebrate animals which have wings. Flight conferred an increased ability to access resources, locate mates and escape predators [28], and has undoubtedly contributed to the success of insects. Despite the obvious advantages of flight, this dispersal capacity has been lost repeatedly [29], [30] in nearly all winged orders [31]. The loss of flight, typically due to a reduction in wing length, has been attributed to the high energy expenditure required in the production and maintenance of flight apparatus, at the expense of other life-history traits [32]. Low temperature may be the key factor for the wing loss [33]. Wings are only found on the mesothorax and metathorax, and the prothorax never bears wings in extant insects. Mesothorax and metathorax of grylloblattids maintain very low variation in shape during ∼300 Million years evolution, which bears the wings in Paleozoic and Mesozoic Era. Most grylloblattid fossils contain an obviously longer meso- and metathorax than prothorax. The length of the meso- and metathorax of modern grylloblattids is normally shorter than the prothorax. This may be associated with the wing loss, which is accompanied by muscle reduction and changes to the thoracic skeleton system.

Threats to grylloblattids and potential distribution areas

As temperature is the main barriers for migration of modern grylloblattids, the distribution area of one species is very limited. Migration among populations is almost certainly severely limited or non-existent in current conditions due to grylloblattids' habitat specificity, limited geographic range of populations, and winglessness [4]. The warming of the planet since the last glaciation, compounded by human-induced global warming in recent years is causing the rapid loss of glaciers and ice sheets [34], [35], [36], [37]. In the next few decades, the rate at which glaciers are melting is expected to increase by two to four times from their already high rate, largely due to anthropogenic causes [34]. Grylloblattids' dependence on glacial margin habitats means that global warming is a direct threat to their future. Resilience of grylloblattid habitat cannot be expected without significant changes in factors linked to glacial decline.

Another potentially significant threat to grylloblattids is development of their habitat. The known localities (Fig. 5A, black dots) of grylloblattids are very remote areas, and the potential distribution areas we inferred have environments similar to those of known distribution localities. As grylloblattids can be found in two typical place: high mountain and ice cave which might from lowland or mountain, we run the two prediction analyses. Firstly, all occurrence locations with coordinates were selected for the raw analysis, which could reflect the all possible areas (Fig. 5A). Our results show that the potential distribution of grylloblattid species are near regions populated by humans (Fig. 5A and 5B) [38]. In 2015 [39], the distribution and density of human populations be greater than in 2000 (Figs 5B–C). Human interference has caused major environmental damage in potential and actual distribution areas of grylloblattids. Based on these evidences, we propose two areas (Fig. 5A, red circles) in which grylloblattids may possibly occur. We assume that the high degree of human interference in Europe (Fig. 5A, blue circle) would greatly reduce the potential to find grylloblattids there.

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Figure 5. The comparison of the prediction map of grylloblattids and the map of Population Density of the world.

(A) Prediction of potential distribution areas of grylloblattids; black dots  =  selected known localities, green areas  =  potential distribution areas, red circles  =  the most potential areas, blue circle  =  the least potential areas. (B) Population Density of the world in 2000 (after CIESIN and CIAT 2005). (C) Population Density of the world in 2015 (after CIESIN, FAO and CIAT 2005).

https://doi.org/10.1371/journal.pone.0012850.g005

Secondly, only high mountain data were used in the specific analysis for the prediction of high mountain grylloblattids (Fig. 6A). This map is almost same to the first prediction analysis (see Fig 5A), but a little bit shrinking in the prediction areas. The amplificatory map of two areas (Fig. 6A, red circles) indicates where grylloblattids may possibly occur.

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Figure 6. Prediction map of grylloblattids based on the 19 coordinates of terrestrial ice crawlers.

(A) Prediction of potential distribution areas of grylloblattids. (B) Areas in the US with the most potential. (C) Areas in Asia with the most potential areas. Black dots  =  selected known localities, purple areas (in A)  =  potential distribution areas, green areas (in B or C)  =  potential distribution areas, red circles (in A)  =  areas with the most potential.

https://doi.org/10.1371/journal.pone.0012850.g006

The purpose of our prediction research is not to explain the distribution of grylloblattids, but to predict where potential areas are. The reason why many grylloblattids have been found in Japan (see Fig. 5A) may be due to high human population density close to pristine grylloblattid habitat. For example, it is doubtful that there are many more new species that could be found in Japan because of how much work has been done on grylloblattids there already. In the recent past, no new species have been found in Japan, but in South Korea and China there have been several new species discovered [2], [40]. We expect that more undiscovered species could exist in many of the other predicted areas shaded green, but that it depends on 1) the accessibility of relatively undisturbed grylloblattid habitat, and 2) the number of people interested and knowledgeable enough to search for and describe new species.

The reason for the collection of Grylloblattella cheni Bai, Wang et Yang sp. nov. by Mr. Ke-Qing Song was an environmental assessment project on planned railway construction in Xinjiang, China. The report (unpublished report for North Xinjiang Environment Exploration Program) based on this assessment concluded that although the precise effects of railway construction on Grylloblattella cheni cannot be determined, there will certainly be detrimental effects on this exceptionally rare species. In order to preserve grylloblattid habitat, we suggest the railway be routed through lower elevation terrain, which would cause minimal disturbance to grylloblattids.

Potential distribution areas of grylloblattids are scattered over much wider areas than the very limited type localities (Fig. 5A). Most of these potential distribution areas are remote areas that are typically low in biodiversity. None of these areas are in the list of the well-known biodiversity hotspots, and insect surveys for conservation purposes are rarely conducted. Therefore it is imperative that more research be done in these regions in order to provide insight into the ecosystems that contain these unique organisms.

Materials and Methods

Nomenclatural Acts

The electronic version of this document does not represent a published work according to the International Code of Zoological Nomenclature (ICZN), and hence the nomenclatural acts contained in the electronic version are not available under that Code from the electronic edition. Therefore, a separate edition of this document was produced by a method that assures numerous identical and durable copies, and those copies were simultaneously obtainable (from the publication date noted on the first page of this article) for the purpose of providing a public and permanent scientific record, in accordance with Article 8.1 of the Code. The separate print-only edition is available on request from PLoS by sending a request to PLoS ONE, 1160 Battery Street Suite 100, San Francisco, CA 94111, USA along with a check for $10 (to cover printing and postage) payable to “Public Library of Science”.

In addition, this published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix “http://zoobank.org/”. The LSID for this publication is: urn:lsid:zoobank.org:pub:1157690F-E3D2-4684-82DB-B6872A7F4964.

Geometric morphometric analysis

Digital images of grylloblattodean pronota for the morphometric analysis were from the references, edited and enhanced by Photoshop (Version 9.0). Eight fossil species belonging to eight genera and 20 extant species belonging to five genera were included in the analysis (Table 2). As most fossils of Grylloblattodea are based on isolated wings or have poorly preserved body features, only eight genera with complete pronota in the fossils are involved included in the analysis (Fig. 7).

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Figure 7. Pronotum shape of 13 grylloblattids for the geometric morphometric analysis.

(A) Blattogryllulus mongolicus Storozhenko, 1988 (Fossil). (B) Parasheimia truncata Aristov, 2004 (Fossil). (C) Plesioblattogryllus magnificus Huang, 2008 (Fossil). (D) Sojanorapbidia martynovae Storozhenko et Novokshonov, 1994 (Fossil). (E) Sylvamicropteron harpax Aristov, 2004 (Fossil). (F) Sylvonympha tshekardensis Novokshonov et Pan'kov, 1999 (Fossil). (G) Tataronympha kamensis Aristov, Novokshonov et Pan'kov, 2006 (Fossil). (H) Tillyardembia antennaeplana Zalessky, 1938 (Fossil). (I) Galloisiana chujoi Gurney, 1961. (J) G. kiyosawai Asahina, 1959. (K) G. kosuensis Namkung, 1974. (L) G. nipponensis (Caudell et King, 1924). (M) G. odaesanensis Kim et Lee, 2007. (N) G. olgae Vrsansky et Storozhenko, 2001. (O) G. sinensis Wang, 1987. (P) G. ussuriensis Storozhenko, 1988. (Q) G. yezoensis Asahina, 1961. (R) G. yuasai Asahina, 1959. (S) Grylloblatta barberi Caudell, 1924. (T) G. campodeiformis Walker, 1914. (U) G. chandleri Kamp, 1963. (V) G. gurneyi Kamp, 1963. (W) G. sculleni Gurney 1937. (X) Grylloblattella cheni Bai, Wang et Yang sp. nov. (Y) G. pravdini (Storozhenko et Oliger, 1984). (Z) G. sayanensis Storozhenko, 1996. (AA) Grylloblattina djakonovi Bey-Bienko, 1951. (AB) Namkungia biryongensis (Namkung, 1974).

https://doi.org/10.1371/journal.pone.0012850.g007

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Table 2. Geometric morphometric analysis of grylloblattodean pronota represented by eight fossil species and 20 extant species.

https://doi.org/10.1371/journal.pone.0012850.t002

In this study, 50 semilandmarks were selected. Photographs were input to tps-UTILS 1.38 [58] and Cartesian coordinates of semilandmarks were digitized with tps-DIG 2.05 [59]. We drew a curve along the outer margin of the pronotum first. Then 50 semilandmarks were resampled by length for the curve. Semilandmark configurations were scaled, translated and rotated against the consensus configuration using the GLS Procrustes superimposition method [60]. We used tps-SMALL 1.2 [61] to test whether the observed variation in shape was sufficiently small that the distribution of points in the tangent space can be used as a good approximation of their distribution in shape space (Fig. 3A). Because shape differences between genera were studied, the average or consensus configuration of semilandmarks for each genus was computed using tps-SUPER 1.14 [62]. Orthogonal least-squares Procrustes average configurations of semilandmarks were computed using generalized orthogonal least-squares procedures. Then the new TPS file with 13 taxa was created for the following process. The coordinates were analyzed using tps-RELW 1.44 [63] to calculate eigenvalues for each principal warp (Fig. 4A). Procrustes distances (the square root of the sum of squared differences between corresponding points) between each of the genera were computed and the matrix was produced by the tps-SPLIN 1.20 [64]. The Procrustes distance matrix was subjected to UPGMA (unweighted pair group method using arithmetic averages) generated by NTSYSpc [65] to determine the phenetic relationships among genera (Fig. 4B). The most important advantage of using Procrustes distances to capture shape variation was that these distances were considered the best method for measuring shape differences among taxa [14], [66], [67], [68], [69], [70].

Prediction of potential distribution areas of grylloblattids

Ecological niches and geographic distributional prediction of ice crawlers were modeled using the Genetic Algorithm for Rule-set Prediction (GARP) [71], implemented as DesktopGarp v.1.1.6 downloaded from http://www.nhm.ku.edu/desktopgarp/Download.html. DesktopGarp is a software package for biodiversity and ecological research, which models ecological niches of species and predicts their potential distributions [71].

The geographic potential distributions were generated with GARP through a genetic algorithm that creates a series of rules matching the species specific ecological characteristics with known location occurrences [72], [73].

The species' current distributional points and the environmental datasets designed from groups of environmental layers were entered into DesktopGarp. The environmental data layers were available through the DesktopGarp website.

The ice crawler occurrence data were obtained from the published literature, available specimen from museum or personal collections. Over hundreds of distribution data of grylloblattids were collected at first. Due to the lack of coordinates for most of them, only 42 occurrence locations with coordinates were selected for our analysis (Table S1). As 23 occurrence locations represented ice caves from lowland, which could not be very idea data resource for the prediction of potential distribution areas of none-cave-living ice crawler. We ran the prediction analysis again based on the 19 coordinates of mountain ice crawler populations, for which data from ice caves were excluded.

Acknowledgments

Discovery of the unique specimen resulted from North Xinjiang Environment Exploration Program presided by Dr. Run-Zhi Zhang, Professor of the Institute of Zoology, Chinese Academy of Sciences. We are grateful to the two anonymous reviewers for helpful comments. Dr. Si-Qin GE, Dr. Huai-Jun XUE, and Mrs. Gan-Yan YANG from the Institute of Zoology, Chinese Academy of Sciences, who have given us much valuable advice on the early version of the manuscript. We thank Mr. Jian WANG and Mr. Ji-Jiang XUE from Forestry Bureau of Aletai, who arranged the collecting trip in Kanas; Prof. Qi-Sen YANG, Dr. Lin XIA from the Institute of Zoology, Chinese Academy of Sciences and Mr. Guo-Zhong ZHANG from the Forestry Bureau of Aletai, who was very helpful with the collecting trip. Mr. Rod Crawford from University of Washington Burke Museum gave great help to Karl Jarvis for the distribution data collecting.

Author Contributions

Conceived and designed the experiments: MB XKY. Analyzed the data: MB YPW. Contributed reagents/materials/analysis tools: SYW KQS ZLW WZL WW. Wrote the paper: MB KJ.

References

  1. 1. Jarvis KJ, Whiting MF (2006) Phylogeny and biogeography of ice crawlers (Insecta: Grylloblattodea) based on six molecular loci: Designating conservation status for Grylloblattodea species. Molecular Phylogenetics and Evolution 41: 222–237.KJ JarvisMF Whiting2006Phylogeny and biogeography of ice crawlers (Insecta: Grylloblattodea) based on six molecular loci: Designating conservation status for Grylloblattodea species.Molecular Phylogenetics and Evolution41222237
  2. 2. Vrsansky P, Storozhenko SY, Labandeira CC, Ihringova P (2001) Galloisiana olgae sp nov (Grylloblattodea: Grylloblattidae) and the paleobiology of a relict order of insects. Annals of the Entomological Society of America 94: 179–184.P. VrsanskySY StorozhenkoCC LabandeiraP. Ihringova2001Galloisiana olgae sp nov (Grylloblattodea: Grylloblattidae) and the paleobiology of a relict order of insects.Annals of the Entomological Society of America94179184
  3. 3. Kamp JW (1963) Descriptions of two new species of Grylloblattidae and of the adult of Grylloblatta barben with an interpretation of their geographical distribution. Ann ent Soc Amer, Baltimore 56: 53–68.JW Kamp1963Descriptions of two new species of Grylloblattidae and of the adult of Grylloblatta barben with an interpretation of their geographical distribution.Ann ent Soc Amer, Baltimore565368
  4. 4. Kamp JW (1979) Taxonomy, distribution, and zoogeographic evolution of Grylloblatta in Canada (Insecta: Notoptera). The Canadian Entomologist 111: 27–38.JW Kamp1979Taxonomy, distribution, and zoogeographic evolution of Grylloblatta in Canada (Insecta: Notoptera).The Canadian Entomologist1112738
  5. 5. Pravdin FN, Storozhenko SY (1977) Novyi Vid Grylloblattid (Insecta, Grylloblattida) iz Yuzhnovo Primorye (A new species of Grylloblattid (Insecta: Grylloblattida) from southern Primorye). Entomol Obozr 56: 352–356.FN PravdinSY Storozhenko1977Novyi Vid Grylloblattid (Insecta, Grylloblattida) iz Yuzhnovo Primorye (A new species of Grylloblattid (Insecta: Grylloblattida) from southern Primorye).Entomol Obozr56352356
  6. 6. Pritchard G, Scholefield P (1978) Observations on the food, feeding behaviour, and associated sense organs of Grylloblatta campodeiformis (Grylloblattodea). Canadian Entomologist 110: 205–212.G. PritchardP. Scholefield1978Observations on the food, feeding behaviour, and associated sense organs of Grylloblatta campodeiformis (Grylloblattodea).Canadian Entomologist110205212
  7. 7. Wang SY (1987) The discovery of Grylloblattodea in china and the description of a new species. Acta Entomologica Sinica 30: 423–429.SY Wang1987The discovery of Grylloblattodea in china and the description of a new species.Acta Entomologica Sinica30423429
  8. 8. Aristov D, Zessin W (2009) [Mallorcagryllus hispanicus n. gen. et sp. - a new grylloblattid (Insecta: Grylloblattida: Blattogryllidae) from the Buntsandstein of the island of Mallorca, Spain.]. Virgo 12: 30–34.D. AristovW. Zessin2009[Mallorcagryllus hispanicus n. gen. et sp. - a new grylloblattid (Insecta: Grylloblattida: Blattogryllidae) from the Buntsandstein of the island of Mallorca, Spain.].Virgo123034
  9. 9. Storozhenko SY (1992) New fossil Grylloblattida Insecta (Insecta: Grylloblattida) from Mongolia. Sovmestnaya Sovetsko-Mongol'skaya Paleontologicheskaya Ekspeditsiya Trudy 41: 122–129.SY Storozhenko1992New fossil Grylloblattida Insecta (Insecta: Grylloblattida) from Mongolia.Sovmestnaya Sovetsko-Mongol'skaya Paleontologicheskaya Ekspeditsiya Trudy41122129
  10. 10. Storozhenko SY (1997) Classification of order Grylloblattida (Insecta), with description of new taxa. Far Eastern Entomologist 42: 1–20.SY Storozhenko1997Classification of order Grylloblattida (Insecta), with description of new taxa.Far Eastern Entomologist42120
  11. 11. Storozhenko S (1988) A review of the family Grylloplattidae [Grylloblattidae] (Insecta). Articulata 3: 167–181.S. Storozhenko1988A review of the family Grylloplattidae [Grylloblattidae] (Insecta).Articulata3167181
  12. 12. Storozhenko SY (1996) A new species of Grylloblattella Storozhenko, 1988 from Siberia (Grylloblattida). Zoosystematica Rossica 4: 320.SY Storozhenko1996A new species of Grylloblattella Storozhenko, 1988 from Siberia (Grylloblattida).Zoosystematica Rossica4320
  13. 13. Storozhenko SY, Oliger AI (1984) A new species of Grylloblattida from northeastern Altai USSR. Entomologicheskoe Obozrenie 63: 729–732.SY StorozhenkoAI Oliger1984A new species of Grylloblattida from northeastern Altai USSR.Entomologicheskoe Obozrenie63729732
  14. 14. Pretorius E, Scholtz CH (2001) Geometric morphometries and the analysis of higher taxa: a case study based on the metendosternite of the Scarabaeoidea (Coleoptera). Biological Journal of the Linnean Society 74: 35–50.E. PretoriusCH Scholtz2001Geometric morphometries and the analysis of higher taxa: a case study based on the metendosternite of the Scarabaeoidea (Coleoptera).Biological Journal of the Linnean Society743550
  15. 15. Rohlf FJ (1993) Relative-warp analysis and example of its application to mosquito wings. In: Marcus LF, Bello E, Garcia-Valdecasas A, editors. Contributions to morphometrics. Madrid: Museo Nacional de Ciencias Naturales. pp. 131–159.FJ Rohlf1993Relative-warp analysis and example of its application to mosquito wings.LF MarcusE. BelloA. Garcia-ValdecasasContributions to morphometricsMadridMuseo Nacional de Ciencias Naturales131159
  16. 16. Sneath PHA, Sokal RR (1973) Numerical taxonomy. New York: Freeman. PHA SneathRR Sokal1973Numerical taxonomy.New YorkFreeman
  17. 17. Wheeler WC, Whiting M, Wheeler QD, Carpenter JM (2001) The phylogeny of the extant hexapod orders. Cladistics 17: 113–169.WC WheelerM. WhitingQD WheelerJM Carpenter2001The phylogeny of the extant hexapod orders.Cladistics17113169
  18. 18. Beutel RG, Gorb SN (2001) Ultrastructure of attachment specializations of hexapods, (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny. Journal of Zoological Systematics and Evolutionary Research 39: 177–207.RG BeutelSN Gorb2001Ultrastructure of attachment specializations of hexapods, (Arthropoda): evolutionary patterns inferred from a revised ordinal phylogeny.Journal of Zoological Systematics and Evolutionary Research39177207
  19. 19. Grimaldi D (2001) Insect evolutionary history from Handlirsch to Hennig, and beyond. Journal of Paleontology 75: 1152–1160.D. Grimaldi2001Insect evolutionary history from Handlirsch to Hennig, and beyond.Journal of Paleontology7511521160
  20. 20. Terry MD, Whiting MF (2005) Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21: 240–257.MD TerryMF Whiting2005Mantophasmatodea and phylogeny of the lower neopterous insects.Cladistics21240257
  21. 21. Cameron SL, Barker SC, Whiting MF (2006) Mitochondrial genomics and the new insect order Mantophasmatodea. Molecular Phylogenetics and Evolution 38: 274–279.SL CameronSC BarkerMF Whiting2006Mitochondrial genomics and the new insect order Mantophasmatodea.Molecular Phylogenetics and Evolution38274279
  22. 22. Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge: Cambridge University Press. D. GrimaldiMS Engel2005Evolution of the insects.CambridgeCambridge University Press
  23. 23. Rasnitsyn AP (1976) Grylloblattids - living representatives of order of Protoblattodea (Insecta). Doklady Akademii Nauk SSSR 228: 502–504.AP Rasnitsyn1976Grylloblattids - living representatives of order of Protoblattodea (Insecta).Doklady Akademii Nauk SSSR228502504
  24. 24. Rasnitsyn AP (1980) [The historical development of the Insecta. Order Grylloblattidea.]. Trudy Paleontologicheskogo Instituta 175: 150–154.AP Rasnitsyn1980[The historical development of the Insecta. Order Grylloblattidea.].Trudy Paleontologicheskogo Instituta175150154
  25. 25. Storozhenko SY (1996) On origin and historical development of the family Grylloblattidae (Insecta: Grylloblattida). Chteniya Pamyati Alekseya Ivanovicha Kurentsova 6: 13–20.SY Storozhenko1996On origin and historical development of the family Grylloblattidae (Insecta: Grylloblattida).Chteniya Pamyati Alekseya Ivanovicha Kurentsova61320
  26. 26. Snodgrass RE (1935) Principles of insect morphology. New York & London: McGraw-Hill Book Co., Inc. RE Snodgrass1935Principles of insect morphology.New York & LondonMcGraw-Hill Book Co., Inc
  27. 27. Huang DY, Nel A, Petrulevicius JF (2008) New evolutionary evidence of Grylloblattida from the Middle Jurassic of Inner Mongolia, north-east China (Insecta, Polyneoptera). Zoological Journal of the Linnean Society 152: 17–24.DY HuangA. NelJF Petrulevicius2008New evolutionary evidence of Grylloblattida from the Middle Jurassic of Inner Mongolia, north-east China (Insecta, Polyneoptera).Zoological Journal of the Linnean Society1521724
  28. 28. Denno RF, Hawthorne DJ, Thorne BL, Gratton C (2001) Reduced flight capability in British Virgin Island populations of a wing-dimorphic insect: the role of habitat isolation, persistence, and structure. Ecological Entomology 26: 25–36.RF DennoDJ HawthorneBL ThorneC. Gratton2001Reduced flight capability in British Virgin Island populations of a wing-dimorphic insect: the role of habitat isolation, persistence, and structure.Ecological Entomology262536
  29. 29. Roff DA (1990) The Evolution of Flightlessness in Insects. Ecological Monographs 60: 389–421.DA Roff1990The Evolution of Flightlessness in Insects.Ecological Monographs60389421
  30. 30. Wagner DL, Liebherr JK (1992) Flightlessness in insects. Trends in Ecology & Evolution 7: 216–220.DL WagnerJK Liebherr1992Flightlessness in insects.Trends in Ecology & Evolution7216220
  31. 31. Roff DA (1994) Habitat persistence and the evolution of wing dimorphism in insects. American Naturalist 144: 772–798.DA Roff1994Habitat persistence and the evolution of wing dimorphism in insects.American Naturalist144772798
  32. 32. Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology 42: 207–230.AJ ZeraRF Denno1997Physiology and ecology of dispersal polymorphism in insects.Annual Review of Entomology42207230
  33. 33. Byers GW (1969) Evolution of Wing Reduction in Crane Flies (Diptera: Tipulidae). Evolution 23: 346–354.GW Byers1969Evolution of Wing Reduction in Crane Flies (Diptera: Tipulidae).Evolution23346354
  34. 34. Haeberli W, Frauenfelder R, Hoelzle M, Maisch M (1999) On rates and acceleration trends of global glacier mass changes. Geografiska Annaler Series a-Physical Geography 81A: 585–591.W. HaeberliR. FrauenfelderM. HoelzleM. Maisch1999On rates and acceleration trends of global glacier mass changes.Geografiska Annaler Series a-Physical Geography81A585591
  35. 35. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, et al. (2001) Climate Change 2001: The Scientific Basis. Cambridge: Cambridge University Press. JT HoughtonY. DingDJ GriggsM. NoguerPJ van der Linden2001Climate Change 2001: The Scientific Basis.CambridgeCambridge University Press
  36. 36. Winkler S, Matthews JA (2010) Observations on terminal moraine-ridge formation during recent advances of southern Norwegian glaciers. Geomorphology 116: 87–106.S. WinklerJA Matthews2010Observations on terminal moraine-ridge formation during recent advances of southern Norwegian glaciers.Geomorphology11687106
  37. 37. Zemp M, Roer I, Kääb A, Hoelzle M, Paul F, et al. (2008) Global Glacier Changes: Facts and Figures. Zürich, Switzerland: World Glacier Monitoring Service. M. ZempI. RoerA. KääbM. HoelzleF. Paul2008Global Glacier Changes: Facts and Figures.Zürich, SwitzerlandWorld Glacier Monitoring Service
  38. 38. University CfIESINCC, (CIAT) CIdAT (2005) Gridded Population of the World Version 3 (GPWv3): Population Density Grids. Palisades, NY: Socioeconomic Data and Applications Center (SEDAC), Columbia University.. University CfIESINCC, (CIAT) CIdAT2005Gridded Population of the World Version 3 (GPWv3): Population Density Grids.Palisades, NYSocioeconomic Data and Applications Center (SEDAC), Columbia University.http://sedac.ciesin.columbia.edu/gpw. http://sedac.ciesin.columbia.edu/gpw.
  39. 39. University CfIESINCC, (FAO) UNFaAP, (CIAT) CIdAT (2005) Gridded Population of the World: Future Estimates, 2015 (GPW2015): Population Density Grids. Palisades, NY: Socioeconomic Data and Applications Center (SEDAC), Columbia University.. University CfIESINCC, (FAO) UNFaAP, (CIAT) CIdAT2005Gridded Population of the World: Future Estimates, 2015 (GPW2015): Population Density Grids.Palisades, NYSocioeconomic Data and Applications Center (SEDAC), Columbia University.http://sedac.ciesin.columbia.edu/gpw. http://sedac.ciesin.columbia.edu/gpw.
  40. 40. Storozhenko SY, Park JK (2002) A new genus of the ice crawlers (Grylloblattida: Grylloblattidae) from Korea. Far East Entomol 114: 18–20.SY StorozhenkoJK Park2002A new genus of the ice crawlers (Grylloblattida: Grylloblattidae) from Korea.Far East Entomol1141820
  41. 41. Storozhenko SY (1988) [New and little-known Mesozoic Grylloblattida (Insecta).]. Paleontologicheskii Zhurnal 1988: 48–54.SY Storozhenko1988[New and little-known Mesozoic Grylloblattida (Insecta).].Paleontologicheskii Zhurnal19884854
  42. 42. Aristov DS (2004) The fauna of grylloblattid insects (Grylloblattida) of the Lower Permian locality of Tshekarda. Paleontological Journal 38: S80–S145.DS Aristov2004The fauna of grylloblattid insects (Grylloblattida) of the Lower Permian locality of Tshekarda.Paleontological Journal38S80S145
  43. 43. Storozhenko SY, Novokshonov VG (1994) Revision of the Permian family Sojanoraphidiidae (Grylloblattida). Russian Entomological Journal 3: 37–39.SY StorozhenkoVG Novokshonov1994Revision of the Permian family Sojanoraphidiidae (Grylloblattida).Russian Entomological Journal33739
  44. 44. Novokshonov VG, Pan'kov NN (1999) A new aquatic insect larva (Plecopteroidea) from the Lower Permian of the Ural. Neues Jahrbuch Fur Geologie Und Palaontologie-Monatshefte 193–198.VG NovokshonovNN Pan'kov1999A new aquatic insect larva (Plecopteroidea) from the Lower Permian of the Ural.Neues Jahrbuch Fur Geologie Und Palaontologie-Monatshefte193198
  45. 45. Aristov DS, Novokshonov VG, Pan'kov NN (2006) Taxonomy of the fossil grylloblattid nymphs (Insecta: Grylloblattida). Paleontological Journal 40: 79–89.DS AristovVG NovokshonovNN Pan'kov2006Taxonomy of the fossil grylloblattid nymphs (Insecta: Grylloblattida).Paleontological Journal407989
  46. 46. Zalessky G (1938) Nouveaux insectes permiens de l'ordre des Embiodea. Ann Soc geol Nord, Lille 63: 62–81.G. Zalessky1938Nouveaux insectes permiens de l'ordre des Embiodea.Ann Soc geol Nord, Lille636281
  47. 47. Gurney AB (1961) Further advances in the taxonomy and distribution of the Grylloblattidae (Orthoptera). Proc Biol Soc Washington 74: 67–76.AB Gurney1961Further advances in the taxonomy and distribution of the Grylloblattidae (Orthoptera).Proc Biol Soc Washington746776
  48. 48. Asahina S (1959) Descriptions of two new Grylloblattidae from Japan. Kontyu, Tokyo 27: 249–252.S. Asahina1959Descriptions of two new Grylloblattidae from Japan.Kontyu, Tokyo27249252
  49. 49. Namkung J (1974) A new species of cave dwelling Grylloblattoidea (Grylloblattidae) from Korea. Korean Journal of Entomology 4: 1–7.J. Namkung1974A new species of cave dwelling Grylloblattoidea (Grylloblattidae) from Korea.Korean Journal of Entomology417
  50. 50. Caudell AL, King JL (1924) A new genus and species of the notopterous family Grylloblattidae from Japan. Proc Entomol Soc Wash 26: 53–60.AL CaudellJL King1924A new genus and species of the notopterous family Grylloblattidae from Japan.Proc Entomol Soc Wash265360
  51. 51. Kim BW, Lee W (2007) A new species of the Genus Galloisiana (Grylloblattodea, grylloblattidae) from Korea. Zoological Science 24: 733–745.BW KimW. Lee2007A new species of the Genus Galloisiana (Grylloblattodea, grylloblattidae) from Korea.Zoological Science24733745
  52. 52. Asahina S (1961) A new Galloisiana from Hokkaido (Grylloblattoidea). Kontyu, Tokyo 29: 85–87.S. Asahina1961A new Galloisiana from Hokkaido (Grylloblattoidea).Kontyu, Tokyo298587
  53. 53. Caudell AL (1924) Note on Grylloblatta with description of a new species. J Wash Acad Sci 14: 369–371.AL Caudell1924Note on Grylloblatta with description of a new species.J Wash Acad Sci14369371
  54. 54. Walker EM (1914) A new species of Orthoptera, forming a new genus and family. Canad Entom London Can 46: (93–98).EM Walker1914A new species of Orthoptera, forming a new genus and family.Canad Entom London Can46(9398)
  55. 55. Gurney AB (1937) Synopsis of the Grylloblattidae with the description of a new species from Oregon (Orthoptera). Pan-Pacific Ent, San Francisco 13: 159–170.AB Gurney1937Synopsis of the Grylloblattidae with the description of a new species from Oregon (Orthoptera).Pan-Pacific Ent, San Francisco13159170
  56. 56. Bei-Bienko GY (1951) A new representative of orthopteroid insects of the group Grylloblattoidea (Orthoptera) in the fauna of the USSR. Ent Obozr, Moscow 31: 506–509.GY Bei-Bienko1951A new representative of orthopteroid insects of the group Grylloblattoidea (Orthoptera) in the fauna of the USSR.Ent Obozr, Moscow31506509
  57. 57. Namkung J (1974) A new species of Galloisiana (Grylloblattidae) from Kosudong-gul Cave in Korea. Korean Journal of Entomology 4: 91–95.J. Namkung1974A new species of Galloisiana (Grylloblattidae) from Kosudong-gul Cave in Korea.Korean Journal of Entomology49195
  58. 58. Rohlf FJ (2006) tps-UTIL, File Utility Program, Version 1.38 [Software and Manual]. New-York: Department of Ecology and Evolution, State University of New York at Stony Brook. FJ Rohlf2006tps-UTIL, File Utility Program, Version 1.38 [Software and Manual].New-YorkDepartment of Ecology and Evolution, State University of New York at Stony Brook
  59. 59. Rohlf FJ (2006) tps-DIG, Digitize Landmarks and Outlines, Version 2.05. [Software and Manual]. New-York: Department of Ecology and Evolution. State University of New York at Stony Brook. FJ Rohlf2006tps-DIG, Digitize Landmarks and Outlines, Version 2.05. [Software and Manual].New-YorkDepartment of Ecology and Evolution. State University of New York at Stony Brook
  60. 60. Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press. FL Bookstein1991Morphometric Tools for Landmark Data: Geometry and Biology.CambridgeCambridge University Press
  61. 61. Rohlf FJ (2003) tps-SMALL. Version 1.20 [software and manual]. New York: Department of Ecology and Evolution, State University of New York at Stony Brook. FJ Rohlf2003tps-SMALL. Version 1.20 [software and manual].New YorkDepartment of Ecology and Evolution, State University of New York at Stony Brook
  62. 62. Rohlf FJ (2004) tps-SUPER. Version 1.14 [software and manual]. New York: Department of Ecology and Evolution, State University of New York at Stony Brook. FJ Rohlf2004tps-SUPER. Version 1.14 [software and manual].New YorkDepartment of Ecology and Evolution, State University of New York at Stony Brook
  63. 63. Rohlf FJ (2006) tps-RELW, Relative Warps Analysis, Version 1.44 [Software and Manual]. New York: Department of Ecology and Evolution. State University of New York at Stony Brook. FJ Rohlf2006tps-RELW, Relative Warps Analysis, Version 1.44 [Software and Manual].New YorkDepartment of Ecology and Evolution. State University of New York at Stony Brook
  64. 64. Rohlf FJ (2004) tps-SPLIN. Thin-plate spline, Version 1.20 [software and manual]. New York: Department of Ecology and Evolution, State University of New York at Stony Brook. FJ Rohlf2004tps-SPLIN. Thin-plate spline, Version 1.20 [software and manual].New YorkDepartment of Ecology and Evolution, State University of New York at Stony Brook
  65. 65. Rohlf FJ (2007) NTSYS-pc Numerical Taxonomy and Multivariate Analysis System, Version 2.20 for Windows [Software and Manual]. New York: Exeter Software. FJ Rohlf2007NTSYS-pc Numerical Taxonomy and Multivariate Analysis System, Version 2.20 for Windows [Software and Manual].New YorkExeter Software
  66. 66. Chapman RE (1990) Conventional Procrustes approaches. In: Rohlf FJ, Bookstein FL, editors. Proceedings ofthe Michigan Morphometrics Workshop. University of Michigan: Museum of Zoology special publication no. 2. Ann Arbor. pp. 251–267.RE Chapman1990Conventional Procrustes approaches.FJ RohlfFL BooksteinProceedings ofthe Michigan Morphometrics Workshop.University of MichiganMuseum of Zoology special publication no. 2. Ann Arbor251267
  67. 67. Goodall CR (1991) Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society 53: 285–339.CR Goodall1991Procrustes methods in the statistical analysis of shape.Journal of the Royal Statistical Society53285339
  68. 68. Goodall CR, Bose A (1987) Procrustes techniques for the analysis of shape and shape change. In: Heiberger R, editor. Computer science and statistics: proceedings of the 19th symposium on the interface. Alexandria, Virginia: American Statistical Association. pp. 86–92.CR GoodallA. Bose1987Procrustes techniques for the analysis of shape and shape change.R. HeibergerComputer science and statistics: proceedings of the 19th symposium on the interfaceAlexandria, VirginiaAmerican Statistical Association8692
  69. 69. Marcus LF, Bello E, Garcia-Valdecasas A (1993) Contrihutions to Morphometrics. Madrid: Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientificas, CSIC. LF MarcusE. BelloA. Garcia-Valdecasas1993Contrihutions to Morphometrics.MadridMuseo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientificas, CSIC
  70. 70. Rohlf FJ (1990) The analysis of shape variation using ordinations of fitted functions. In: Sorensen JT, editor. Ordinations in the study of morphology, evolution and systeinntics of insects: applications and quantitative genetic rationales. Amsterdam: Elsevier. FJ Rohlf1990The analysis of shape variation using ordinations of fitted functions.JT SorensenOrdinations in the study of morphology, evolution and systeinntics of insects: applications and quantitative genetic rationalesAmsterdamElsevier
  71. 71. Stockwell DRB, Peters D (1999) The GARP Modeling System: problems and solutions to automated spatial prediction. International Journal of Geographical Information Science 13: 143–158.DRB StockwellD. Peters1999The GARP Modeling System: problems and solutions to automated spatial prediction.International Journal of Geographical Information Science13143158
  72. 72. Levine RS, Yorita KL, Walsh MC, Reynolds MG (2009) A method for statistically comparing spatial distribution maps. International Journal of Health Geographics 8: 1–7.RS LevineKL YoritaMC WalshMG Reynolds2009A method for statistically comparing spatial distribution maps.International Journal of Health Geographics817
  73. 73. Oberhauser K, Peterson AT (2003) Modeling current and future potential wintering distributions of eastern North American monarch butterflies. Proceedings of the National Academy of Sciences of the United States of America 100: 14063–14068.K. OberhauserAT Peterson2003Modeling current and future potential wintering distributions of eastern North American monarch butterflies.Proceedings of the National Academy of Sciences of the United States of America1001406314068