Biodiversity, ecology, and behavior of the recently discovered insect order Mantophasmatodea
- 5.7k Downloads
The spectacular discovery of the new insect order Mantophasmatodea in 2002 was immediately followed by detailed studies on morphology and scattered information on different aspects of its behavior and general biology. A distinct feature of these predatory insects is the development of large arolia, which are typically held upright; hence, their common name is heelwalkers. The first mantophasmatodean species were described based on two museum specimens originally collected in Tanzania and Namibia. To date, these insects have been observed at surprising levels of diversity and abundance in Namibia and South Africa. For our studies on the phylogenetic relationships within Mantophasmatodea, we collected and analyzed numerous populations that belong to all known mantophasmatodean lineages, including East African populations. These collections not only provided a comprehensive biogeographical overview but also facilitated a comparative analysis of behavior, which was mainly analyzed under laboratory conditions. Here, we review and discuss the published data, as well as provide additional information on Mantophasmatodea distribution, evolutionary lineages, morphology, and biology, with a specific focus on reproductive biology.
KeywordsBehavior Biodiversity Evolutionary lineages Life history Mantophasmatodea Polyneoptera
General remarks and intraordinal relationships
Mantophasmatodeans superficially resemble mantises and stick insects. Different common names are used in the literature, including gladiator [37,38], rock crawler , and heelwalker (e.g., [25,30,40,41]). Because `heelwalker’ reflects the typical Mantophasmatodea phenotype, we prefer this designation. Both sexes of all known species, including fossil species [38,39,42] are apterous, which yields a nymph-like appearance. This appearance might be one reason that the Mantophasmatodea specimens were not recognized as members of a new insect order for a long time. Mantophasmatodean fossils were discovered in Baltic amber [38,39,43] which indicates a wide distribution in the past. Jurassic fossil findings (165 mya) in China confirm this hypothesis . Currently, Mantophasmatodea have a relict global distribution; most of the 18 described species are concentrated in western Southern Africa areas, except for Tanzaniophasma subsolanum (Tanzaniophasmatidae) in East Africa [1,4,5,30,44,45].
The extant Mantophasmatodea species have been provisionally grouped into three families: Tanzaniophasmatidae (which comprise only the described Tanzanian species of Tanzaniophasma), Austrophasmatidae (9 described species from African genera Namaquaphasma, Karoophasma, Hemilobophasma, Lobatophasma, Austrophasma, Viridiphasma), and the Namibian genus Striatophasma, Mantophasmatidae (8 described species from Namibian genera Tyrannophasma, Praedatophasma, Mantophasma, Sclerophasma, Pachyphasma). Another family-level group has been proposed for accommodating Praedatophasma and Tyrannophasma . In particular, the species identity within the Mantophasmatidae and the placement of Striatophasma in Mantophasmatidae or Austrophasmatidae must be clarified in future studies. A recent phylogenetic analysis of peptide hormone sequences suggests at least eight distinct lineages in Mantophasmatodea, including Tyrannophasma, Praedatophasma, Pachyphasma, Mantophasma (incl. Sclerophasma), Tanzaniophasma, Striatophasma, Austrophasmatidae sensu , and an undescribed taxon from the Richtersveld (see ). A second undescribed taxon from the Richtersveld (Wipfler & Predel; in prep.) may link Striatophasma from Namibia and the South African Austrophasmatidae. The monotypic Tyrannophasma, Praedatophasma, and Pachyphasma, as well as the two undescribed taxa from the Richtersveld, are relict taxa with a limited distribution range. In contrast, Mantophasma, Striatophasma, the South African Austrophasmatidae sensu , and most likely the poorly known Tanzaniophasma clade are currently successful and widespread taxa. Although a number of Mantophasma species have been described [1,4,46], recent analyses of numerous populations of the genus Mantophasma did not reveal conclusive lineage sorting within this taxon . Even the relationship between the Mantophasma lineage and Sclerophasma paresisense is poorly resolved  and requires further analyses to resolve the taxonomical status of this clade. The relationships within the family Austrophasmatidae, which was originally proposed to encompass taxa from the Western and Northern South African Cape Provinces, are well-supported at the genus and species levels. Ambiguities exist on an intrafamilial level for analyses of mitochondrial DNA sequences  and peptide hormone sequences . However, these analyses clearly indicate that the family Austrophasmatidae derived from Namibian Mantophasmatodea species. Species from this family may have evolved in a rapidly speciating lineage, which produced a monophyletic group of mostly allopatric species .
Distribution patterns and habitats
The spatial patterns of Mantophasmatodea in Southern Africa have been influenced by range fragmentation on a large scale (Namibian versus South African species) and range-edge speciation on a smaller scale. The latter form of speciation was likely driven by geological uplift during the Miocene to Pliocene , serial climatic oscillations during the Pleistocene , and alternating dry and wet climatic fluctuations. Thus, Mantophasmatodea speciation in Southern Africa was most likely allopatric through vicariance, which has been assumed for other insects  and arthropods (Diplopoda; ) in the region. Remarkably, the core regions of their recent distribution, such as the Brandberg in Namibia and Succulent Karoo-Fynbos biomes [55-57] typically show exceptional levels of biodiversity and endemism. In these regions, Mantophasmatodea are part of a very unique insect fauna [58,59]. Notably in the context of Mantophasmatodea distribution, no additional mantophasmatodean taxa have been identified within the large Mantophasma distributional range, whereas two distinct monotypic genera are sympatric in different ecological niches on the Brandberg Massif immediately outside the Mantophasma range. Both the genera Tyrannophasma and Pachyphasma appear restricted to the Brandberg Massif and have not been observed in other areas. The Brandberg Massif (the highest mountain in Namibia) has volcanic origins and is isolated from the longitudinal Namibian escarpment (Mantophasma habitat); this isolation has generally ensured that it is a significant relict habitat for numerous endemic organisms (see [53,55]). On the Brandberg Massif plateau, Pachyphasma brandbergense was found in the same biotope as Tyrannophasma gladiator. The large and impressive-looking grey-brown T. gladiator is mainly found in grass tussocks (see also ); however, under dry conditions, nymphs have also been found in dense bushes (altitude 1400-2400 m). The much smaller and greenish P. brandbergense is the only mantophasmatodean taxon primarily collected from flowering composite bushes; the ecological relevance of this finding is unknown. The Brandberg Plateau vegetation is characterized by plant species confined to the upper regions of mountains (higher than 1500 m); Asteraceae is the most speciose family . The different Mantophasma populations (including Sclerophasma paresisense) inhabit well-vegetated mountains in central Namibia up to the Otavi Mountains in the northeast; they also live in mountainous mopane savanna (Kaokoveld) in the northwest. Throughout most of their range, these insects are common in grasses, shrubs, and even trees given sufficient rainfall (see ). The density of individuals in a population can be surprisingly high, which is somewhat unexpected for an insect group that has been overlooked for such a long time period. The genus Striatophasma, which was mainly collected south/southeast of the Mantophasma distribution, typically inhabits dry regions with scattered vegetation, and specimens have often been collected from dwarf bushes. In the Gamsberg/Hakos Mountains, Mantophasma and Striatophasma are sympatric. Austrophasmatidae, which live in the winter-rain South African region, were typically found in habitats with sparse to scattered vegetation. Eberhard et al.,  reported a preference of Viridiphasma clanwilliamense to a small tree (Euclea recemosa), but for most species, we did not observe a preference for hiding on a specific plant species; clearly, Austrophasmatidae select dense bushes or grass tussocks, which provide camouflage and a sufficient prey spectrum. The Kraalbos Galenia africana, a bush that is poisonous to sheep and is common in overgrazed or otherwise disturbed Western/ Northern Cape areas, appears to be particularly attractive to mantophasmatodeans. The occurrence of heelwalkers in strongly disturbed areas suggests that these insects are less sensitive to environmental damage as long as prey is available. At least for the Austrophasma and Hemilobophasma populations, we found that nymphs prefer bushes, whereas adults were typically collected from large grass tussocks. Copulating heelwalkers have regularly been observed in these grasses. Most Austrophasmatidae clades were collected from low altitudes to mountainous locations up to 2000 m, which indicates that different altitudes with changing vegetation types are not effective dispersal barriers for heelwalkers.
Occasionally, Mantophasmatodea actively drop in the vegetation. In most cases, they land upright on their legs ("cat-like") on the ground or in the correct direction in small branches of shrubs and grasses. Experiments using high-speed cameras suggest that heelwalkers actively influence the landing position due to their highly flexible body axis (see Additional file 6: Video 2A and Additional file 7: Video 2B). Similarly sized unwinged mantises and phasmids were unable to behave similarly; however, the mantises attempted to perform a `loop’, but required much more distance between the start and end points (Predel, unpublished). In the field and in captivity, healthy heelwalkers are reluctant to immediately walk away after dropping. When these insects did not land on their legs but on their backs, they changed their positions with a sudden movement immediately after landing and stopped again (see Additional file 8: Videos 3A and Additional file 9: Video 3B). Due to this behavior, which may be maintained for 30 sec or even longer, it is sometimes difficult to detect heelwalkers in detritus after beating a bush; many arthropods, such as ants, beetles, cockroaches, and spiders, run around actively under these circumstances. In nature, this strategy likely prevents detection by insect-hunting mammals or birds.
The Mantophasmatodea antennae are long, filiform, and have a flagellum well separated in basi- and distiflagellum; unique feature among insects [4,17,18]. While walking or hiding, these insects continuously wave their antennae in a manner similar to that of cockroaches (i.e., both antennae alternatively move up and down) (see Additional file 11: Video 5). During these motions, the flagellomeres are typically bent downwards. Antenna-flickering has been observed upon contact with a sexual partner and prey. This behavior indicates intensive chemical signal use. Potential glandular structures have been identified in two of the distal flagellomeres [4,18,36]. Occasionally, males walk with their abdomens upwards, similarly to scorpions (e.g., when approaching a sexual partner).
A diurnal habit has been observed in Mantophasma specimens (see also ). Occasionally, we found these insects sitting in the upper parts of grasses and outer shrub branches during the hottest portion of the day (11 a.m. - 5 p.m.); however, the Mantophasma specimens were more abundant in these locations after nightfall. In the laboratory, Mantophasma specimens showed greater activity during the day compared with Austrophasmatidae species, including foraging and sexual behaviors (see  and below). For all species, mating and drumming behaviors were predominantly observed at night in the laboratory, including dusk and dawn.
Life cycle, growth, and life history
Mantises and cockroaches, which were often collected at the same location as the heelwalkers, laid eggs/egg cases even under simplified laboratory conditions (e.g., in plastic boxes without a soil cover), but for Mantophasmatodea, oviposition was not observed under these simplified conditions. This reluctance to oviposit was evident. However, Mantophasmatodea specimens readily copulated in the laboratory if provided the opportunity (see below). Pregnant Mantophasmatodea females laid eggs almost immediately if sufficient soil was provided, and we obtained more than 30 pods with fertile eggs from 20 T. gladiator females after copulation in the laboratory. Uchifune  obtained multiple egg pods from Karoophasma biedouwense (Austrophasmatidae); individual females laid up to four egg pods over a short period, i.e., a few days, and 50 - 100 eggs total during their adulthood . In this species, oviposition was observed in September and typically occurred in the morning when the temperature was low and the humidity was high . Under artificial laboratory conditions, Mantophasmatodea breeding was unsuccessful in most cases. We tested different dormancy scenarios using T. gladiator egg pods (G. Köhler, unpubl. data). Neither a dry and warm period over several months nor dry conditions followed by a cooling (4°C) period over several months initiated hatching. In all scenarios, a water supply was used to terminate dormancy, which simulated the rainy season and appeared to initiate hatching in the field. The egg fertilization rates varied from 48-95% in our experiments, and the embryos reached the anatrepsis phase. From these observations, we assumed a diapause. However, successful rearing in Sclerophasma paresisense and Praedatophasma maraisi (in fact, Tyrannophasma gladiator, see locality) was reported by , who used increased moisture and rising temperatures following a cold period.
T. gladiator nymphs that hatched reached adulthood after 3.5-4 months ; the adults survived at least two months in our laboratory. First instar Striatophasma naukluftense nymphs were collected and reared; the oldest adult died at 136 days (4.5 months). For the winter-active Austrophasmatidae species, the developmental period appears to be shorter, but the unpredictable weather conditions strongly influence their life spans. Drilling and Klass  indicated approximately 55 days (excluding the first instar phase) in L. redelinghuysense; our laboratory experiments (21-23°C) have shown that third instar Austrophasmatidae larvae (localities: S04, S15, S18, S26, S32; see Figure 1) reached adulthood within less than a month. In the laboratory, we observed a shorter life span in males compared with fertile females. Typically, Mantophasmatodea molted during the night and ingested their exuviae; therefore, counting the number of instar stages for these insects was difficult. In only a few cases, the fragile Mantophasmatodea exuviae were found hanging on the top or wall of the rearing container. Hockman et al.,  used antenna development (i.e., the increasing number of basiflagellum annuli) as the criterion for assessing instars and reported 5 nymph instars in L. redelinghuysense. The first instar nymphs possessed four annuli in the basiflagellum and seven hairy annuli in the distiflagellum. For each instar, two additional annuli were derived from the most basal annulus (meriston); therefore, the number of annuli in the adult L. redelinghuysense basiflagellum was 14. Because consistent antennal development was also observed for other mantophasmatodean taxa , the assumed 8-10 instars in T. gladiator is likely an overestimate.
There is no available information on mortality factors, including predation and parasitism, in the field. Camouflage appears to be important for these small predators, which are vulnerable to attack by birds, lizards, and predaceous insects that are present in the same microhabitat. Escape behavior, i.e., jumping away from a bush or grass tussock, was rarely observed. However, heelwalkers can jump for a short distance (see above). In particular, the summer-active Mantophasmatidae species regularly co-occur with mantises, mainly the genus Miomantis, which were collected using the same collection method. However, on the microhabitat scale, we found that a high heelwalker density was primarily linked to relatively low mantis abundance, even if mantises were more frequent elsewhere in the immediate neighborhood. Although we did not perform quantitative studies, this observation indicates extermination or possible avoidance of intra-guild predation between these insects.
Prey and feeding behavior
The literature includes only a few observations on how Mantophasmatodea find and handle their prey in the field [5,33]. A hide and wait strategy (in combination with slow stalking) is very likely and is concordant with the nocturnal activity of most species. In the laboratory, Mantophasmatodea nymphs and adult Austrophasmatidae were mainly fed different Drosophila species. Larger Mantophasmatidae and Tanzaniophasmatidae specimens were fed house and flesh flies, as well as different size Gryllus nymphs. Additional prey that were successfully provided in captivity include mosquitos, plant hoppers, booklice, moths (including larvae), termites, bush crickets, antlion lacewings, may flies, and small earthworms. Adis et al.,  also fed the insects dead mealworms (Tenebrio). In captivity, crickets were refused as prey by many Austrophasmatidae, but not Mantophasmatidae. For T. gladiator, suggested that cockroaches and moths were prey in the Brandberg area. In a single experiment, we placed two late instar Mantophasma spec. nymphs (N21, Erongo Mountains) with a mantis nymph (Miomantis sp.) of the same size and from the same locality in a plastic box (100x100x40). The mantis was the prey. Cannibalism among nymphs and adults (also between females) has been regularly observed in captivity (see also [19,33]). In certain instances, females have successfully attacked males after mating or without mating contacts in both small pots and larger cages.
When hunting Drosophila, Mantophasmatodea waited or sometimes walked a few millimeters to the flies. With a sudden motion, they moved forward and caught the prey with their mandibles (see Additional file 12: Videos 6A, Additional file 13: Videos 6B, Additional file 14: Videos 6C and Additional file 15: Videos 6D). Thus, small prey, such as fruit flies, can be caught without using the legs. Occasionally, we observed that Mantophasmatodea used the tarsi of a foreleg to catch a fruit fly and bring it to their mouthparts. The insects embrace (face-to-face) larger prey using their spiny forelegs and, often, their mid-legs (Figure 12; see also  for T. gladiator); the prey is immediately consumed. In a single case, we removed an A. gansbaaiense female's victim (a male of the same species) immediately after the first attack to the neck and found the ventral nerve cord severed. This behavior was not consistent, but  also reported initial neck bites with larger flies. Meal consumption requires a short time and does not necessarily exclude body appendages (see Additional file 16: Video 7). Adis et al.,  observed that Mantophasmatodea occasionally bite their prey's head off (e.g., Musca). We occasionally observed this behavior when we fed the Austrophasmatidae specimens using Drosophila. In few cases, the heelwalkers only used the heads for eating/feeding and neglected the remaining bodies from up to ten fruit flies.
All Mantophasmatodea species exhibit strong sexual dimorphism in the external genital structure , and males are, on average, smaller and more slender compared with females. The male reproductive system includes testes, a deferent duct, seminal vesicles, and accessory glands  and is proliferated in the abdomen. Depending on the species, pregnant females have 8-15 eggs per ovary, which are surrounded by a thin cover of tissue and typically oviposited in a single pod (but see also , which includes a description of pods with 10-12 eggs). The female's weight increases remarkably during egg maturation (wet weight in g) (e.g., Mantophasma kudubergense (0.14-0.22)  and Austrophasmatidae sp. n. (0.063-0.152; S18, Vanrhynsdorp)). For Karoophasma biedouwense and Hemilobophasma montaguense, 50-100 eggs total per lifetime have been reported . Under laboratory conditions, Mantophasmatodea mate readily; therefore, we observed different aspects of their sexual behavior, such as sexual communication, partner finding, courtship, and copulation, in several species and compared these data with previous descriptions in .
Temporal characteristics of vibrational signals for three males of Striatophasma naukluftense and six males from the Sclerophasma/Mantophasma clade
Pulse repetition time (ms)/CV(%)
Pulse train duration (ms)/CV(%)
Number of pulses per pulse train/CV(%)
19.46 ± 2.16/11%
5365.4 ± 409.6/7%
57.4 ± 5.38/9%
n = 70
n = 7
n = 7
19.2 ± 2.41/125%
4395.7 ± 221.7/5%
50.2 ± 3.3/7%
n = 40
n = 4
n = 4
35.6 ± 2.43/6%
2537.5 ± 323.3/13%
28.8 ± 2.93/10%
n = 60
n = 6
n = 6
24.75 ± 9.39/38%
4099.53 ± 1437.02/35%
45.46 ± 14.8/32.5%
Sclerophasma (N14 )
21.03 ± 3.77/17%
1300 ± 122.5/9%
14.89 ± 1.17/7%
n = 90
n = 9
n = 9
1939.2 ± 266.7/13%
20.7 ± 2.6/12.5%
n = 11
n = 11
24.05 ± 7.5/31%
2059.5 ± 277.8/13%
24 ± 3.0/12.5%
n = 60
n = 6
n = 6
39.03 ± 3.65/9%
1689 ± 83.3/4%
19 ± 0.9/5%
n = 60
n = 6
n = 6
74.08 ± 4.7/6%
1628.6 ± 111.3/7%
12.1 ± 0.9/7%
n = 70
n = 7
n = 7
78.5 ± 2.12/2%
3205 ± 15/0.4%
13 ± 0
n = 20
n = 2
n = 2
Average (N9,N10, N14, N15, N20, N31)
47.34 ± 27.33/57%
1970.22 ± 660.1/33.5%
17.33 ± 4.79/28%
Based on the studies conducted using Mantophasmatodea, the following questions remain. 1) It is not clear whether repetitive pulse trains constitute a single call, as proposed in  and . Alternatively, repetitive pulse trains could compose consecutive calls. 2) Certain parameters studied ([20,22], and this study) are inter-correlated. The number of pulses per pulse train might depend on the pulse train duration. As another example, the pulse train repetition time is the sum of the inter-pulse train interval and pulse train duration. It is difficult to determine which parameter is most important for females to discriminate among male calls from different species because of these strong inter-correlations. 3) In insect communication, call performance also depends on the specimen condition and ambient temperature (Boumans, pers. communication). Stonefly studies have demonstrated that temperature has an important impact on the frequency but not the number of pulses . However, physical constitution affects the number of pulses per pulse train (Boumans, in prep.). After submitting the manuscript, the authors collected in the Richterveld (South Africa) males of two different species (Namaquaphasma ookiepense; Austrophasmatidae gen. n. sp. n. S01) in the same bush and placed them in separate plastic boxes in the field. The N. ookiepense males produced short pulse trains of about a second (see also ). In striking contrast to these short signals were the pulse trains of the second species which lasted 4-6 sec.
Courtship and mating behavior
The males generally appear to be at risk of attack by the female, as indicated by their rapid mounting. Zompro et al.,  reported that Mantophasma kudubergense males retreated by jumping away if the females appeared agitated after mounting. In Austrophasmatidae sp. n. (S18, Vanrhynsdorp), we observed that a female defended herself against a mounted male by both leg kicking and biting (see Additional file 21: Video 11). The elements of sexual behavior, such as drumming, antennae flickering for chemical cues, and antennae contact, can be interpreted as species recognition behavior  or courtship behavior to reduce female attacks; the elements might be involved in both behaviors. As described for Mantophasma kudubergense by , we observed intense pumping movements at the tip of the abdomen for Austrophasmatidae males; thereafter, spherical eversion of the phallic lobes was observed. Eberhard and Picker  considered this action an indication of direct sperm transfer from males to females. This behavior was observed during the first 1-2 min of copulation and at least three times during the first hour of copulation. In our observations we did not identify similar time patterns for pumping in Austrophasmatidae. Pumping occurred at different periods during prolonged copulation. In Austrophasmatidae sp. n. (S18, Vanrhynsdorp) we observed a semi-liquid, gelatinous substance between the external genital structures of males and females during the last phase of copulation (Figure 21C). We assume that this substance was released by the male and that it was a type of mating plug, not a spermatophore.
Copulation frequency and time
Copulation times for several Mantophasmatodea species in the laboratory
Observed copulation times in hours
Number of observed copulations
Karoophasma botterkloofense (S16)
68.5 (S.E. ±4.56)
Austrophasmatidae sp. n. (S18)
Hemilobophasma montaguense (S26)
Austrophasma gansbaaiense (S32)
24 R, 24 R, 64
Mantophasma spec. (N21)
Hemilobophasma sp.n. 1 x H. cf. montaguense2
Mantophasmatodea in general***
Up to 96
Analysis of variance to determine the effects of 1) initial body weight (in g), 2) treatment duration (in hours), and 3) treatments (starvation/desiccating vs. mating) on the percentage of body weight lost in Austrophasmatidae sp. n . males (S18, Vanrhynsdorp)
Source of Variation
Sum of square
Initial body weight
Duration of treatment
Only a few years after the first Mantophasmatodea was described, the literature includes an impressive scientific knowledge on its diversity and biology. In contrast to the well-known distribution range in Southern Africa, however, the Mantophasmatodea range and diversity in East Africa have not been explored as extensively. In addition, the assignments of the known genera to different erected families must be clarified in a thorough revision. Future novel discoveries regarding general aspects of their biology will largely depend on successful breeding in captivity. One particular aspect of their biology is their tendency toward broad species distribution with many local populations. This phenomenon is, in part, due to low dispersal abilities (winglessness, low mobility, and low chance of dispersal for all stages, including eggs). Using mass fingerprints of peptide hormones to map the different populations, it appears possible that intraspecific migration/replacement/hybridization can be followed over a long time period, which is another unique possibility provided by these fascinating insects.
Sampling and export permissions
The insects were captured and exported with permission from the Western and Northern Cape Nature Conservation Boards (no. 2297/2003, 0697/2004, 0554/2004), the Ministry of Environment and Tourism of Namibia (research/collecting permits 891/2005, 1041/2006), and Malawi (Government Document: Department of Forestry Specimens Collection Permit 21/01/2011/no.1).
SR and RP conducted field samplings and observations. Rearing, laboratory observations including video and vibrational signal tapping were performed by RP and partly by SR. The mating cost experiment was carried out and analyzed by SR. JM analyzed the vibrational signals. Data interpretation and preparation of the manuscript was done by SR, RP and JM. The final manuscript was written by RP and SR. All authors read, commented on and approved the final manuscript.
We wish to thank the following individuals for support during the numerous field trips and for their help in the laboratory work with Mantophasmatodea: Susanne Neupert (Köln), Wolf Hütteroth (Konstanz), Mike Picker (Cape Town), Adrian Scheidt (Groningen), Martin Scheidt (Vienna), Moritz and Marie Predel (Jena), Rene Köhler (Köln), Alexander König (Göttingen), Udo Neugebauer (Saalburg), Thomas Schmalenberg (Leipzig), Holger Vollbrecht (Windhoek), Martin Fischer (Jena) and Benson Muramba (Windhoek). We thank Louis Boumans (Oslo) for useful comments on our vibrational studies. We also acknowledge comments from Mike Picker on a former version of the manuscript and Dirk U. Bellstedt (Stellenbosch) for plant determination. This study was supported by travel grants from the Boehringer Ingelheim Stiftung, the British Ecological Society, and the Orthoperists' Society of America. Remains of orbatids in intestines were confirmed by Torstein Solhøy, Roy A. Norton, and Arne Fjellberg (Bergen; in litt.).
Additional file 5: Video 1D- Female is jumping over a male which tries to mount and copulate afterwards; Karoophasma botterkloofense.(MOV 2 MB)
Additional file 10: Video 4 - Grooming behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).
Additional file 11: Video 5 - Antenna-flickering, Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 319 KB)
Additional file 12: Video 6A - Foraging behavior; Karoophasma botterkloofense.(MOV 430 KB)
Additional file 13: Video 6B - Foraging behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 1 MB)
Additional file 14: Video 6C - Foraging behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 1 MB)
Additional file 15: Video 6D - Foraging behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 598 KB)
Additional file 16: Video 7 - Foraging behavior (details); Pachyphasma brandbergense.(MOV 11 MB)
Additional file 17: Video 8a, Drumming behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 2 MB)
Additional file 18: Video 8B - Drumming behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 346 KB)
Additional file 19: Video 9B - Mating behavior; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 7 MB)
Additional file 20: Video 10 - Female foraging whilst in copula; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 965 KB)
Additional file 21: Video 11 - Female defense against male; Austrophasmatidae sp. nov. (S18, Vanrhynsdorp).(MOV 2 MB)
- 4.Klass K-D, Picker MD, Damgaard J, van Noort S, Tojo K: The taxonomy, genitalic morphology, and phylogentic relationships of southern African Mantophasmatodea (Insecta). Entomologische Abhandlungen. 2003, 61: 3-67.Google Scholar
- 5.Zompro O, Adis J, Bragg PE, Naskrecki P, Meakin K, Wittneben M, Saxe V: A new genus and species of Mantophasmatidae. Insecta: Mantophasmatodea) from Brandberg Massif, Namibia, with notes on behaviour. Cimbebasia. 2003, 19: 13-24.Google Scholar
- 6.Zompro O: Inter- and intra-ordinal relationships of the Matophasmatodea, with comments on the phylogeny of polyneopteran orders (Insecta: Polyneoptera). Mitteilungen des Geologisch. 2005, 89: 85-114.Google Scholar
- 8.Tsutsumi T, Machida R, Tojo K, Uchifune T, Klass KD, Picker MD: Transmission electron microscopic observations of the egg membranes of a South African heel-walker Karoophasma biedouwensis (Insecta: Mantophasmatodea). Proc Arthropodan Embryol Soc Jpn. 2004, 39: 23-29.Google Scholar
- 9.Uchifune T, Machida R, Tsutsumi T, Tojo K: Chorion of a South African heel-walker, Karoophasma biedouwensis Klass et al. SEM observations (Insecta: Mantophasmatodea). Proc Arthropodan Embryol Soc Jpn. 2006, 41: 29-35.Google Scholar
- 12.Pass G, Gereben-Krenn B-A, Merl M, Plant J, Szucsich NU, gel M: Phylogenetic relationships of the orders of Hexapoda: contributions from the circulatory organs for a morphological data matrix. Arthropod Syst Phylogeny. 2006, 64: 165-203.Google Scholar
- 13.Beutel RG, Gorb SN: A revised interpretation of the evolution of attachment structures in Hexapoda with special emphasis on Mantophasmatodea. Arthropod Syst Phylogeny. 2006, 64: 3-25.Google Scholar
- 16.Buder G, Klass K-D: The morphology of tarsal processes in Mantophasmatodea. Deutsche Entomologische Zeitschrift. 2013, 60: 5-23.Google Scholar
- 19.Tojo K, Machida R, Klass K-D, Picker MD: Biology of South African heel-walkers, with special reference to reproductive biology (Insecta: Mantophasmatodea). Proc Arthropodan Embryol Soc Jpn. 2004, 39: 15-21.Google Scholar
- 26.Machida R, Tojo K, Tsutsumi T, Uchifune T, Klass KD, Picker MD, Pretorius L: Embryonic development of heel-walkers: Reference to some preevolutionary stages (Insecta: Mantophasmatodea). Proc Arthropodan Embryol Soc Jpn. 2004, 39: 31-39.Google Scholar
- 27.Tsutsumi T, Tojo K, Uchifune T, Machida R: Ovarian structure and oogenesis of the South African heel-walker Karoophasma biedouwensis (Insecta: Mantophasmatodea). Proc Arthropodan Embryol Soc Jpn. 2005, 40: 15-22.Google Scholar
- 32.Kjer KM, Carle FL, Litman J, Ware J: A molecular phylogeny of Hexapoda. Arthropod Systematics & Phylogeny. 2006, 2006 (64): 35-44.Google Scholar
- 33.Adis J, Marais E, Moombolah-Goagoses E, Zompro O: Gladiatoren: Gespenstische Räuber. Spektrum Wissensch. 2003, 2003: 64-69.Google Scholar
- 34.Walker JA: Mantophasmatodea - a new order of insects. Bull Amateur Entomologists' Soc. 2003, 62: 72-78.Google Scholar
- 35.Zompro O: Mantophasmatodea - Gladiatoren im Insektenreich. Arthropoda. 2008, 16: 4-25.Google Scholar
- 36.Klass K-D: Mantophasmatodea, Die zuletzt entdeckte Insektenordnung. Nat Mus. 2009, 139: 218-227.Google Scholar
- 40.Machida R, Tojo K: Heel walkers, a new insect order Mantophasmatodea. (In Japanese). Kontyu to Shizen. 2003, 38: 26-31.Google Scholar
- 41.Picker M, Griffiths C, Weaving A: Field guide to insects of South Africa. 2004, Struik Publishers, Cape TownGoogle Scholar
- 43.Arillo A, Ortuno VM, Nel A: Description of an enigmatic insect from Baltic amber. Bulletin de la Société entomologique de France. 1997, 102: 11-14.Google Scholar
- 46.Zompro O, Adis J: Notes on Namibian Mantophasma Zombro, Klass Kristensen & Adis 2002, with descriptions of three new species (Insecta: Mantophasmatodea: Mantophasmatidae: Mantophasmatini). Russ Entomol J. 2006, 15: 21-24.Google Scholar
- 47.Mloza-Banda HR: Development and application of conservation agriculture in Malawi's smallholder subsistence and commercial farming systems. Proceedings of Workshop on Conservation Farming for Sustainable Agriculture: 20-24 October 2002. Edited by: Mloza-Banda HR, Kumwenda WF, Manda M, Bwalya M. 2003, Land Resources Conservation Department, Lilongwe, MalawiGoogle Scholar
- 48.Williams J: Adoption of conservation agriculture in Malawi. Master thesis. 2008, Nicholas School of Environment of Duke University, Durham, North CarolinaGoogle Scholar
- 49.Holm E: Notes on faunas bordering on the Namib Desert. Namib Ecology: 25 years of Namib Research. Edited by: Seely MK. 1990, Transvaal Museum Monographs, Pretoria, 55-60.Google Scholar
- 51.Partridge TC: Evolution of landscapes. Vegetation of Southern Africa. Edited by: Cowling RM, Richardson DM, Pierce SM. 1997, Cambridge University Press Cambridge, Cambridge, 5-20.Google Scholar
- 52.Haughton SH: Geological history of Southern Africa. 1969, Cape Town, The Geological Society of South AfricaGoogle Scholar
- 54.Redman GT, Hamer ML: The distribution of southern African Harpagophoridae Attems, 1909 (Diplopoda: Spirostreptida). Afr Invertebr. 2003, 44: 213-226.Google Scholar
- 55.Kirk-Spriggs AH, Marais E: Dâures-biodiversity of the Brandberg Massif. Namibia Cimbebasia Memoir. 2000, 9: 1-389.Google Scholar
- 56.Cowling R: The ecology of Fynbos. Nutrition, fire and diversity. 1992, Oxford University Press, Cape TownGoogle Scholar
- 57.Lovegrove B: The living deserts of Southern Africa. 1993, Fernwood Press, VlaebergGoogle Scholar
- 59.African Biodiversity: Molecules, Organisms, Ecosystems. Proceedings of the 5th International Symposium on Tropical Biology, Museum Alexander Koenig, Bonn. 2005, Springer, New YorkGoogle Scholar
- 60.Craven P, Craven D: The flora of the Brandberg, Namibia. Cimbebasia Memoir. 2000, 9: 49-67.Google Scholar
- 62.Wipfler B: Mantophasmatodea. Insect Morphology and Phylogeny. Edited by: Beutel RG, Friedrich F, Ge S-Q, Yang X-K. 2014, De Gruyter, Berlin, 272-277.Google Scholar
- 64.Uchifune T: Collection and rearing of a South African heel-walker, Karoophasma biedouwensis Klass et al. (Insecta: Mantophasmatodea). Science Report of the Yokosuka City Museum. 2008, 55: 23-28.Google Scholar
- 65.Power JH: On the biology of Acanthoplus bechuanus Per (Orthoptera: Tettigoniidae). J Entomological Soc South Africa. 1958, 21: 376-381.Google Scholar
- 66.New TR: Insects as predators. 1991, New South Wales University Press, SydneyGoogle Scholar
- 69.Dixon AFG, Russel RJ: The effectiveness of Anthocoris nemorum and A. confusus (Hemiptera: Anthocoridae) as predators of the sycamore aphid, Drepanophisum platanoides. Entomologia Experimentales et Applicata. 1972, 13: 194-207.Google Scholar
- 71.Moran MD, Hurd LE: Relieving food limitations reduces survivorship of a generalist predator. Ecology. 1997, 78: 1266-1270.Google Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.