Proturans

Proturans belong to the Phylum Euarthropoda, Class Entognatha, and Class Protura. The Protura constitute a taxon of hexapods that were previously thought to be insects and now are considered as a class on their own. Proturans are cosmopolitan in distribution (except for both polar regions and snow zones of mountains) with more than 800 described species belonging to three distinct orders (Acerentomata, Eosentomata, and Sinentomata) and seven families (Acerentomidae, Antelientomidae Eosentomidae, Fujientomidae, Hesperentomidae, Protentomidae, and Sinentomidae). As of 2019, seventy-six genera are known worldwide, with nearly 300 species contained within the single cosmopolitan genus, Eosentomon. There are about twenty-six species in North America, though there is no exact number of species reported, to date, from Arkansas. However, four species of Eosentomon—including E. caddoense, E. maryae, E. megatibience, and E. quapawense—are known from Arkansas’s Ouachita Mountains. It has been suggested that only ten percent of all extant species have been described.

Evolutionarily speaking, there is convincing evidence that the Protura are basal to all other hexapods, although not all researchers consider them Hexapoda. As such, this renders the monophyly of Hexapoda uncertain. Unique among hexapods, proturans show anamorphic development, whereby body segments are added during molts.

Because they are so inconspicuous, it was not until the early twentieth century that proturans were first discovered. Two Italian entomologists, Filippo Silvestri (1873–1949) and Antonio Berlese (1863–1927), discovered the group independently. The initial species to be formerly described in 1907 was Acerentomon doderoi, by Silvestri, found among small invertebrates collected by the micro-coleopterologist Agostino Dodero (1864–1937) in Genoa, Italy.

Proturans are very small (less than 2 mm [0.78 in.] long) soil-dwelling invertebrates that have no eyes, cerci, wings, tentorium, or antennae. They lack pigmentation and are usually yellow, white, or pale brown. The sensory function of the antennae is satisfied by the forelegs (first of three pairs) of five-segmented legs, which are held up, pointing forward, and have many tarsal sensilla and sensory hairs. The conical head possesses two pseudoculi that have an unknown function. The body is cylindrical and elongated with a postanal telson (tail) at the end. The mouthparts are enclosed within the head capsule (entognathous) and consist of thin mandibles and maxillae. The first three abdominal segments possess limb-like appendages called “styli.” In the mature adult, the genitalia are internal, and the genital opening can be found between the eleventh segment and the telson. In both sexes, these genitalia are everted from a chamber.

In terms of respiration, members of Eosentomidae (Eosentomata) have a simple tracheal system and possess spiracles, whereas those in the Acerentomata lack these two structures and perform gas exchange by simple diffusion.

Proturans inhabit various habitats, including in leaf litter, lichens, mosses; beneath rocks; under the bark of trees; in animal burrows such as those of voles and the European mole (Talpa europea); and in moist soil and humus of temperate forests. They are generally restricted to the uppermost 10 cm (3.9 in.) of substrate but have been found under pasture soil as deep as 50 cm (20 in.). Here, they aid in decomposition by assisting in the breakdown of leaf litter and recycling organic nutrients. They, thus play a significant role in soil formation and composition, which is vital in soil restoration. Although they are sometimes considered rare to uncommon, they are probably often unnoticed because of their small size. However, densities of over 90,000 individuals per square meter have been counted from a forest in Germany.

Although the food items of proturans have not been well studied, they are thought to feed on decaying vegetable matter and fungi in nature. But, in culture, individuals have fed on mycorrhizal fungi, dead Acari (mites and chiggers), and mushroom powder. The presence of a styliform (distinctly sclerotized apex) mouthpart suggests they are fluid feeders, with evidence that some species remove fungal hyphal contents via peristaltic movements like a sucking pump.

Proturans are important prey items for small invertebrates, such as mites, pseudoscorpions, and spiders. When they are disturbed, proturans appear to raise the end of the abdomen in a defensive posture similar to that adopted by scorpions.

Reproductively, proturans that live near the soil surface generally have longer legs and one generation per year, while those with shorter legs live deeper and reproduce less seasonally. In addition, some migratory species move to deeper layers for the winter and shallower layers for the summer. It is unknown whether proturans transfer sperm by copulation, or indirectly, as in all other groups of apterygotan insects. However, the presence of a flagellated sperm in many species suggests indirect sperm transfer via spermatophores. Proturan eggs have been observed in only a few species, and embryogenesis (egg period) may occur within two months. After hatching, five developmental stages follow: (1) a prenymph that has only weakly developed mouthparts and nine abdominal segments; (2) nymph I that has fully developed mouthparts; (3) nymph II that has ten abdominal segments; (4) maturus junior that has 12 abdominal segments; and (5) the adult. Although the nymph has nine abdominal segments, the number increases through molting until the full adult complement of twelve is reached. Additional molts may occur, but they do not add any more body segments, and it is not known whether the adults continue to molt through their lives. One family, the Acerentomidae, somewhat differs in development stages by having an extra preimago stage, with partially developed genitalia, between the maturus junior and the adult.

Because proturans remain rarely collected and unknown from many large geographical areas of North America, little is known about the proturans of Arkansas. However, four species of Eosentomon—including E. caddoense, E. maryae, E. megatibience, and E. quapawense—are known from the Ouachita Mountains of the state.

For additional information:
Allen, Robert T. “Studies on the North American Protura 1. Catalogue and Atlas of the Protura of North America; Description of New Species; Key to the Species of Eosentomon.” Proceedings of the Academy of Natural Sciences of Philadelphia 156 (2007): 97–116.

Bernard, E. C. “New Species, Clarifications, and Changes in Status within Eosentomon Berlese (Hexapoda: Protura: Eosentomidae) from the United States.” Proceedings of the Biological Society of Washington 103 (1990): 861–890.

———. “Two New Species of Protura (Insecta) from North America.” Proceedings of the Biological Society of Washington 98 (1985): 72–80.

Bonet, F., and Søren L. Tuxen. “Reexamination of Species of Protura Described by H. E. Ewing.” Proceedings of the United States National Museum 112 (1960): 265–305.

Ewing, H. E. “The Protura of North America.” Annals of the Entomological Society of America 33 (1940): 495–551.

Galli, Loris, Julia Shrubovych, Yun Bu, and Matteo Zinni. “Genera of the Protura of the World: Diagnosis, Distribution, and Key.” Zookeys 772 (2018): 1–45.

Kraus, J., and W. Funke. “Extraordinary High Density of Protura in a Windfall Area of Young Spruce Plants.” Pedobiologia 43: 44–46.

Lagerlöf, J., and O. Andrén. “Abundance and Activity of Collembola, Protura and Diplura (Insecta, Apterygota) in Four Cropping Systems.” Pedobiologia 35 (1991): 337–350.

Nosek, Josef. The European Protura. Their Taxonomy, Ecology and Distribution with Keys for Determination. Genève (Switzerland): Muséum d`Histoire Naturelle, 1973.

Pass, Günther, and Nikolaus U. Szucsich. “100 Years of Research on the Protura: Many Secrets Still Retained.” Soil Organics 83 (2011): 309–334.

Shrubovych, Julia, Daniela Bartel, Nikolaus U. Szucsich, Monika G. Resh, and Günther Pass. “Morphological and Genetic Analysis of the Acerentomon doderoi Group (Protura: Acerentomidae) with Description of A. cristiani Sp. Nov.” Plos One 11 (2016): e0148033.

Shrubovych, Julia, J. Rusek, J. Smykla, and E. C. Bernard. “Review of North American Verrucoentomon Species (Protura: Acerentomidae, Nipponentominae), with a Key to Species of the Related Genus Imadateiella Rusek.” Florida Entomologist 98 (2015): 215–222.

Shrubovych, Julia, Josef Starý, and Cyrille A. D’Haese. “Molecular Phylogeny of Acerentomidae (Protura), with Description of Acerentuloides bernardi Sp. Nov. From North America.” Florida Entomologist 100 (2017): 433–443.

Szeptycki, Andrzej. “Catalogue of the World Protura.” Acta Zoologica Cracoviensia 50B (2007): 1–210.

———. “The Present Knowledge of Protura.” Fragmenta Faunistica 40 (1997): 307–311.

Tipping, Christopher, and Robert T. Allen. “Description of Two New Species of Eosentomon from the Ouachita Mountains of Arkansas (Protura, Eosentomidae).” Journal of the Kansas Entomological Society 67 (1994): 253–266.

———. “Description of Two New Species of Eosentomon from the Ouachita Mountains of Arkansas with a Key to the Species with the 6/4 Setal Pattern on Sterna IX/X (Protura: Eosentomidae).” Journal of the New York Entomological Society 103 (1996): 287–301.

Tuxen, Søren L. “Phylogenetical Trends in the Protura.” Zeitschrift für zoologische Systematik und Evolutionsforschung 1 (1963): 277–310.

———. The Protura. A Revision of the Species of the World. With Keys for Determination. Paris: Hermann, 1964.

Yin, Wen-Y. Arthropoda. Protura. Fauna Sinica. Beijing: Science Press, 1999.

Yin, Wen-Y., and L. Z. Xue. “Comparative Spermatology of Protura and its Significance on Proturan Systematics.” Scientia Sinica, Series B 36 (1993): 575–586.

Zhang, Z., and Wen-Y. Yin. “A Revision of the Species and Genera of the Subfamily Anisentominae.” Entomotaxonomia 6 (1984): 59–76.

Chris T. McAllister
Eastern Oklahoma State College

Henry W. Robison
Sherwood, Arkansas