Consumer strategies of terrestrial gastropods and isopods

Summary Morphological, physiological and ecological evidence is used to show that terrestrial gastropods and isopods, although both can be considered as primary consumers, deal quite differently with the vegetabilic matter they use as food. Gastropods are both efficient digesters and assimilators whereas isopods are efficient digesters but usually inefficient assimilators. This combination may require the isopods to turn to coprophagy as a means of recovering some of the products of digestion that they had been unable to assimilate during the first passage of food through the gut. Furthermore, the faeces of isopods may contain dissolved nutrients and digestive enzymes that could be distributed through various routes of the food web of which these animals are parts.Supported by the Fonds zur Förderung der wissenschaftlichen Forschung in Österreich, project no. 2851     

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.     

Physiology of terrestrial isopods

• 1.1. This article reviews the physiology of oniscidean isopods, a group of terrestrial crustaceans known commonly as woodlice or sowbugs.
• 2.2. The oniscideans are represented by several hundred species in 34 families and occupy habitats ranging from sea beach to woodland, grassland and desert.
• 3.3. The widespread interest in woodlice stems, in part, from their evolutionary transition from marine to terrestrial habit directly over sea beaches. Representative stages of this evolutionary transition are extant within the oniscidean group.
• 4.4. Water and water relations have featured prominently in the accession to land by woodlice; consequently, these topics have been the focus of much historical and recent research work. The present review builds on a strong foundation of behavioural research on water relations and explores the evolutionary success of these unique crustaceans from a physiological point of view, emphasizing recently published work.
• 5.5. Topics include gas exchange and effects on VO₂, marsupial adaptations, water-vapour absorption, ammonia excretion, moulting and its neuroendocrine control, nutrition and osmotic regulation

     

The terrestrial isopods (Crustacea) of Aldabra

Among a collection of terrestrial isopods from Aldabra were 13 species, six of which are new: Littorophiloscia aldabrana, Philoscina insularis, Trichorhina triocellata, Nagurus kensleyi, Pseudodiploexochus cuspidatus and Venezillo pseudoparvus. Alloniscus pigmentatus Budde-Lund and Tura angusta Budde-Lund are re-described and figured. The taxonomy of six species of Alloniscus Dana from the Indian Ocean is discussed and Alloniscus nacreus Collinge from Madagascar is illustrated. The species Armadillo parvus Budde-Lund and Sphaerillo collaris Budde-Lund are transferred to the genus Venezillo Verhoeff. The distribution of all the species is given together with the composition of the oniscidean fauna of Aldabra.     

Sheltering behavior of terrestrial isopods in grasslands

Abstract. The hypotheses that the sheltering behavior of four species of terrestrial isopods varies in relation to differences in their morphological, physiological, and behavioral adaptations to the terrestrial environment were tested using artificial refugia together with independent estimates of density to derive an index of sheltering activity. (1) Porcellio scaber sheltered significantly more than Platyarthrus hoffmannseggi, Armadillidium vulgare , or Philoscia muscorum , which sheltered the least. (2) There was a decline in the sheltering index (SI) for all four species after the breeding season, continuing through to the autumn and remaining low throughout the winter. (3) Changes in the sheltering behavior of each species in relation to changes in environmental conditions were used to interpret known differences in the position and breadth of their resource utilization curves along a gradient of rabbit grazing intensity. (4) Porcellio scaber sheltered more where the soil was more calcareous, P. muscorum more under the shade of trees, and both P. muscorum and A. vulgare more in grazed than in ungrazed swards. (5) Sheltering behavior was found to be positively correlated to both rainfall and soil temperature the day before sampling for A. vulgare but negatively to rainfall for P. muscorum. There was a positive relationship between the SI for P. scaber and daily air temperature range. (6) Variations in the sheltering behavior of these four species of terrestrial isopod are discussed in the context of their foraging and digestive strategies and in relation to their morphological, physiological, and behavioral adaptations to the terrestrial environment.     

Diversity of terrestrial isopods in the northern Tunisian wetlands

To evaluate the influence of wetland types on the distribution of terrestrial isopods, species richness, relative abundance and diversity indices were studied in the supralittoral zone of 95 wetlands in the north‐western of Tunisian dorsal, belonging to six types: lagoon, hill reservoir, river, dam, lake and sebkha. We tested the following hypothesis: (i) is isopod diversity influenced by wetland types? (ii) is isopod diversity influenced by bioclimatic zones? and (iii) what are the environmental factors influencing isopod distribution? A total of 3255 individuals belonging to twenty species of terrestrial isopods were captured. Species richness differs significantly between wetland types. A highly significant positive relationship between species richness and both humidity and altitudinal gradient was described. The dendrogram of similarities showed a divergence of the lagoons compared to the remaining wetland types.     

Molecular evolution of the androgenic hormone in terrestrial isopods

In crustaceans, the androgenic gland (AG), thanks to the synthesis of the androgenic gland hormone (AGH), controls the differentiation of the primary and secondary male sexual characters. In this study, we amplified 12 new AGH cDNAs in species belonging to five different families of the infra-order Ligiamorpha of terrestrial isopods. Putative essential amino acids for the production of a functional AGH protein exhibit signatures of negative selection and are strictly conserved including typical proteolytic cleavage motifs, a putative N-linked glycosylation motif on the A chains and the eight Cys positions. An insulin-like growth factor motif was also identified in Armadillidium AGH sequences. The phylogenetic relationships of AGH sequences allowed one to distinguish two main clades, corresponding to members of the Armadillidiidae and the Porcellionidae families which are congruent with the narrow specificity of AG heterospecific grafting. An in-depth understanding of the regulation of AGH expression would help deciphering the interaction between Wolbachia, widespread feminizing endosymbiotic bacteria in isopods, and the sex differentiation of their hosts.     

Patterns of taxonomic diversity among terrestrial isopods

The publication of the world catalog of terrestrial isopods some ten years ago by Schmalfuss has facilitated research on isopod diversity patterns at a global scale. Furthermore, even though we still lack a comprehensive and robust phylogeny of Oniscidea, we do have some useful approaches to phylogenetic relationships among major clades which can offer additional insights into isopod evolutionary dynamics. Taxonomic diversity is one of many approaches to biodiversity and, despite its sensitiveness to biases in taxonomic practice, has proved useful in exploring diversification dynamics of various taxa. In the present work, we attempt an analysis of taxonomic diversity patterns among Oniscidea based on an updated world list of species containing 3,710 species belonging to 527 genera and 37 families (data till April 2014). The analysis explores species diversity at the genus and family level, as well as the relationships between species per genera, species per families, and genera per families. In addition, we consider the structure of isopod taxonomic system under the fractal perspective that has been proposed as a measure of a taxon’s diversification. Finally, we check whether there is any phylogenetic signal behind taxonomic diversity patterns. The results can be useful in a more detailed elaboration of Oniscidea systematics.     

Patterns in the release of gaseous ammonia by terrestrial isopods

Summary In the fall and in early spring P. scaber and O. asellus released gaseous ammonia in the form of more or less regularly spaced bursts. In the spring about twice as much ammonia was released by O. asellus than in the fall. In late spring and summer, however, both species released ammonia in a rhythmic fashion, with a maximum at noon and early in the afternoon, and a minimum early at night. Sometimes a second maximum occurred late at night.In O. asellus the addition of a moist substrate to the reaction chamber shifted the maximum of the release of ammonia from noon to late night and early morning.Fed specimens of P. scaber released only about one-third as much NH₃ as fasting animals and—at least in constant darkness—with a period of much reduced amplitude.It is concluded that the rhythmical release of ammonia is inversely related to the pattern of locomotory activity of these animals. This would implicate mechanisms that regulate either the production or the release of ammonia in such a way that the maximum occurs at a time when the animals' production of energy is at a minimum and when they are protected against loss of water by sitting in their moist retreats.The work at Innsbruck was supported by the Fonds zur Förderung der wissenschaftlichen Forschung of Austria.     

Widespread Wolbachia infection in terrestrial isopods and other crustaceans

Wolbachia bacteria are obligate intracellular alpha-Proteobacteria of arthropods and nematodes. Although widespread among isopod crustaceans, they have seldom been found in non-isopod crustacean species. Here, we report Wolbachia infection in fourteen new crustacean species. Our results extend the range of Wolbachia infections in terrestrial isopods and amphipods (class Malacostraca). We report the occurrence of two different Wolbachia strains in two host species (a terrestrial isopod and an amphipod). Moreover, the discovery of Wolbachia in the goose barnacle Lepas anatifera (subclass Thecostraca) establishes Wolbachia infection in class Maxillopoda. The new bacterial strains are closely related to B-supergroup Wolbachia strains previously reported from crustacean hosts. Our results suggest that Wolbachia infection may be much more widespread in crustaceans than previously thought. The presence of related Wolbachia strains in highly divergent crustacean hosts suggests that Wolbachia endosymbionts can naturally adapt to a wide range of crustacean hosts. Given the ability of isopod Wolbachia strains to induce feminization of genetic males or cytoplasmic incompatibility, we speculate that manipulation of crustacean-borne Wolbachia bacteria might represent potential tools for controlling crustacean species of commercial interest and crustacean or insect disease vectors.     

Post-parturial reproduction in terrestrial isopods: a partial review

This review deals with some aspects of terrestrial isopod reproduction including breeding season, breeding periods, patterns and strategies, parturition, number and size of broods and mancae. Reproductive period is described by the exact dates (i.e. season) marsupial females were collected in the field, and the duration of the breeding period. The information for both aspects was generally obtained through field work by observing marsupial females. Two reproductive patterns are used by terrestrial isopods, either a discrete (i.e. seasonal) or a continuous (i.e. non-seasonal) pattern. The discrete pattern can be either annual when females breed once a year, or they can breed biannually or multi-annually (two or more times during the year). This conclusion is based generally on observing marsupial females in the field. Therefore, this information does not apply to the reproductive pattern of the individual female since a female may use either or both patterns, i.e. seasonal and continuous. Only by raising individual females singly (with a male) can this point be clarified. This way, the breeding strategy of the same individual female can be studied. The subject is discussed and reviewed based on my research data.     

The ultrastructure of the androgenic gland in Porcellio scaber Latr. (terrestrial isopods)

Summary This paper presents the normal ultrastructural features of the androgenic gland in Porcellio scaber. It describes the changes in the organelles of its cells through the course of the secretory cycle, which terminates with the regression and destruction of these holocrine glandular cells. As products of this activity, the electron-opaque bodies (granules, lysosomes, agglomerates) and clear substances accumulate in the cytoplasm. With the destruction of the cell membrane, the entire cell content passes into the spaces of the haemocoele. The morphological modifications of the mitochondria and rough endoplasmic reticulum are the most striking changes.

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Résumé Les auteurs présentent, dans ce travail, les aspects ultrastructuraux normaux de la glande androgène chez l'oniscoïde Porcellio scaber. On montre, par des phases successives, les modifications morpho-fonctionnelles des organites cellulaires jusqu'à la fin du cycle sécrétoire, qui finit par la dégradation et la destruction des cellules glandulaires, dont la fonction est de type holocrin. Comme produits de cette activité, des corps éléctrono-opaques (grains, agglomerats, lysosomes) et des substances claires apparaissent dans le cytoplasme. Par la destruction de la membrane plasmique, tout le contenu cellulaire est éliminé dans les espaces haemocoeliens, soit par écoulement soit par fragments. Le RE et le chondriome subissent les modifications les plus spectaculaires.

     

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.     

Tonic immobility in terrestrial isopods: intraspecific and interspecific variability

Many arthropods, including terrestrial isopods, are capable of entering a state of tonic immobility upon a mechanical disturbance. Here we compare the responses to mechanical stimulation in three terrestrial isopods Balloniscus glaber, Balloniscus sellowii and Porcellio dilatatus. We applied three stimuli in a random order and recorded whether each individual was responsive (i.e. showed tonic immobility) or not and the duration of the response. In another trial we related the time needed to elicit tonic immobility and the duration of response of each individual. Balloniscus sellowii was the least responsive species and Porcellio dilatatus was the most, with 23% and 89% of the tested individuals, respectively, being responsive. Smaller Balloniscus sellowii were more responsive than larger individuals. Porcellio dilatatus responded more promptly than the Balloniscus spp. but it showed the shortest response. Neither sex, size nor the type of stimulus explained the variability found in the duration of tonic immobility. These results reveal a large variability in tonic immobility behavior, even between closely related species, which seems to reflect a species-specific response to predators with different foraging modes.     

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.     

Effects of terrestrial isopods on the decomposition of woodland leaf litter

Summary The indirect contribution terrestrial isopods make to decomposition processes by stimulating microbial activites has been quantified in laboratory experiments. The extent to which microbial metabolism is enhanced as a result of the passage of Betula pendula leaf litter through the alimentary system of isopods was measured for both freshly fallen and decayed leaves. Faeces derived from 1 g freshly fallen litter lost 75 mg g^-1 D.W. more than did intact leaves, as a result of enhanced microbial metabolism. Faeces derived from 1 g of previously decayed leaves, which were shown to be the preferred food of isopods, lost only 17.5 mg g^-1 D.W. more than intact decaying leaves. The isopod's direct contribution to soil metabolism was calculated to be 151 mg and 138 mg g^-1 litter ingested when fed on freshly fallen and decayed leaves respectively. It is concluded that the physical and chemical changes in the leaf substrate which result from fragmentation and digestion by isopods do not necessarily accelerate the subsequent decomposition of the litter very significantly. Fungal propagule density was 3.2x and 3.6x higher in faeces derived from freshly fallen and decayed leaves respectively than in the intact litter. Numbers of viable bacteria were correspondingly 126x and 34x higher in faeces than in the freshly fallen and the decayed leaves. Levels of microbial inhibitors were lower in the faeces than in the leaves but levels of free amino acids stayed higher for longer in the faeces than they did in intact litter. In the field the physical removal of litter by the soil macrofauna from surface to deeper and moister microsites may be the most important indirect contribution that they make to decomposition processes.     

Faunistic data and biogeography of terrestrial isopods from Tunisian wetlands

In Tunisia, while wetlands are considered as remarkable habitats for their faunal and floral diversity, few studies on the biogeography and the diversity of terrestrial isopods were performed. To fill this gap, we carried out a field study in the supralittoral zone of 146 Tunisian wetlands belonging to eight types (lagoon, river, lake, sebkha, dam, hill reservoir, beach and chott) and to five bioclimatic zones (humid, subhumid, semi‐arid, arid and Saharan). Field work was carried out in spring 2010. Terrestrial isopods were collected in the morning by hand search each time with the same sampling effort. During the study, 22 species of terrestrial isopods belonging to nine families were collected. Porcellio variabilis, Porcellio laevis, Chaetophiloscia elongata and Armadillidium pelagicum are the most common species identified. From the northern to the southern regions, a gradual decrease in species richness has been shown. The identified species belonged to different biogeographical categories: Mediterranean, Mediterranean‐Atlantic, North Africa with circum‐Sicilian islands, semi‐arid and Saharan species. Some of these species are endemic to Tunisia (Porcellio dominici) or to North Africa (Armadillidium sulcatum, Armadillidium tunisiense, Porcellio marginenotatus and P. variabilis). Terrestrial isopod species differ according to wetland type and bioclimatic zone.     

Traits underpinning desiccation resistance explain distribution patterns of terrestrial isopods

Predicted changes in soil water availability regimes with climate and land-use change will impact the community of functionally important soil organisms, such as macro-detritivores. Identifying and quantifying the functional traits that underlie interspecific differences in desiccation resistance will enhance our ability to predict both macro-detritivore community responses to changing water regimes and the consequences of the associated species shifts for organic matter turnover. Using path analysis, we tested (1) how interspecific differences in desiccation resistance among 22 northwestern European terrestrial isopod species could be explained by three underlying traits measured under standard laboratory conditions, namely, body ventral surface area, water loss rate and fatal water loss; (2) whether these relationships were robust to contrasting experimental conditions and to the phylogenetic relatedness effects being excluded; (3) whether desiccation resistance and hypothesized underlying traits could explain species distribution patterns in relation to site water availability. Water loss rate and (secondarily) fatal water loss together explained 90 % of the interspecific variation in desiccation resistance. Our path model indicated that body surface area affects desiccation resistance only indirectly via changes in water loss rate. Our results also show that soil moisture determines isopod species distributions by filtering them according to traits underpinning desiccation resistance. These findings reveal that it is possible to use functional traits measured under standard conditions to predict soil biota responses to water availability in the field over broad spatial scales. Taken together, our results demonstrate an increasing need to generate mechanistic models to predict the effect of global changes on functionally important organisms.