Effects of group size on aggregation against desiccation in woodlice (Isopoda: Oniscidea)

Aggregation in terrestrial isopods, a behaviour that results in the formation of dense clusters, is readily accepted as a mechanism of resistance to desiccation. Thus, aggregation is considered to be an adaptation to terrestrial life in this fully terrestrial suborder of crustaceans. In the present study of Porcellio scaber Latreille, a cosmopolitan species, individual water loss is investigated experimentally as a function of the size of the aggregates and, for the first time, over a large range of group sizes (groups of 1, 10, 20, 40, 60, 80 and 100 individuals). From the perspective of an isolated individual, aggregation behaviour is effective in reducing the rate of water loss whatever the group size, and reduces the individual water loss rate by more than half in large groups. However, the water loss rate of an individual follows a power law according to group size. Accordingly, if the addition of individuals to small groups strongly reduces the water losses per individual, adding individuals to large groups only slightly reduces the individual water losses. Thus, the successful reduction of the water loss rate by this aggregation behaviour is confirmed, although only up to a certain limit, particularly if the number of individuals per aggregate exceeds 50–60 under the experimental conditions used in the present study. Moreover, the individual surface area exposed to the air, as a function of group size, follows a similar pattern (i.e. a similar power law). Thus, a geometrical explanation is proposed for the nonlinear water losses in woodlice aggregates. These results are discussed in relation to the group sizes observed both in the laboratory and the field.     

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.     

Molecular evolution of the small subunit ribosomal DNA in woodlice (Crustacea, Isopoda, Oniscidea) and implications for Oniscidean phylogeny

The small subunit ribosomal DNA (ssu rDNA) of 13 isopods was sequenced. The entire length of the ribosomal gene is unusually long, resulting from the presence of five expansion elements accounting for more than 40% of the gene. We found that in terrestrial isopods the length of the ssu rDNA ranges from 2414 bp (Ligidium hypnorum) to 3537 bp (Cubaris murina). This is the longest metazoan ssu rDNA reported to date. The conserved regions are highly informative for analysis of the early nodes of the tree, whereas the variable expansion elements are better suited to reconstruction of the branching pattern between closely related taxa. The suggested relationship among Synochaeta, Crinochaeta, and Diplochaeta based on the conserved regions confirms that based on previous morphological analyses. In contrast, the phylogeny within the Crinochaeta based on the entire ssu rDNA including the variable domains is in conflict with that based on most of the morphological analyses. The phylogenetic analyses of the ssu rDNA support a repeated independent evolution of the three different types of pleopodal lungs in the Crinochaeta.     

Using woodlice (Isopoda,Oniscoidea) to demonstrate orientation behaviour

Woodlice show two behavioural kineses as adaptations to prevent water loss. These are attraction to solid objects, including each other, (thigmokinesis), and attraction to dark places (negative photqkinesis). The interaction between these two kineses was tested in a classroom experiment, in which one to five woodlice were placed in a petri dish with one half painted black. The strongest response was the thigmotactic attraction, with negative photokinesis playing a secondary role. From these experiments students learn about cooperation, taxes (directional responses to stimulus i.e. the woodlice move towards or away from a stimulus) and kineses (non-directional response to stimulus, i.e. the woodlice respond by showing an increase or decrease in activity level), and experimental design.     

The Best Timing of Mate Search in Armadillidium vulgare (Isopoda,Oniscidea)

Mate choice is mediated by many components with the criteria varying across the animal kingdom. Chemical cues used for mate attractiveness can also reflect mate quality. Regarding the gregarious species Armadillidium vulgare (isopod crustacean), we tested whether individuals can discriminate conspecifics at two different levels (between sex and physiological status) based on olfactory perception. Tested conspecifics were individuals of the same or opposite sex, with the females at different moult stages. We found that the attractiveness of individuals was mediated by short-distance chemical cues and tested individuals were able to discriminate and prefer individuals of the opposite sex. Moreover, male preference to female increased during their moulting status as they matured. Males were particularly more attracted by females with appearing white calcium plates, which corresponds to the beginning of their higher receptivity period. These differences in attractiveness due to sex and physiological status are likely to shape the composition of aggregates and facilitate mate finding and optimize the reproductive success for both males and females. Thus aggregation pheromones could be linked to sex pheromones in terrestrial isopods.     

潮虫亚目(甲壳动物亚门:等足目)二中国新纪录种

通过对山西省境内等足目进行调查研究,发现等足目潮虫亚目鼠妇科腊鼠妇属2个新纪录种,分别为多变腊鼠妇Porcellionides variabilis Jackson,1926和弗罗里达腊鼠妇Porcellionides floria Garthwaite&Sassaman,1985.多变腊鼠妇主要鉴别特征为体色各部分颜色多变,雄性第1腹肢的外肢节近鳃盖状,下端具一弧形凹陷,上端具波浪状凹刻;弗罗里达腊鼠妇主要鉴别特征为头胸部近似长方形,第7胸肢座节末端具2枚硬刺.所有检视标本保存于山西师范大学生命科学学院动物实验室.     

Alterations in habituation of the tail flip response in epigean and troglobitic crayfish

We demonstrate that the probability of the crayfish, P. clarkii, to tail flip in response to a touch on the dorsal tail fan is dependent on both the size and the behavioral state of the animal. Alterations in the animal's internal physical state, such as when the animal autotomizes its chelipeds, will cause larger-sized animals to tail flip; if they were not autotomized, then no tail flip response would occur. Altering the external environment by removal of water causes small crayfish, which normally habituate slowly, to rapidly habituate. Observation of large adult crayfish in a species, O. australis packardi, one that evolved to live in total cave darkness, revealed that they are more likely to tail flip than are the sighted, adult P. clarkii. Results indicate that the behavioral state of the crayfish can result in rapid and long-term alterations in the tail flip response and in habituation rates to repetitive stimuli. This ability to show plasticity in gain setting may be regulated by neuromodulators and can occur in large adults of the sighted crayfish. Differences between the two species indicate that size may not be the sole contributing factor to account for tail flip behaviors. J. Exp. Zool. 290:163-176, 2001.     

Ecotypic differentiation and phenotypic plasticity in reproductive traits of Armadillidium vulgare (Isopoda: Oniscidea)

Armadillidium vulgare differed in growth and survivorship on two field sites. Growth rates were higher at a site with consistently higher quality food than at the other site where less high-quality food was produced and which was less predictably accessible. Survivorship was higher at the second site where temperature fluctuations were consistently smaller. Individuals from the two populations were kept for 6 months under the same food and temperature conditions and patterns of resource allocation to reproductive traits analysed. Members of the population from the site with good growth conditions had significantly higher reproductive allocation, by 13.5%, and larger broods, by 9.1%, than those from the site with poor growth conditions. Contrary to theoretical predictions, they also had significantly larger offspring, by 7.5% dry mass. Larger offspring survived better than small ones. This differential survivorship, by 20% for a 3.4% difference in live mass, was much more pronounced under conditions of moisture stress and under fluctuating temperature regimes. Larger offspring would therefore be at a selective advantage on the site with more severe temperature fluctuations. Phenotypic plasticity in reproductive traits in response to experimental changes in food quality, temperature and crowding were monitored. Reproductive allocation was increased by 20.8% under conditions of higher food quality, by 14.7% at higher temperatures, and by 12.5% under less crowded conditions. Brood size, but not offspring dry mass, increased when food quality increased. When crowding increased by 25.0%, the size of broods remained the same but the dry mass of individual offspring decreased by 11.2%. Members of the population from the site with more variable access to high-quality food showed more plasticity in reproductive traits in response to changes in food supply than members of the population from the site with the more predictable food supply. Members of the population from the site with more stable temperatures showed less plasticity to temperature changes than members of the population from the site with greater temperature fluctuations. It is concluded that the observed microevolutionary processes and phenotypic plasticity have adaptative value as responses to spatial and temporal heterogeneity in environmental conditions.     

Mineral Deposition in Bacteria-Filled and Bacteria-Free Calcium Bodies in the Crustacean Hyloniscus riparius (Isopoda: Oniscidea)

Crustacean calcium bodies are epithelial sacs which contain a mineralized matrix. The objectives of this study were to describe the microscopic anatomy of calcium bodies in the terrestrial isopod Hyloniscus riparius and to establish whether they undergo molt-related structural changes. We performed 3D reconstruction of the calcium bodies from paraffin sections and analyzed their structure with light and electron microscopy. In addition, we analyzed the chemical composition of their mineralized matrices with micro-Raman spectroscopy. Two pairs of these organs are present in H. riparius. One pair is filled with bacteria while the other pair is not. In non-molting animals, the bacteria-filled calcium bodies contain apatite crystals and the bacteria-free calcium bodies enclose CaCO₃-containing concretions with little organic matrix. During preparation for molt, an additional matrix layer is deposited in both pairs of calcium bodies. In the bacteria-filled calcium bodies it contains a mixture of calcium carbonate and calcium phosphate, whereas only calcium carbonate is present in bacteria-free calcium bodies. After ecdysis, all mineral components in bacteria-free calcium bodies and the additional matrix layer in bacteria-filled calcium bodies are completely resorbed. During calcium resorption, the apical surface of the calcium body epithelium is deeply folded and electron dense granules are present in spaces between epithelial cells. Our results indicate that the presence of bacteria might be linked to calcium phosphate mineralization. Calcium bodies likely provide a source of calcium and potentially phosphate for the mineralization of the new cuticle after molt. Unlike other terrestrial isopods, H. riparius does not form sternal CaCO₃ deposits and the bacteria-free calcium bodies might functionally replace them in this species.     

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.     

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.     

Homeostatic responses in the gut of Porcellio scaber (Isopoda: Oniscidea) optimize litter degradation

In order to examine the influence of differences in food conditions on gut characteristics in Porcellio scaber, pH-manipulated and microbially inoculated leaf litter from three different tree species were offered. Microbial activity was clearly influenced by the pH levels of the leaves. Analyses of the pH levels in the gut indicated the ability of P. scaber to buffer the pH value in the intestinal tract to about 5.5–6.0 in the anterior hindgut, and to about 6.0–6.5 in the posterior hindgut. The pH levels of the gut sections remained in this range, within a range of food pH from 4.0 to 7.5, no matter what kind of leaves the animals were fed. Homeostatic responses to changes in food pH guarantee optimized digestion of leaf litter. However, when the pH level of the litter dropped below 3.5, P. scaber was not able to maintain the pH conditions in the gut. Furthermore, microorganisms colonizing the litter biased the pH level in the anterior hindgut where digestive processes mainly take place. These results indicate a decline of litter quality with regard to the nutrition of terrestrial isopods, caused by acidification and consequently reduced microbial activity. Accepted: 19 July 1997     

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.     

Shelter site use and secondary sex ratios in the woodlice Armadillidium vulgare and Porcellio scaber (Crustacea: Isopoda)

In grassland populations of the woodlice Armadillidium vulgare and Porcellio scaber (Latreille) the sex ratio in hand collections from beneath wooden offcuts and roofing tiles varied through the breeding season. The proportion of males was higher in these collections from surface refugia than in independent estimates of the population sex ratio taken from soil cores. Collections became female-biased in June and July when most females were carrying broods, most notably in P. scaber . It is suggested that males use surface shelter between foraging events. A. vulgare males are particularly abundant under boards in May as they become active on the soil surface in order to locate mates. Females may find the higher and more equable temperatures in refugia attractive because they reduce brood development time but the cost of this advantage is the risk of failure to balance moisture requirements. These patterns of habitat use by the sexes have important implications for several population processes, the evolution of life-history tactics and the development of mating systems in these species.     

Discontinuous ammonia excretion and glutamine storage in littoral Oniscidea (Crustacea: Isopoda): testing tidal and circadian models

A key evolutionary development facilitating land colonization in terrestrial isopods (Isopoda: Oniscidea) is the intermittent liberation of waste nitrogen as volatile ammonia. Intermittent ammonia release exploits glutamine (Gln) as an intermediary nitrogen store. Here, we explore the relationship between temporal patterns of ammonia release and Gln accumulation in three littoral oniscideans from Southern California. Results are interpreted in terms of water availability, habitat, activity patterns, and ancestry. A two-way experimental design was used to test whether ammonia excretion and Gln accumulation follow a tidal or diel periodicity. Ammonia excretion was studied in the laboratory using chambers with or without available seawater and using an acid trap to collect volatile ammonia. Ligia occidentalis releases ammonia directly into seawater and accumulates Gln during low tide (48.9 ± 6.5 μmol g^?1 at low tide, 24.1 ± 3.0 μmol g^?1 at high tide), indicating that excretion is tidally constrained. Alloniscus perconvexus and Tylos punctatus can excrete ammonia directly into seawater or utilize volatilization. Both species burrow in sand by day and show a diel excretory pattern, accumulating Gln nocturnally (31.8 ± 2.7 μmol g^?1 at dawn and 21.8 ± 2.3 μmol g^?1 at dusk for A. perconvexus; 85.7 ± 15.1 μmol g^?1 at dawn and 25.4 ± 2.9 μmol g^?1 at dusk for T. punctatus) and liberating ammonia diurnally. Glutaminase shows higher activity in terrestrial (0.54–0.86 U g^?1) compared to intertidal (0.25–0.31 U g^?1) species, consistent with the need to generate high PNH₃ for volatilization. The predominant isoform in Armadillidium vulgare is phosphate dependent and maleate independent; phosphate is a plausible regulator in vivo.