Armadillidium Vulgare Research Articles

Behavioral pattern of pill bugs revealed in virtually infinite multiple T-maze

A behavior called turn alternation has been studied extensively in terrestrial isopods. This behavior is seen when they alternate their path choice on successive trials of the T-maze test. We made the multiple T-maze device which consists of two turntables with a T-maze mounted on each and examined the behavior of 36 pill bugs (Armadillidium vulgare) that each completed 130 successive T-maze trials. As a result, in addition to turn alternation, turn repetition (turning in the same direction on two successive turns) appeared at a rate of 20%. In the turn sequences, we observed segments consisting of successive turn alternations and defined the number of turn alternations in a segment as the length of it. Cumulative frequency distribution of segment lengths obeyed power law with exponent of 1.76. This result suggests that pill bugs in the multiple T-maze device behaved as Levy walkers which forage in an environment, where resources are unpredictably distributed.

The Effect of Urbanization on Trace Element Concentration and Symmetry of Woodlice (Armadillidium vulgare Latreille, 1804)

Woodlice are top consumers of a three-trophic system (soil, leaf litter, woodlice), and they are closely related to pollutant absorbing surfaces such as soil, leaf litter, and organic matter. We studied the effects of urbanization on trace element concentrations and fluctuating asymmetry of Armadillidium vulgare (Crustacea: Isopoda) individuals in and around Debrecen city, Hungary. Along an urbanization gradient (urban, suburban, and rural areas), trace element concentrations (Ba, Cu, Fe, Mn, Pb, and Zn) of woodlice and bioconcentration factor (BCF) were analyzed. Asymmetry was also measured in metric traits of woodlice: the length of three segments of antennae, the body length, and the width of the 3rd segment of pereon. We found significant differences in Ba and Cu concentration of A. vulgare individuals along the urbanization gradient. The highest Cu concentration was found in woodlice from the urban area and the highest Ba concentration was found in the individuals from the rural area. The Ba concentration was higher in females than in males. The BCF values of Cu indicated that A. vulgare accumulated this element from soil and leaf litter. There was no significant difference in symmetry of the bilateral traits of woodlice along the urbanization gradient based on FA levels. Our results showed that the urbanization had remarkable effect on the Ba and Cu concentration of woodlice which were originated from traffic pollution. At the same time, the anthropogenic activities did not affect the symmetry of the tested traits of A. vulgare individuals.

Genetic variability in populations of the terrestrial isopod Armadillidium vulgare living in soils with different land uses

The Argentine Pampas region is recognized by its high productivity and fertility, which make its soils suitable for agricultural use. However, the intensification of agricultural activities over the last forty years has led to an intense disturbance regime, characterized by an increase in the soil degradation rate. Soil degradation and its relationship with soil fauna communities are crucial issues in resource management. In this study, we investigated the effects of land-use change on the genetic variability of the terrestrial isopod Armadillidium vulgare, chosen as a biological model. The diversity and population genetic structure of this species were analyzed using inter-simple sequence repeat (ISSR)-PCR markers, in three land uses in two localities of Luján, Buenos Aires, Argentina. Genetic variability was high in natural grassland populations and lower in agricultural land uses. Both conventional FST analysis and Bayesian approach for dominant markers showed significant genetic differences between land uses within each locality. The loss of genetic variability and the population genetic structure can be used as indicators of system disturbance. Thus, in the soils studied, the degree of genetic variability of representative populations of the soil fauna can be a good indicator of the disturbance degree.

Aggregative behavior and intraspecific communication mediated by substrate-borne vibrations in terrestrial arthropods: An exploratory study in two species of woodlice

Gregarious behavior and aggregative phenomena among conspecifics in woodlice are thought to be a form of evolutionary adaptation to the terrestrial environment which has given these animals multiple advantages, e.g., against desiccation and predation. The reasons behind these phenomena, however, have not fully been clarified yet. This exploratory study has the aim to assess displacement and aggregation state relatively to the presence of substrate-borne vibrations in two different species of terrestrial isopods. To this goal, a circular arena was used to collect data from adult individuals of Armadillo officinalis, a stridulating species, and Armadillidium vulgare, a non-stridulating species, both exposed and non-exposed to micro-vibrations. Our results showed that exposed individuals of A. officinalis significantly react to micro-vibrations positioning themselves preferentially far from the vibrational source compared to non-exposed individuals of the same species. Furthermore, both the number of aggregates and of isolated subjects significantly increase in the presence of substrate-borne vibrations than in the absence of micro-vibrations. No statistically significant association with substrate-borne vibrations was found for A. vulgare for both placement and number of aggregates and of isolated subjects. Unlike A. vulgare, A. officinalis appears very sensitive to micro-vibrations which seem to represent a source of disturbance or potential danger. Substrate-borne vibrations seem to affect the capability of this species to aggregate leading to a greater number of aggregates and isolated subjects as if animals were a bit disoriented. This behavior might be related to a possible capability of this species to use micro-vibrations for inter- and intraspecific communication.

Roly-Uoly Egg Sacs: Isopods Used as Replacement Egg Sacs by the Wolf SpiderPardosa valens(Araneae: Lycosidae)

Abstract Wolf spider females have the distinctive behaviour of carrying the egg sac attached to the spinnerets. If this egg sac is dislodged, the female will retrieve and reattach it, if possible. However, in some instances, a female may reattach another object of similar size or shape as a replacement for a lost egg sac. Here, I report the first example of an isopod, Armadillidium vulgare, being used as a substitute for a missing egg sac in Pardosa valens Barnes, 1959 from southeastern Arizona.

Investigating the Molecular Genetic Basis of Cytoplasmic Sex Determination Caused by Wolbachia Endosymbionts in Terrestrial Isopods.

In animals, sexual differences between males and females are usually determined by sex chromosomes. Alternatively, sex may also be determined by vertically transmitted intracellular microbial endosymbionts. The best known cytoplasmic sex manipulative endosymbiont is Wolbachia which can, for instance, feminize genetic males into phenotypic females in the terrestrial isopod Armadillidium vulgare. However, the molecular genetic basis of cytoplasmic sex determination is unknown. To identify candidate genes of feminization induced by Wolbachia strain wVulC from A. vulgare, we sequenced the genome of Wolbachia strain wCon from Cylisticus convexus, the most closely related known Wolbachia strain to wVulC that does not induce feminization, and compared it to the wVulC genome. Then, we performed gene expression profiling of the 216 resulting wVulC candidate genes throughout host developmental stages in A. vulgare and the heterologous host C. convexus. We identified a set of 35 feminization candidate genes showing differential expression during host sexual development. Interestingly, 27 of the 35 genes are present in the f element, which is a piece of a feminizing Wolbachia genome horizontally transferred into the nuclear genome of A. vulgare and involved in female sex determination. Assuming that the molecular genetic basis of feminization by Wolbachia and the f element is the same, the 27 genes are candidates for acting as master sex determination genes in A. vulgare females carrying the f element.

Aqueous-based tissue clearing in crustaceans

BackgroundInvestigation of the internal tissues and organs of a macroscopic organism usually requires destructive processes, such as dissection or sectioning. These processes are inevitably associated with the loss of some spatial information. Recently, aqueous-based tissue clearing techniques, which allow whole-organ or even whole-body clearing of small rodents, have been developed and opened a new method of three-dimensional histology. It is expected that these techniques will be useful tools in the field of zoology, in which organisms with highly diverse morphology are investigated and compared. However, most of these new methods are optimized for soft, non-pigmented organs in small rodents, especially the brain, and their applicability to non-model organisms with hard exoskeletons and stronger pigmentation has not been tested.ResultsWe explored the possible application of an aqueous-based tissue clearing technique, advanced CUBIC, on small crustaceans. The original CUBIC procedure did not clear the terrestrial isopod, Armadillidium vulgare. Therefore, to apply the whole-mount clearing method to isopods with strong pigmentation and calcified exoskeletons, we introduced several pretreatment steps, including decalcification and bleaching. Thereafter, the clearing capacity of the procedure was dramatically improved, and A. vulgare became transparent. The internal organs, such as the digestive tract and male reproductive organs, were visible through sclerites using an ordinary stereomicroscope. We also found that fluorescent nuclear staining using propidium iodide (PI) helped to visualize the internal organs of cleared specimens. Our procedure was also effective on the marine crab, Philyra sp.ConclusionsIn this study, we developed a method to clear whole tissues of crustaceans. To the best of our knowledge, this is the first report of whole-mount clearing applied to crustaceans using an aqueous-based technique. This technique could facilitate morphological studies of crustaceans and other organisms with calcified exoskeletons and pigmentation.

Feminizing Wolbachia influence microbiota composition in the terrestrial isopod Armadillidium vulgare

Wolbachia are widespread heritable endosymbionts of arthropods notorious for their profound effects on host fitness as well as for providing protection against viruses and eukaryotic parasites, indicating that they can interact with other microorganisms sharing the same host environment. Using the terrestrial isopod crustacean Armadillidium vulgare, its highly diverse microbiota (>200 bacterial genera) and its three feminizing Wolbachia strains (wVulC, wVulM, wVulP) as a model system, the present study demonstrates that Wolbachia can even influence the composition of a diverse bacterial community under both laboratory and natural conditions. While host origin is the major determinant of the taxonomic composition of the microbiota in A. vulgare, Wolbachia infection affected both the presence and, more importantly, the abundance of many bacterial taxa within each host population, possibly due to competitive interactions. Moreover, different Wolbachia strains had different impacts on microbiota composition. As such, infection with wVulC affected a higher number of taxa than infection with wVulM, possibly due to intrinsic differences in virulence and titer between these two strains. In conclusion, this study shows that heritable endosymbionts such as Wolbachia can act as biotic factors shaping the microbiota of arthropods, with as yet unknown consequences on host fitness.

Estimation of the walking ability of an exotic terrestrial isopod Armadillidium vulgare Latreille by field and laboratory measurements

Estimation of the walking ability of an exotic terrestrial isopod Armadillidium vulgare Latreille by field and laboratory measurements

Predatory risk increased due to egg‐brooding in Armadillidium vulgare (Isopoda: Oniscidea)

AbstractCost of reproduction is associated with a reduction in subsequent survival or future breeding success. A decrease in survival rate of parents during or after reproduction reduces the probability of their future reproduction. However, few studies have demonstrated such survival costs to parents. Females of Armadillidium vulgare hold their eggs in a marsupium and brood these until the young hatch. Caring for eggs in a marsupium seems to place a large burden on brooding females, and it restricts their predator avoidance behaviour. As such, costs of care may increase the mortality rates of brooding females. To reveal the costs of parental care, we examined the effects of egg brooding on behaviour and predation risk. Egg‐brooding females decreased speed of locomotion and rolling duration, and were killed by predators at a higher rate. Our results indicate that egg brooding in A. vulgare has costs in the form of predation risk.

Producing offspring in Armadillidium vulgare: Effects of genetic diversity and inbreeding.

Genetic diversity is known to be correlated to fitness traits, and inbred individuals often display lower values for life history traits. In this study, we attempt to quantify how inbreeding affects such traits in the terrestrial isopod Armadillidium vulgare by performing inbred and non-inbred crosses under laboratory conditions. We estimated genetic characteristics of parents and offspring, and related them to fecundity and fertility measures, as well as offspring growth and survival. Our study shows that a decrease in offspring number might result from mortality around birth, but not to changes in fecundity, fertilization rate, or developmental failure between inbred and non-inbred crosses. More heterozygous females tended to be bigger and had a higher fecundity, which could have implications in mate choice. No effect of inbreeding was detected on offspring growth and survival. These results can be related to previously observed effects of genetic characteristics on mating strategies in A. vulgare, and could shed light on mechanisms of inbreeding avoidance in this species.

Citrus gummosis incidence and role of ants (Lasius grandis) and snails (Helix aspersa) as vectors of the disease in Tunisia

SummarySurveys were conducted between November 2011 and December 2013 to determine the distribution and the incidence of citrus gummosis in Tunisia. Forty‐two citrus orchards in three different citrus areas were surveyed. Symptoms of gummosis were observed in 59.52% of the orchards. The highest incidence was observed in the Cap Bon area. The involvement of some invertebrates in the epidemiology of citrus gummosis was also confirmed. Species of ants (Lasius grandis), snails (Helix aspersa and Rumina decollata) and worms (Armadillidium vulgare) collected from 2012 until 2014 were tested for the presence of Oomycetes. Phytophthora nicotianae and Phytopythium vexans were isolated from the bodies of Lasius grandis and also from bodies and faeces of Helix aspersa. However, no Oomycetes were isolated from the bodies of Rumina decollata and Armadillidium vulgare. In vitro assays, Helix aspersa was fed with P. nicotianae‐ and Ph. vexans‐infected citrus bark showed the existence of those pathogens in 79.1% of the faeces of snails. In vivo assays, snails and ants were able to transmit the pathogens vertically from the base of potted 2‐year‐old trees citrus variety Clementine Mandarin cv. Hernandina, to other parts of the tree.

Males prefer virgin females, even if parasitized, in the terrestrial isopod Armadillidium vulgare.

In many species, males increase their reproductive success by choosing high‐quality females. In natural populations, they interact with both virgin and mated females, which can store sperm in their spermatheca. Therefore, males elaborate strategies to avoid sperm competition. In the terrestrial isopod Armadillidium vulgare, females can store sperm and produce several clutches. Moreover, this species can be parasitized by Wolbachia, which feminizes genetic males, transforming them into functional females. Our study compared attractiveness and mate choice when a male is exposed to both virgin and experienced females (i.e., females who have produced offspring and rested for 6 months), with or without Wolbachia. Our results revealed that males are more attracted to virgin females than experienced females, even if these virgin females are parasitized. Moreover, the chemical analysis highlighted different odors in females according to their reproductive and infection (Wolbachia‐free or vertically Wolbachia‐infected) status. Males attempted copulation more frequently and for longer with virgin females, even if Wolbachia‐infected, while experienced females refused further copulation. The evolutionary consequences of both male choice and female resistance on their fitness are discussed in this study.

Acaulide, an Osteogenic Macrodiolide from Acaulium sp. H-JQSF, an Isopod-Associated Fungus.

Acaulide (1), a macrodiolide with an unprecedented framework, was characterized along with its shunt products-acaulones A (2) and B (3)-from the culture of Acaulium sp. H-JQSF associated with the isopod Armadillidium vulgare. The spiro-linked 14-, 14-, and 6-membered cycles of 1 arise likely from iterative intermolecular Michael addition reactions. Biological evaluation in the prednisolone-induced osteoporotic zebrafish demonstrated that 1 is antiosteoporotic at 0.4 and 2.0 μM.

Life histories and soil water content preferences of sympatric exotic and native terrestrial isopods

AbstractExotic species have negative effects on the ecosystems they enter, but often coexist with native species. Clarifying mechanisms behind the coexistence of native and exotic species is important for evaluating effects of such exotic species on native ecosystems. In Japan, at least seven terrestrial isopod species are considered exotic and some have been found with native species. The mechanisms of their coexistence have never been researched. This study examines the hypothesis that an exotic isopod species, Armadillidium vulgare, and native Mongoloniscus koreanus differ in their life histories and soil water content preferences, and that these differences facilitate their coexistence. Field observation revealed that populations of the two species were stably maintained despite large overlap in their life histories and breeding periods, although A. vulgare showed more variability in some aspects of life history than M. koreanus. Two types of choice experiments were carried out to identify their preferences for soil water content levels. The “alone” experiment, where one individual was used per experimental box, showed that the two species were different in preference for soil water content. However, the “group” experiment, where ten individuals of the two species (five of each species) were used per experimental box, suggested that A. vulgare changed its preference from when it was alone, showing preference similar to that of the M. koreanus individuals in the same box. Thus, we concluded that the two species can coexist at the study site, but that the hypothesized mechanisms for their coexistence were not proven in this study.

Symbiotic Bacteria Influence the Odor and Mating Preference of Their Hosts

In many species, chemical communication is a determining factor in mate choice. Some species use the composition of cuticular compounds to discriminate between potential mates. Moreover, the presence of parasites can also influence mate choice and alter the odor of an individual. In the current study, we tested the effect of the endosymbiont Wolbachia, which is naturally present in the terrestrial isopod Armadillidium vulgare and can induce male feminization in the species. We compared male attraction to different types of females (Wolbachia-free, females naturally infected by Wolbachia, Wolbachia-injected females, and females injected with a bacteria-free suspension). Our behavioral assays revealed that males consistently preferred Wolbachia-free females and that this preference correlates to changes in cuticular compounds. Males also preferred naturally infected females over Wolbachia-injected females. The ability of males to discriminate between females could result in Wolbachia impacting its host phenotype, thus affecting the odor of the host. Female odor is the result of an honest signal that makes it possible for males to discriminate between Wolbachia-infected and non-infected females. The male preference for Wolbachia-free females is adaptive, and long-term studies have demonstrated that such choices confer improved fitness.

Aboveground macrodetritivores and belowground soil processes: Insights on species redundancy

Quantifying the level of overlap between species-specific effects in a given process – i.e. their functional redundancy–remains a central issue in predicting the shape of diversity-productivity or diversity-stability relationships. We compared the indirect effects of six aboveground macro-detritivores on two belowground processes, cellulose decay and nutrient mineralization, in single-species microcosms (n=5) containing standardized substratum, mixed litter, and four individuals of detritivores. In all microcosms, there was an overall increase in phosphate and decrease in nitrate and ammonium over four weeks. Cellulose decay was ≈30%. Compared to fauna-free controls, there were a few noticeable fauna effects: decay was higher in microcosms with Armadillidium vulgare and Porcellio scaber, nitrate immobilization was lower in Cylindroiulus caeruleocinctus microcosms, and ammonium immobilization was lower in A. vulgare and P. scaber microcosms. The multivariate effects were idiosyncratic and related to a high intraspecific variation. Contrary to our expectations, the most noticeable difference was between P. scaber and Trachelipus rathkii. Our results point to redundancy due to high intraspecific variation. It is postulated that, if redundancy arises from high intraspecific variation, upon the loss of species, large population sizes of remaining species from the same functional group might explain positive effects of redundancy on ecosystem resilience.

Changes in turn alternation pattern in response to substrate-borne vibrations in terrestrial isopods

The present study focuses on the relationship existing between the phenomenon of turn alternation and substrate-borne vibrations in woodlice. Armadillo officinalis was utilized as a behavioral model in comparison to Armadillidium vulgare so as to assess its capability of perceiving external vibrations too. A T-maze with multiple exits was used to collect information on the pattern of turn alternation in i) adult individuals of A. officinalis exposed, and ii) not exposed to micro-vibrations, and iii) adult individuals of A. vulgare exposed to micro-vibrations. Turn alternation was assessed as the number of times that an animal turned on the opposite side in the T-maze. Our results showed a statistically significant association between turn alternation pattern and both exposure to micro-vibrations and species of the animals. According to our best-fitting model, A. officinalis not exposed and A. vulgare exposed to substrate-borne vibrations have 97% and 98% lower odds, respectively of being in a higher category of turn alternations compared to a lower category than exposed individuals of A. officinalis. A. officinalis seems to be very reactive to substrate-borne vibrations, unlike A. vulgare. This different reactivity might be related to a more complex defense mechanism developed as an evolutionary adaptation to the xeric environment, and/or to a means of communication mediated by substrate-borne vibrations, like in insects.

Crop Seedling Susceptibility to Armadillidium vulgare (Isopoda: Armadillidiidae) and Ommatoiulus moreletii (Diplopoda: Iulidae).

The isopod, Armadillidium vulgare (Latreille) (Isopoda: Armadillidiidae), and the millipede, Ommatoiulus moreletii (Lucas) (Diplopoda: Iulidae), are increasingly being reported as pests of emerging broadacre crop seedlings in southern Australia. This is thought to be due to the increased adoption of stubble retention practices, leading to increased abundance of these soil-dwelling organisms. Here, we evaluate the propensity of A. vulgare and O. moreletii to damage a range of crop seedlings. Through the combined analysis of a controlled feeding trial and field reports, we show A. vulgare is able to feed on and damage a range of pulses, legumes, cereals, and oilseeds, as emerging seedlings. O. moreletii had a more restricted range of feeding, being limited to lupin, lucerne, and canola in the feeding trial. These results are discussed in the context of developing pest management guidelines for these species.

When GIS zooms in: spatio-genetic maps of multipaternity in Armadillidium vulgare.

Geographic information system (GIS) tools are designed to illustrate, analyse and integrate geographic or spatial data, usually on a macroscopic scale. By contrast, genetic tools focus on a microscopic scale. Because in reality, landscapes have no predefined scale, our original study aims to develop a new approach, combining both cartographic and genetic approaches to explore microscopic landscapes. For this, we focused on Armadillidium vulgare, a terrestrial isopod model in which evolutionary pressures imposed by terrestrial life have led to the development of internal fertilisation and, consequently, to associated physiological changes. Among these, the emergence of internal receptacles, found in many taxa ranging from mammals to arthropods, allowed females to store sperm from several partners, enabling multipaternity. Among arthropods, terrestrial isopods like the polygynandrous A. vulgare present a female structure, the marsupium, in which fertilised eggs migrate and develop into mancae (larval stage). To test our innovative combined approach, we proposed different males to four independent females, and at the end of incubation in the marsupium, we mapped (using GIS methods) and genotyped (using 12 microsatellite markers) all the incubated mancae. This methodology permitted to obtain spatio-genetic maps describing heterozygosity and spatial distribution of mancae and of multipaternity within the marsupial landscape. We discussed the interest of this kind of multidisciplinary approach which could improve in this case our understanding of sexual selection mechanisms in this terrestrial crustacean. Beyond the interesting model-focused insights, the main challenge of this study was the transfer of GIS techniques to a microscopic scale and our results appear so as pioneers rendering GIS tools available for studies involving imagery whatever their study scale.