Colonization of Colliery Spoil Heaps by Millipedes (Diplopoda) and Terrestrial Isopods (Oniscidea) in the Sokolov Region, Czech Republic

Successive development of millipede and terrestrial isopod assemblages in colliery spoil heaps in the Sokolov region (northwest Bohemia, Czech Republic) was studied during the years 1993–1998. Younger colliery spoil heaps were characterized by a lower number and low density of millipede species. The millipedes Polydesmus inconstans, Polydesmus testaceus, and Craspedosoma rawlinsii represented the main pioneer species. Alder afforestation proved to be more suitable for the recolonization of millipede populations, especially for the predominant Julus scandinavius. Terrestrial isopods colonized all parts of the heaps, including the youngest open plots. The most frequent isopod, Trachelipus rathkii, is a colonizing species with an apparently high adaptability to different environmental conditions. The isolated character of the extensive heap areas, together with existing extreme soil conditions, resulted in slow recolonization and a successional development of stable populations of these animals. However, the relatively high densities of millipede and isopod assemblages in suitable alder afforestation can represent further potential sources for colonization of other open‐heap areas.     

Diversity and function of fungi associated with the fungivorous millipede,Brachycybe lecontii

Fungivorous millipedes (subterclass Colobognatha) likely represent some of the earliest known mycophagous terrestrial arthropods, yet their fungal associates remain elusive. Here we describe relationships between fungi and the fungivorous millipede, Brachycybe lecontii. Their fungal community is surprisingly diverse, including 176 genera, 39 orders, four phyla, and several undescribed species. Of particular interest are twelve genera conserved across wood substrates and millipede clades that comprise the core fungal community of B. lecontii. Wood decay fungi, long speculated to serve as the primary food source for Brachycybe species, were absent from this core assemblage and proved lethal to millipedes in pathogenicity assays while entomopathogenic Hypocreales were more common in the core but had little effect on millipede health. This study represents the first survey of fungal communities associated with any colobognath millipede, and these results offer a glimpse into the complexity of millipede fungal communities.     

Guilty by association: an evaluation of millipedes as pests of carrot and sweet potato

An evaluation of the pest potential of millipede species occurring in Ontario sweet potato and carrot fields was conducted in response to recent grower concerns about the presence of millipedes in close proximity to damaged vegetables. This study is the first North American survey of millipedes on arable soils and the first evaluation of North American millipede damage to sweet potatoes and carrots. Through field surveys, Cylindroiulus caeruleocinctus was found to be the dominant millipede species in Ontario sweet potatoes and carrots. Fields were surveyed over the growing season, and the factors important to each species’ abundance were evaluated using Minimum AIC Estimation (MAICE). Post‐harvest damage assessments were performed, and MAICE analysis was used to determine which arthropod and environmental parameters were most important in explaining damage to sweet potatoes and carrots. Wireworm (Elateridae) abundance was consistently found to explain root damage better than C. caeruleocinctus abundance, and it is concluded that the majority of field‐observed damage was caused by wireworms. C. caeruleocinctus was negatively correlated with both wireworms and damage in carrot fields and is not likely to be a pest of that vegetable. However, abundance of C. caeruleocinctus in sweet potatoes was positively correlated with both wireworms and damage. This species may cause some damage to sweet potato tubers under field conditions, but management tactics should focus on wireworms as the primary source of damage.     

Methane Production and Methanogenic Archaea in the Digestive Tracts of Millipedes (Diplopoda)

Methane production by intestinal methanogenic Archaea and their community structure were compared among phylogenetic lineages of millipedes. Tropical and temperate millipedes of 35 species and 17 families were investigated. Species that emitted methane were mostly in the juliform orders Julida, Spirobolida, and Spirostreptida. The irregular phylogenetic distribution of methane production correlated with the presence of the methanogen-specific mcrA gene. The study brings the first detailed survey of methanogens’ diversity in the digestive tract of millipedes. Sequences related to Methanosarcinales, Methanobacteriales, Methanomicrobiales and some unclassified Archaea were detected using molecular profiling (DGGE). The differences in substrate preferences of the main lineages of methanogenic Archaea found in different millipede orders indicate that the composition of methanogen communities may reflect the differences in available substrates for methanogenesis or the presence of symbiotic protozoa in the digestive tract. We conclude that differences in methane production in the millipede gut reflect differences in the activity and proliferation of intestinal methanogens rather than an absolute inability of some millipede taxa to host methanogens. This inference was supported by the general presence of methanogenic activity in millipede faecal pellets and the presence of the 16S rRNA gene of methanogens in all tested taxa in the two main groups of millipedes, the Helminthophora and the Pentazonia.     

A New Dimension in Documenting New Species: High-Detail Imaging for Myriapod Taxonomy and First 3D Cybertype of a New Millipede Species (Diplopoda,Julida, Julidae)

We review the state-of-the-art approaches currently applied in myriapod taxonomy, and we describe, for the first time, a new species of millipede (Ommatoiulus avatar n. sp., family Julidae) using high-resolution X-ray microtomography (microCT) as a substantive adjunct to traditional morphological examination. We present 3D models of the holotype and paratype specimens and discuss the potential of this non-destructive technique in documenting new species of millipedes and other organisms. The microCT data have been uploaded to an open repository (Dryad) to serve as the first actual millipede cybertypes to be published.     

Impact of microphallid trematodes on the survivorship, growth, and reproduction of an isopod (Cyathura carinata)

Crustaceans are second intermediate hosts to several microphallid species (Trematoda). Some of these parasites are potentially pathogenic or manipulative. A laboratory experiment was performed to assess the impact of microphallids on the survival, growth and fecundity of Cyathura carinata, a protogynous hermaphroditic isopod, widespread within European estuaries. For nearly 12 weeks, experimental populations of infected and non-infected isopods were kept at 25 °C. C. carinata carrying microphallid cysts showed higher mortality rates than non-infected specimens and were not able to produce embryos. The reduced fecundity of infected isopods could be caused by parasite-induced castration and/or by mating failure due to behavioural modifications in one of the sexes. It might also be associated with lower growth rates and lower moulting frequencies, since infected C. carinata were significantly smaller than the non-infected after 9 weeks. This may imply a setback for the isopods to achieve sexual maturity (which may also affect the population sex ratio) and for females to lay their eggs in the marsupia. Regardless of the mechanisms involved, microphallids may have severe consequences for their host populations, through negative effects on survival, growth and fecundity. For species with direct development, such as C. carinata, parasite-induced reproduction failure may contribute to temporal fluctuations of abundance. Based on the present results, it is recommended to include parasites as an important factor influencing host populations from shallow-water ecosystems.     

Evolutionary transition to XY sex chromosomes associated with Y-linked duplication of a male hormone gene in a terrestrial isopod

Sex chromosomes are highly variable in some taxonomic groups, but the evolutionary mechanisms underlying this diversity are not well understood. In terrestrial isopod crustaceans, evolutionary turnovers in sex chromosomes are frequent, possibly caused by Wolbachia, a vertically-transmitted endosymbiont causing male-to-female sex reversal. Here, we use surgical manipulations and genetic crosses, plus genome sequencing, to examine sex chromosomes in the terrestrial isopod Trachelipus rathkei. Although an earlier cytogenetics study suggested a ZZ/ZW sex chromosome system in this species, we surprisingly find multiple lines of evidence that in our study population, sex is determined by an XX/XY system. Consistent with a recent evolutionary origin for this XX/XY system, the putative male-specific region of the genome is small. The genome shows evidence of Y-linked duplications of the gene encoding the androgenic gland hormone, a major component of male sexual differentiation in isopods. Our analyses also uncover sequences horizontally acquired from past Wolbachia infections, consistent with the hypothesis that Wolbachia may have interfered with the evolution of sex determination in T. rathkei. Overall, these results provide evidence for the co-occurrence of multiple sex chromosome systems within T. rathkei, further highlighting the relevance of terrestrial isopods as models for the study of sex chromosome evolution.Subject terms: Evolutionary genetics, Genome evolution     

An evolutionary timescale for terrestrial isopods and a lack of molecular support for the monophyly of Oniscidea (Crustacea: Isopoda)

The marine metazoan fauna first diversified in the early Cambrian, but terrestrial environments were not colonized until at least 100 million years later. Among the groups of organisms that successfully colonized land is the crustacean order Isopoda. Of the 10,000 described isopod species, ~ 3,600 species from the suborder Oniscidea are terrestrial. Although it is widely thought that isopods colonized land only once, some studies have failed to confirm the monophyly of Oniscidea. To infer the evolutionary relationships among isopod lineages, we conducted phylogenetic analyses of nuclear 18S and 28S and mitochondrial COI genes using maximum-likelihood and Bayesian methods. We also analyzed a second data set comprising all of the mitochondrial protein-coding genes from a smaller sample of isopod taxa. Based on our analyses using a relaxed molecular clock, we dated the origin of terrestrial isopods at 289.5 million years ago (95% credibility interval 219.6–358.9 million years ago). These predate the known fossil record of these taxa and coincide with the formation of the supercontinent Pangaea and with the diversification of vascular plants on land. Our results suggest that the terrestrial environment has been colonized more than once by isopods. The monophyly of the suborder Oniscidea was not supported in any of our analyses, conflicting with classical views based on morphology. This draws attention to the need for further work on this group of isopods.     

Assemblages of terrestrial isopods (Isopoda, Oniscidea) in a fragmented forest landscape in Central Europe

Terrestrial isopods were collected in 13 forest fragments differing in area (within the range of 0.1 and 254.5 ha), shape and composition of forest vegetation (thermophilous oak, mesophilous oak-hornbeam, thermophilous oak-hornbeam, acidophilous oak, basiphilous oak, beech oak-hornbeam, moist mixed deciduous forest, plantations of deciduous and coniferous trees), all situated in the Český kras Protected Landscape Area, Czech Republic, Central Europe. Number of sites sampled in each fragment of forest depended on its size and ranged from 1 to 7. Altogether 30 sites were sampled. Soil samples (5 per site collected twice a year) and pitfall trapping (5 traps per site in continuous operation throughout a year) during 2008–2009 yielded a total of 14 species of terrestrial isopods. The highest densities and highest epigeic activities of terrestrial isopods were recorded in the smallest fragments of woodland. Although a wider range of habitats were sampled in the larger fragments of woodland there was not a greater diversity of species there and the population densities and epigeic activities recorded there were lower. Porcellium collicola was most abundant in small fragments of woodland regardless the vegetation there. Armadillidium vulgare and Protracheoniscus politus were statistically more abundant in the larger fragments of woodland. The results indicate that forest fragmentation does not necessarily result in a decrease in the species richness of the isopod assemblages in such habitats.     

Granivory in terrestrial isopods

Abstract Granivory (seed feeding) evolved in many animal groups. Field observations hint at the existence of granivory in terrestrial isopods (Crustacea: Isopoda: Oniscidea), for which it was previously unknown. In this paper granivory in terrestrial isopods is addressed for the first time, focusing on (i) seed acceptance in the presence of plant litter and (ii) size as a constraint for acceptance and consumption. In a laboratory choice experiment, Armadillidium vulgare consumed seeds of Capsella bursa‐pastoris and Poa annua when plant litter was present. In a no‐choice experiment, seeds of seven plant species were offered to four isopod species giving 13 combinations in total [A. vulgare (seven species of seeds), Oniscus asellus (two), Porcellio scaber (two), and Porcellionides pruinosus (two)]. The tested isopods differed in their acceptance (proportion of individuals consuming seeds) and consumption (both number and amount of seeds eaten) of seed species. Size as a constraint was demonstrated in A. vulgare offered Cirsium arvense seed, since the probability that this large seed was eaten increased with body size of the isopod. In the other 10 seed–isopod pairs, seed consumption increased linearly with isopod body size. Granivory is thus widespread in terrestrial isopods, although the tendency to eat seeds differs between species.     

The distribution and abundance of the Portuguese millipede Ommatoiulus moreletii (Diplopoda: Iulidae) in Australia

The Portuguese millipede Ommatoiulus moreletii is widespread in South Australia, well-established in Victoria and Tasmania and has recently been found in Perth. Western Australia. It is predicted that this millipede will eventually occur in pest numbers in large areas of southern Australia. Within South Australia, O. moreletii initially erupts in very large numbers following invasion of a new area, then declines to a lower abundance. The decrease in abundance may be caused by a shortage of food. There was no evidence to suggest changes in the sex ratio, age distribution or percentage maturity of O. moreletii following invasion. However, millipedes in newly-invaded areas were larger (and therefore more fecund in the case of females) than those in older populations. There was no evidence that O. moreletii is competing with native millipedes in South Australia. Three to four years after a bushfire in a Eucalyptus woodland, there was no difference between the numbers of O. moreletii in burnt and unburnt areas.     

Diversity and distribution of millipedes (Diplopoda) in the Campo Ma'an National Park,southern Cameroon

Diplopods (millipedes) are one of the important groups of terrestrial Arthropoda in tropical forest ecosystems. Despite their ecological importance, data on millipede populations are still scarce and outdated in Cameroon. The first comparative eco‐faunistic analysis is presented of two local populations of Diplopoda in two lowland rainforests (nearly primary and secondary) during 12 months (2015–2016) at the southern periphery of the Campo Ma'an National Park in southern Cameroon. The millipedes were collected using pitfall trapping and quadrat sampling, their diversity and distribution analyzed with the help of two diversity indexes and two nonparametric estimators. Overall, 27 species in eighteen genera, ten families and four orders were revealed in the two forests, yet each faunule was about equally rich (23 and 22 species in the primary and secondary forest, respectively) and peculiar (five and four species unique, respectively). The Odontopygidae was the most abundant family, which made up to 33% of the total species diversity. The most abundant species in both forests was Aporodesmus gabonicus (26.8% of occurrences). This study shows that despite the similarity in millipede species richness between both habitats, the species composition of all habitats was different. Some species occurred in two habitats whilst others were restricted to only one habitat.     

Reference values for feeding parameters of isopods (Porcellio scaber,Isopoda, Crustacea)

The advantage of using terrestrial isopods in toxicity studies is that a battery of parameters can be tested at different levels of biological complexity. Feeding parameters for example link organism level response to potential ecological consequences but a problem with using feeding parameters in toxicity tests with terrestrial isopods is their high variability. The aim of our study was to set benchmark values for feeding parameters for isopod Porcellio scaber (Isopoda, Crustacea) in laboratory-controlled experiments. In the work presented here, the daily feeding rate of the central 50% of the control population of Porcellio scaber and a correlation between feeding rate and isopod weight were set. Values outside these ranges need additional evaluation to increase the relevance of test outcomes. We suggest using benchmark values for feeding parameters as well as the coefficient of variation (a) to identify animals with altered feeding parameters with respect to controls, and (b) to assess the data quality in each experiment.     

Demography of some non-native isopods (Crustacea,Isopoda, Oniscidea) in a Mid-Atlantic forest,USA

Introduced species dominate the terrestrial isopod fauna in most inland habitats of North America, including urban landscapes. These non-native species are often very abundant and thus potentially play a significant role in detritus processing. We monitored isopod assemblages in an urban forest for a year to examine the relationship between surface activity and abiotic environmental factors, and to analyze reproductive characteristics that might contribute to their successful establishment. Using pitfall trap samples we recorded five species, two of which, Trachelipus rathkii and Cylisticus convexus, were highly abundant. We determined size, sex and reproductive state of each individual. Surface activity of both species reflected variability in abiotic stress factors for isopods, such as soil moisture and soil temperature. Early spring the main trigger was soil temperature while later in the season increasing temperature and decreasing soil moisture jointly affected population dynamics. Activity significantly correlated with soil moisture. The temporal pattern of sex ratios supported the secondary sex ratio hypothesis. Males dominated the samples on the onset of the mating season in search of females. The pattern was reversed as females searched for suitable microsites for their offspring. Size independent fecundity decreased as conditions became more stressful late in the season.     

Pathogenic effect of entomopathogenic nematode-bacterium complexes on terrestrial isopods

In this study, we evaluated the effect of entomopathogenic nematodes (EPNs) Steinernema carpocapsae, Steinernema feltiae and Heterorhabditis bacteriophora, symbiotically associated with bacteria of the genera Xenorhabdus or Photorhabdus, on the survival of eight terrestrial isopod species. The EPN species S. carpocapsae and H. bacteriophora reduced the survival of six isopod species while S. feltiae reduced survival for two species. Two terrestrial isopod species tested (Armadillidium vulgare and Armadillo officinalis) were found not to be affected by treatment with EPNs while the six other isopod species showed survival reduction with at least one EPN species. By using aposymbiotic S. carpocapsae (i.e. without Xenorhabdus symbionts), we showed that nematodes can be isopod pathogens on their own. Nevertheless, symbiotic nematodes were more pathogenic for isopods than aposymbiotic ones showing that bacteria acted synergistically with their nematodes to kill isopods. By direct injection of entomopathogenic bacteria into isopod hemolymph, we showed that bacteria had a pathogenic effect on terrestrial isopods even if they appeared unable to multiply within isopod hemolymphs. A developmental study of EPNs in isopods showed that two of them (S. carpocapsae and H. bacteriophora) were able to develop while S. feltiae could not. No EPN species were able to produce offspring emerging from isopods. We conclude that EPN and their bacteria can be pathogens for terrestrial isopods but that such hosts represent a reproductive dead-end for them. Thus, terrestrial isopods appear not to be alternative hosts for EPN populations maintained in the absence of insects.     

Locomotory,ventilatory and metabolic responses of the subterranean Stenasellus virei (Crustacea,Isopoda) to severe hypoxia and subsequent recovery

The locomotory and ventilatory activities and the intermediary and energy metabolism modifications of the hypogean aquatic isopod crustacean Stenasellus virei were investigated in severe hypoxia (Po₂ < 0.03 kPa) and subsequent recovery. The aims of this study were i) to determine why the subterranean species displayed a greater tolerance of hypoxia than numerous other epigean crustaceans, ii) to confirm previous results obtained with four hypogean and epigean crustaceans, iii) to compare the responses to severe hypoxia in hypogean amphipods and isopods, and iv) to better understand the ecological problems of the hypogean organisms survival in subterranean habitats. S. virei responded to experimental long-term, severe hypoxia with classical anaerobic metabolism mainly characterized by a decrease in adenosine triphosphate (ATP) and phosphagen, utilization of glycogen and glutamate, and accumulation of lactate and alanine. Lactate was also largely excreted by this organism, which is unusual for crustaceans in general. Compared to most other epigean crustaceans, the isopod S. virei showed high amounts of stored glycogen and arginine phosphate. These differences in glycogen and phosphagen stores, and the ability to reduce energetic expenditures linked to locomotion and ventilation, extended the survival of S. virei under experimental anaerobiosis. During recovery, the isopod S. virei showed a higher capacity for glyconeogenesis from lactate and a faster and total replenishment of ATP and arginine phosphate levels than epigean crustaceans. Data concerning responses to hypoxia and subsequent recovery in S. virei are similar to those previously obtained with two other hypogean amphipods, except that this isopod did not synthesize succinate in anaerobiosis.     

The terrestrial Isopoda (Crustacea,Oniscidea) of Rapa Nui (Easter Island), with descriptions of two new species

Nine species of terrestrial isopods are reported for the Polynesian island of Rapa Nui (Easter Island) based upon museum materials and recent collections from field sampling. Most of these animals are non-native species, but two are new to science: Styloniscus manuvaka sp. n. and Hawaiioscia rapui sp. n. Of these, the former is believed to be a Polynesian endemic as it has been recorded from Rapa Iti, Austral Islands, while the latter is identified as a Rapa Nui island endemic. Both of these new species are considered ‘disturbance relicts’ and appear restricted to the cave environment on Rapa Nui. A short key to all the oniscidean species presently recorded from Rapa Nui is provided. We also offered conservation and management recommendations for the two new isopod species.     

Distribution of millipedes (Myriapoda,Diplopoda) along a forest interior – forest edge – grassland habitat complex

We studied the distribution of millipedes in a forest interior-forest edge-grassland habitat complex in the Hajdúság Landscape Protection Area (NE Hungary). The habitat types were as follows: (1) lowland oak forest, (2) forest edge with increased ground vegetation and shrub cover, and (3) mesophilous grassland. We collected millipedes by litter and soil sifting. There were overall 30 sifted litter and soil samples: 3 habitat types × 2 replicates × 5 soil and litter samples per habitats. We collected 9 millipede species; the most abundant species was Glomeris tetrasticha, which was the most abundant species in the forest edge as well. The most abundant species in the forest interior was Kryphioiulus occultus, while the most abundant species in the grassland was Megaphyllum unilineatum. Our result showed that the number of millipede species was significantly lower in the grassland than in the forest or in the edge, however there were no significant difference in the number of species between the forest interior and the forest edge. We found significantly the highest number of millipede individuals in the forest edge. There were differences in the composition of the millipede assemblages of the three habitats. The results of the DCCA showed that forest edge and forest interior habitats were clearly separated from the grassland habitats. The forest edge habitat was characterized by high air temperature, high soil moisture, high soil pH, high soil enzyme activity, high shrub cover and low canopy cover. The IndVal and the DCCA methods revealed the following character species of the forest edge habitats: Glomeris tetrasticha and Leptoiulus cibdellus. Changes in millipede abundance and composition were highly correlated with the vegetation structure.     

Benthic isopods (Crustacea,Malacostraca) from the Ross Sea,Antarctica: species checklist and their zoogeography in the Southern Ocean

In this study isopod species of the Ross Sea were investigated. Literature until May 2008 was checked to provide an overview of all known and described species in the Ross Sea. This species checklist was then enlarged through material of the 19th Italica expedition in 2004. During this expedition for the first time a small mesh net (500 μm) was used. Nine thousand four hundred and eighty one isopod specimens were collected during this expedition. Through this material the number of isopod species in the Ross Sea increased from 42 to 117 species, which belong to 20 families and 49 genera. Fifty-six percentage of the isopods species collected during the Italica expedition are new to science. The zoogeography of the 117 species was investigated. A non-transformed binary presence-absence data matrix was constructed using the Bray–Curtis coefficient. The results were displayed in a cluster analysis and by nonmetric multidimensional scaling (MDS). This paper gives a first insight into the occurrence and distribution of the isopod species of the Ross Sea.     

Macaronesian millipedes (Diplopoda) with emphasis on endemic species swarms on Madeira and the Canary Islands

Endemic species swarms constitute large fractions of the millipede faunas of Madeira (29 species of the Cylindroiulus madeirae group, plus six species of Acipes , out of a total of 60 species) and the Canary Islands (46 species of Dolichoiulus , plus four species of the Glomeris alluaudi-group , out of a total of about 79 species). The poorer faunas of the Azores (22 species) and the Cape Verde Islands (15 species) in contrast only include a few endemics. The Cylindroiulus madeirae group and Dolichoiulus show a high degree of diversity of structure (size, colour, leg length etc.) and habitat (laurisilva, xeric habitats, caves). The C. madeirae group, unlike Dolichoiulus , is strongly concentrated in the laurisilva. In this habitat, microhabitat differentiation is pronounced in both swarms.