The origin of terrestrial isopods (Crustacea: Isopoda: Oniscidea)

Living isopods of the suborder Oniscidea (commonly called woodlice) are the only group of Crustacea almost entirely composed of terrestrial forms. Furthermore, woodlice are completely independent from the aquatic environment from which they originally arose. From marine ancestors, woodlice are a key taxon to study the conquest of the land among arthropods because of their interesting gradation of morphological, physiological and behavioral adaptations for terrestriality. However, the origin and evolution of this model group are still poorly known. Herein, we provide a synthesis of the oniscidean fossil record to replace this group in a deep-time context. Because members of the Oniscidea are difficult to fossilize, their fossil record alone is undoubtedly fragmentary and not representative of their complete evolutionary history, but it maintains an important relevance by providing reference points. To date, the first attested occurrences of Oniscidea are recorded from the Early Cretaceous. At this time, woodlice were already widely distributed (from Western Europe to Eastern Asia) with several species. By evaluating phylogenetic studies, palaeobiogeographic context of fossil specimens and current biological considerations, we discuss and support a pre-Pangaean origin of the Oniscidea, in the Late Paleozoic—most likely during the Carboniferous.     

Histological studies on the marsupium of two terrestrial isopods (Crustacea,Isopoda, Oniscidea)

The marsupium, a brood pouch in peracarid crustaceans (Crustacea, Malacostraca) has evolved in terrestrial environment for providing nutrition and optimal conditions for embryogenesis. In the present study we give details on the histology and ultrastructure of its constituting elements such as oostegites and cotyledons. Marsupia of two different eco-morphological types of woodlice, namely the non-conglobating species Trachelipus rathkii Brandt, 1833 and the conglobating species Cylisticus convexus De Geer, 1778 were investigated. Light microscopic (LM) studies showed some differences in the main structure of the two species’ brood pouch: in Trachelipus rathkii, a ‘clinger’ type woodlice, the oostegites bend outwards during brood incubation as growing offspring require more space, while in Cylisticus convexus, a ‘roller’ type isopod, the sternites arch into the body cavity to ensure space for developing offspring and still allowing conglobation of the gravid females. The quantitative analysis of the oostegites’ cuticle proved that the outer part is about 2.5 - 3 times thicker compared to the inner part in both species. Electron microscopic (TEM) examinations show only small histological differences in the oostegites and cotyledon structure of the two species. Cellular elements and moderately electron dense fleecy precipitate are found in the hemolymph space between the two cuticles of oostegites. The cells contain PAS positive polysaccharide areas. TEM studies revealed some differences in the cotyledon ultrastructure of the two species. Cotyledons of Trachelipus rathkii consist of cells with cristate mitochondria and granular endoplasmic reticulum with cisterns. Cotyledons of Cylisticus convexus consist of cells with densely cristate mitochondria and ribosomes attached to vesicular membrane structures. In both species cells with electron dense bodies were observed. We conclude that - besides the differences in marsupial shapes - the fine structure of the oostegites and cotyledons is hardly affected by the eco-morphological type, specifically the conglobating or non-conglobating character of the studied species.     

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.     

Ultrastructure of CaCO3 deposits of terrestrial isopods (Crustacea, Oniscidea)

 The ultrastructure of the sternal CaCO₃ deposits of 3 species of the Diplochaeta and 15 of the Crinochaeta was investigated by means of scanning electron microscopy of fractured surfaces. In the Diplochaeta Li-gia italica and L. oceanica, the deposits consist exclusively of individual spherules with diameters between 0.2 and 1.4 μm. No material was observed within the spaces between the spherules. In Ligidium hypnorum, two structurally distinct regions exist. A proximal layer resembling the deposit of Ligia italica and L. oceanica and a distal layer in which the spherules appear to be fused with each other. In the species of the Crinochaeta, the CaCO₃ deposits comprise a spherular region which resembles the deposits of Ligidium hypnorum, and a homogeneous layer located between the spherular part of the deposit and the hypodermal cell layer. In some species the diameters of the spherules may be up to 3.1 μm. In the homogeneous layer and the distal spherular layer more calcium per volume can be stored than in the proximal spherular layer in which the spaces between the spherules are devoid of CaCO₃. This suggests that the multiple layered deposits are an adaptation to terrestrial life, as a consequence of the need for increased resorption of cuticular calcium. Accepted: 7 January 1997     

The diversity of terrestrial isopods in the natural reserve "Saline di Trapani e Paceco" (Crustacea, Isopoda, Oniscidea) in northwestern Sicily

Ecosystems comprising coastal lakes and ponds are important areas for preserving biodiversity. The natural reserve "Saline di Trapani e Paceco" is an interesting natural area in Sicily, formed by the remaining strips of land among salt pans near the coastline. From January 2008 to January 2010, pitfall trapping was conducted in five sampling sites inside the study area. The community of terrestrial isopods was assessed using the main diversity indices. Twenty-four species were collected, only one of them endemic to western Sicily: Porcellio siculoccidentalis Viglianisi, Lombardo & Caruso, 1992. Two species are new to Sicily: Armadilloniscus candidus Budde-Lund, 1885 and Armadilloniscus ellipticus (Harger, 1878). This is high species richness for a single reserve in Sicily. The extended sampling period also allowed us to study species phenology. Most of the species exhibited higher activity in spring than in autumn while some species also exhibited lower activity in the summer. The species richness revealed that the study area is in an acceptable conservation status; Shannon and Pielou indices also confirmed a more or less even distribution of individuals belonging to different species.     

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.     

Morphology and evolution of respiratory structures in the pleopod exopodites of terrestrial Isopoda (Crustacea, Isopoda, Oniscidea)

The morphology of the respiratory structures located in the pleopod exopodites of terrestrial Isopoda is described for representative species of different genera. Special emphasis is set on the evolution of these lungs in the context of phylogenetic relationships as revealed by other morphological characters. In the most primitive species of the Oniscidea, and still of subordinate taxa of the Crinocheta, respiration takes place in the thin ventral integument of the exopodites. The evolution of dorsal respiratory fields with a weakly wrinkled surface occurred at least six times within the Crinocheta. In five of these cases, a further development can be observed. The evolution of a partly covered respiratory field with strongly wrinkled surface may have taken place six times. It is assumed that completely internalized lungs with spiracles surrounded by a water‐repellent surface microsculpture, evolved at least six times independently within the Oniscidea: in the Tylidae, Actaecia, Aphiloscia, the Eubelidae, the Armadillidae and in a taxon probably comprising Porcellionidae plus Armadillidiidae.     

The ultrastructure of the midgut epithelium in millipedes (Myriapoda,Diplopoda)

The midgut epithelia of the millipedes Polyxenus lagurus, Archispirostreptus gigas and Julus scandinavius were analyzed under light and transmission electron microscopies. In order to detect the proliferation of regenerative cells, labeling with BrdU and antibodies against phosphohistone H3 were employed. A tube-shaped midgut of three millipedes examined spreads along the entire length of the middle region of the body. The epithelium is composed of digestive, secretory and regenerative cells. The digestive cells are responsible for the accumulation of metals and the reserve material as well as the synthesis of substances, which are then secreted into the midgut lumen. The secretions are of three types – merocrine, apocrine and microapocrine. The oval or pear-like shaped secretory cells do not come into contact with the midgut lumen and represent the closed type of secretory cells. They possess many electron-dense granules (J. scandinavius) or electron-dense granules and electron-lucent vesicles (A. gigas, P. lagurus), which are accompanied by cisterns of the rough endoplasmic reticulum. The regenerative cells are distributed individually among the basal regions of the digestive cells. The proliferation and differentiation of regenerative cells into the digestive cells occurred in J. scandinavius and A. gigas, while these processes were not observed in P. lagurus. As a result of the mitotic division of regenerative cells, one of the newly formed cells fulfills the role of a regenerative cell, while the second one differentiates into a digestive cell. We concluded that regenerative cells play the role of unipotent midgut stem cells.     

A biogeographical analysis of terrestrial isopods (Isopoda, Oniscidea) from the central Aegean islands (Greece)

Abstract. Terrestrial isopods (Isopoda, Oniscidea) of forty-three central Aegean islands and islets are analysed from a biogeographical point of view. The oniscid fauna consists of sixty-nine species, thirty-two genera and fourteen families and is characterized by Aegean elements that have an eastern Mediterranean origin. Endemism is at the level of 20%, similar to that of oniscids from other Mediterranean archipelagoes. Analysis of species distribution through both idiographic and quantitative approaches (faunal similarity among islands using Jaccard's index, simple matching indices and the UPGMA clustering technique) resulted in the recognition of a major disjunction between Kykladesplus-Ikaria and eastern islands-plus-Astypalea and four noteworthy island groups: the eastern islands, Naxos-Ikaria, Amorgos, and all other Kyklades. Island similarities are generally consistent with the known palaeogeography of the area with the exception of Ikaria's placement with Naxos among the Kyklades. Also, the 'eastern' character of Astypalea is in conflict with evidence from other known taxa.     

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.     

The allometry of metabolism in southern African millipedes (Myriapoda: Diplopoda)

Abstract. We determined standard metabolic rate at 25°C in forty-eight species of millipede from southern Africa and compared these data with confident measures of standard metabolic rate previously published for other arthropod groups.Metabolic rate in millipedes was not significantly different from that in beetles, ants or spiders once body mass effects had been accounted for, but was significantly higher than that in ticks.The exponent for the mass scaling of metabolic rate did not vary significantly between the five arthropod orders.Our best estimate for the relationship between standard metabolic rate (μl O₂ h^-1) and body mass (mg) in non-tick arthropods was 0.86 mass^0.73.     

A Red List of terrestrial isopods (Isopoda: Oniscidea) in Flanders (northern Belgium) and its implications for conservation

Journal of Insect Conservation - Although diversity and abundance of arthropods have been shown to decline globally, they are underrepresented in nature conservation efforts and policies....     

Biology and population dynamics of Porcellionides sexfasciatus (Crustacea,Isopoda, Oniscidea)

The biology and the population dynamics of Porcellionides sexfasciatus Budde-Lund (1879) were studied on a field and carried out at Garat Naam (Kasserine, Tunisia) from July 1996 to June 1998. The reproduction exhibited a seasonal pattern extending from February/March to October/November. The juveniles appeared in the population from April to November. Size frequency distributions were analysed and 14 cohorts were recognised during the sampling period. Six cohorts were identified at the first sampling and eight new ones on the other samplings. Among these latter cohorts, three were tracked till they disappeared. Minimum average length of new cohorts ranged from 3.07 +/- 0.35 mm to 3.47 +/- 0.2 mm. Maximum average length of cohorts was 10.42 mm. P. sexfasciatus is a semi-annual species (females producing two or three broods per year), with iteroparous and amphogenes females (females reproducing twice or more in their life and producing both males and females), and bivoltine life cycle (two generations per year). The females are able to produce two broods, in the laboratory, without new mating. Fecundity and fertility, corresponding to the number of eggs or embryos per brood, appeared positively correlated with females' size. Although oscillating throughout the year, the sex ratio was often in equilibrium.     

Dietary effects on growth, reproduction, body composition and stress resistance in the terrestrial isopods Oniscus asellus and Porcellio scaber

The effect of differences in food composition on growth, body composition and cold tolerance of the isopods Porcellio scaber (Latreille) and Oniscus asellus (L.) has been studied. The effect on reproduction of P. scaber was included. Total lipid and protein content remained the same in O. asellus, given food with a nitrogen content of 2.4, 2.5, 2.8 or 3.1% for 8 weeks. Those fed on 3.1% N gained significantly more weight than those fed on 2.4, 2.5 or 2.8% N. Cold tolerance after a period of low temperature acclimation could not be tested, due to high mortality at the subzero treatment. Haemolymph osmolality increased after the winter acclimation for all food treatments. Juvenile P. scaber, given food of 1.8, 2.5 or 3.1% N, showed no difference in growth over 18 weeks, nor in body composition over 14 weeks. Diet did not influence cold tolerance ability and haemolymph osmolality remained the same with changing cold tolerance of the animals. Gravid females of P. scaber were separated to examine the effect of diet on reproduction. Diet did not influence the number of juveniles, nor their weight. In all food treatments, a significant correlation was found between the weight of the female and the number and weight of her offspring.     

Laboratory infection of terrestrial isopods (Crustacea: Isopoda) with neoaplectanid and heterorhabditid nematodes (Rhabditida: Nematoda)

Under laboratory conditions, the nematodes Neoaplectana carpocapsae and Heterorhabditis heliothidis were able to infect and develop inside the hemocoel of terrestrial isopods belonging to the genus Porcellio. Armidillidium vulgare was also infected by N. carpocapsae, but this host was less susceptible than Porcellio. Results show that, under suitable ecological conditions, it would be feasible to utilize N. carpocapsae as a biological control agent of sowbugs (Porcellio spp.). This is the first report showing the ability of neoaplectanids and heterorhabditids to invade representatives of the Crustacea.     

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.     

The agnarid terrestrial isopods (Isopoda,Oniscidea, Agnaridae) of the province of Qazvin,Iran, with a description of a new species

Six species of terrestrial isopods from the province of Qazvin, central Iran, are recorded. Three species, Hemilepistus klugii (Brandt, 1833), Protracheoniscus ehsani Kashani, 2014 and Mongoloniscus persicus Kashani, 2014, were previously reported from the province. Hemilepistus elongatus Budde-Lund, 1885 and Protracheoniscus major (Dollfus, 1903) are recorded for the first time, and one species, Protracheoniscus sarii sp. n., is described as new. The diagnostic characters of the new species are figured.     

Description of the postmarsupial manca stages of Armadillidium granulatum (Crustacea,Isopoda, Oniscidea)

The development of the postmarsupial manca stages of Armadillidium granulatum Brandt, 1833 was studied in detail by morphological analysis. Ovigerous females were reared separately under controlled conditions, allowing us to follow the stages of development from release from the marsupium until the appearance of the first juvenile stage, identified by the full development of the seventh pair of pereopods. Each newborn was followed to record the subsequent moults that identify the three postmarsupial manca stages. Manca stage M I had a mean duration of 6 h, manca stage M II 15 days, and manca stage M III 32 days. The cephalothorax width was measured to provide a growth measure for each stage. The mean values of the cephalothorax width were: 0.512 mm (± 0.083 SD) for M I, 0.677 mm (± 0.058 SD) for M II and 1.194 mm (± 0.079 SD) for M III. The morphological modifications in the three postmarsupial manca stages were described, the body parts illustrated, and SEM images taken. The distinguishing characteristics among mancas were discussed, and comparisons made with manca stages of other terrestrial isopod species.