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

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

Thermal and oxygen conditions during development cause common rough woodlice (Porcellio scaber) to alter the size of their gas-exchange organs

Terrestrial isopods have evolved pleopodal lungs that provide access to the rich aerial supply of oxygen. However, isopods occupy conditions with wide and unpredictable thermal and oxygen gradients, suggesting that they might have evolved adaptive developmental plasticity in their respiratory organs to help meet metabolic demand over a wide range of oxygen conditions.To explore this plasticity, we conducted an experiment in which we reared common rough woodlice (Porcellio scaber) from eggs to maturation at different temperatures (15 and 22 °C) combined with different oxygen levels (10% and 22% O₂). We sampled animals during development (only females) and then examined mature adults (both sexes). We compared woodlice between treatments with respect to the area of their pleopod exopodites (our proxy of lung size) and the shape of Bertalanffy’s equations (our proxy of individual growth curves).Generally, males exhibited larger lungs than females relative to body size. Woodlice also grew relatively fast but achieved a decreased asymptotic body mass in response to warm conditions; the oxygen did not affect growth. Under hypoxia, growing females developed larger lungs compared to under normoxia, but only in the late stage of development. Among mature animals, this effect was present only in males. Woodlice reared under warm conditions had relatively small lungs, in both developing females (the effect was increased in relatively large females) and among mature males and females.Our results demonstrated that woodlice exhibit phenotypic plasticity in their lung size. We suggest that this plasticity helps woodlice equilibrate their gas exchange capacity to differences in the oxygen supply and metabolic demand along environmental temperature and oxygen gradients. The complex pattern of plasticity might indicate the effects of a balance between water conservation and oxygen uptake, which would be especially pronounced in mature females that need to generate an aqueous environment inside their brood pouch.     

Carbon-based secondary compounds in the lichen Hypogymnia physodes deter detrivorous woodlice

Woodlice are not widely recognized as lichen-feeding invertebrates. We sought to discover whether the woodlouse, Porcellio scaber, could feed on the lichen Hypogymnia physodes and if the lichen carbon-based secondary compounds CBSCs would reduce grazing. We cut lichen thalli in two pieces, one was non-destructively rinsed in acetone to remove CBSCs; the other served as a control. Both pieces were fed to woodlice in a choice experiment. The CBSC concentration of individual thalli ranged from 3 to 19%. The woodlice grazed all pieces, but preferred the acetone-rinsed pieces, depending on the amount of CBSCs present in the non-extracted counterpart. The woodlice were not deterred from feeding on samples with CBSC concentrations ≤5%, which corresponded to natural contents in shade-adapted thalli. This suggested that P. scaber tolerates this amount of compounds at least in the short-term. In conclusion, P. scaber can feed on H. physodes, but CBSCs deter them from feeding.     

Does temperature and oxygen affect duration of intramarsupial development and juvenile growth in the terrestrial isopod Porcellio scaber (Crustacea,Malacostraca)?

According to the temperature-size rule (TSR), ectotherms developing under cold conditions experience slower growth as juveniles but reach a larger size at maturity. Whether temperature alone causes this phenomenon is unknown, but oxygen limitation can play a role in the temperature-size relationship. Oxygen may become limited under warm conditions when the resulting higher metabolism creates a greater demand for oxygen, especially in larger individuals. We examined the independent effects of oxygen concentration (10% and 22% O₂) and temperature (15 °C and 22 °C) on duration of ontogenic development, which takes place within the maternal brood pouch (marsupium), and juvenile growth in the terrestrial isopod common rough woodlouse (Porcellio scaber). Individuals inside the marsupium undergo the change from the aqueous to the gaseous environment. Under hypoxia, woodlice hatched from the marsupium sooner, but their subsequent growth was not affected by the level of oxygen. Marsupial development and juvenile growth were almost three times slower at low temperature, and marsupial development was longer in larger females but only in the cold treatment. These results show that temperature and oxygen are important ecological factors affecting developmental time and that the strength of the effect likely depends on the availability of oxygen in the environment.     

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.     

Predatory Versatility in Females of the Scorpion <Emphasis Type="Italic">Bothriurus bonariensis</Emphasis> (Scorpiones: Bothriuridae): Overcoming Prey with Different Defensive Mechanisms

Scorpions are dominant predators in some environments. Nevertheless, most studies of predatory behavior in scorpions have focused on diet composition whereas some other relevant aspects, such as predatory strategy, have been poorly explored. Herein we evaluate the prey acceptance and predatory strategy of the scorpion Bothriurus bonariensis against sympatric prey with different defenses. As prey, we selected earwigs (Forficula cf. auricularia) which use pincer-like defensive appendages, hard-bodied isopods (Armadillium vulgare) known for their conglobation defensive strategy, soft bodied isopods (Porcellio cf. scaber), which secrete noxious substances as defense mechanisms, cockroaches with limited defensive mechanisms (Blatta cf. orientalis.) and spiders (Lycosa cf. poliostoma) which possess venomous fangs. Prey were offered to 21 adults of B. bonariensis in random order until all prey had been offered to all scorpions. Prey consumption and the number of attempts needed for capture were recorded. We also evaluated the effect of sting use on immobilization time as well as the prey capture strategies on the most consumed prey. We found that despite using a similar number of attempts for capturing all prey, spiders and armadillid isopods were less consumed than other prey. Immobilization times were longer for earwigs than for armadillid isopods and cockroaches. Scorpions used alternative predatory strategies against these aforementioned prey, although the stinger was used against all of them. These results show that scorpions are able to use different predatory strategies which might allow them to include prey with diverse defensive strategies in their diet.     

Suitability of woodlice prey for generalist and specialist spider predators: a comparative study

1. Predators select a prey according to its energetic and nutritional composition. Generalist predators avoid, whereas specialists often specialise on well‐defended prey. The aim of this study was to find the suitability of woodlice prey for generalist and specialist predators by comparing their handling efficiency. 2. Laboratory experiments were performed in which specialist and generalist predators were reared on monotypic diets comprising one or other of two woodlice species that differ in their defensive strategies: rollers (Armadillidium) and clingers (Porcellio). A control group was reared on a mixture of arthropods (excluding woodlice). Three spider predators were used that differ in their adaptations to deal with woodlice prey: a woodlice specialist, Dysdera crocata; an oligophagous generalist, Pholcus phalangioides, that also captures woodlice; and a euryphagous generalist, Tegenaria domestica, that does not feed on woodlice. The frequency of capture was recorded and various fitness parameters were measured, namely survival, growth rate, and ontogenetic development. 3. It was found that the specialist, D. crocata, performed best on the Porcellio diet, and similarly well on Armadillidium and mixed diets. The two generalists, P. phalangioides and T. domestica, had poor performance on both woodlice diets but performed well on the mixed diet. 4. The results show that woodlice are unsuitable prey for both oligophagous and euryphagous generalist predators.     

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.     

Behavioral Adaptations of Terrestrial Isopods

In their response to environmental stimuli, terrestrial isopodsshow various trends that are correlated with their ecology andphysiology. With the transition from sea to the littoral zone (Ligia), orientationto light changes from positive to negative. Yet, since theseisopods are positively hygrokinetic even at very high humidities,their hygroreaction is of greater significance than their photoreaction. In isopods from mesic habitats (Oniscus, Porcellio, Armadillidium)photoreaction becomes of less significance than in littoralspecies, until in some species it reverts to positive (Armadillidium).Sometimes the positive photoreaction occurs only at high temperatures(Porcellio), a pattern of behavior correlated with thermoregulationby evaporative cooling. Similarly, in mesic species the responseto humidity becomes less significant than in littoral species,resuming importance mainly when the isopods become dehydrated(Armadillidium). Finally, in isopods from xeric habitats in semi-arid and desertregions (Armadillo, Venezillo), photoreaction is strongly negativeexcept in Hemilepistus at lower temperatures. All of these isopodsare positively hygrokinetic only at low humidities and are stronglynegatively thermoactive, indicating a drop in activity at hightemperatures. The photonegative response in these isopods isstronger than the hygroreaction.     

Body shape in terrestrial isopods: A morphological mechanism to resist desiccation?

Woodlice are fully terrestrial crustaceans and are known to be sensitive to water loss. Their half‐ellipsoidal shapes represent simple models in which to investigate theoretical assumptions about organism morphology and rates of exchange with the environment. We examine the influence of surface area and mass on the desiccation rates in three eco‐morphologically different species of woodlice: Oniscus asellus, Porcellio scaber, and Armadillidium vulgare. Our analysis indicates that the rate of water loss of an individual depends on both the initial weight and the body surface area. Interspecific and intraspecific analyses show that the mass‐specific water loss rate of a species decreases along with the ratio of surface area to volume. In particular, we show that body shape explains the difference in mass‐specific water loss rates between A. vulgare and P. scaber. This observation also explains several known ecological patterns, for example, the distribution and survivorship of individuals. However, in addition to body size and shape, water loss in terrestrial isopods depends also on the coefficient of permeability (i.e., a measure of water loss rate per surface unit), which is high in O. asellus and lower (and at similar levels) in P. scaber and A. vulgare. We discuss morphological, physiological, and behavioral aspects of water loss avoidance in terrestrial isopods. J. Morphol. 276:1283–1289, 2015. © 2015 Wiley Periodicals, Inc.     

Determination of benzo(a)pyrene in isopods (Porcellio scaber Latr.) exposed to contaminated food

• 1.1. A method is presented for the determination of the polycyclic aromatic hydrocarbon benzo(a)pyrene (BaP) in the isopod Porcellio scaber, using reversed-phase HPLC with fluorescence detection.
• 2.2. This technique has a detection limit for BaP in P. scaber of approximately 3.2 ng g⁻¹ fresh weight.
• 3.3. BaP was assimilated from food by P. scaber.
• 4.4. After four weeks of ad libitum feeding on BaP-contaminated food, concentrations in the isopods were approximately 30–40 times lower than those in the food.
• 5.5. Male and female isopods did not differ in BaP concentration. Variation among males seemed to be much higher than among females.

     

Tonic immobility in 12 elasmobranchs: Use as an aid in captive husbandry

Tonic immobility (TI), also known as animal hypnosis, has been observed in a wide variety of taxa and reported in all vertebrate classes with the exception of Agnatha. To date, TI has been reported in six species of elasmobranchs. Preliminary results are presented here for five species of galeomorph sharks, one species of squalomorph shark, and six species of batoids. Tonic immobility was induced in the leopard shark. Triakis semifasciata; the whitetip reef shark, Triaenodon obesus; the blacktip reef shark, Carcharhinus melanopterus; the Caribbean reef shark, Carcharhinus perezi; the swellshark, Cephaloscyllium ventriosum; the California round ray, Urolophus halleri; the shovelnose guitarfish, Rhinobatos productus; the clearnose skate. Raja eglanteria; the cownose ray, Rhinoptera bonasus; and the southern stingray, Dasyatis americana. The broadnose sevengill shark, Notorynchus cepedianus and the yellow stingray, Urolophus jamaicensis failed to exhibit the tonic immobility response, but only one individual of each species was tested. The average induction time ranged from 16.7 sec in the shovelnose guitarfish to 45.7 sec in the clearnose skate. Average duration times ranged from 34.3 sec in the clearnose skate to 274.0 sec in the Caribbean reef shark. Depending upon the species involved, TI has been used as an aid in a few husbandry and medical procedures in captive elasmobranches at the National Aquarium in Baltimore. These procedures have included gross examination, measuring lengths, tube feeding, and drawing blood via caudal venipuncture. Using tonic immobility during these procedures is beneficial as once induced, the subject's struggling is minimal and usually requires little restraint. © 1994 Wiley-Liss, Inc.     

Anti-predator behaviour depends on male weapon size

Tonic immobility and escape are adaptive anti-predator tactics used by many animals. Escape requires movement, whereas tonic immobility does not. If anti-predator tactics relate to weapon size, males with larger weapons may adopt tonic immobility, whereas males with smaller weapons may adopt escape. However, no study has investigated the relationship between weapon size and anti-predator tactics. In this study, we investigated the relationship between male weapon size and tonic immobility in the beetle Gnathocerus cornutus. The results showed that tonic immobility was more frequent in males with larger weapons. Although most studies of tonic immobility in beetles have focused on the duration, rather than the frequency, tonic immobility duration was not affected by weapon size in G. cornutus. Therefore, this study is the first, to our knowledge, to suggest that the male weapon trait affects anti-predator tactics.     

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.     

High Repeatability of Anti-Predator Responses and Resting Metabolic Rate in a Beetle

Measures of repeatability are essential for understanding behavioral consistency and individual differences in behavior, i.e. animal personalities. We studied anti-predator responses of the yellow mealworm beetle (Tenebrio molitor) and performed behavioral tests in plastic containers representing a typical laboratory environment of T. molitor. Behavioral tests were repeated in Eppendorf test tubes where we also measured resting metabolic rate (RMR). Results show that the response latency to a threatening/startling stimulus, and the total time spent in the state of tonic immobility, correlated across the tests. The behavioral responses were repeatable and RMR covaried phenotypically with personality: we found a negative correlation between response latency time and time spent immobile, a positive correlation between response latency and RMR, and a negative correlation between RMR and total time spent immobile. These correlations were also similar across trials performed in the Eppendorf test tubes and the plastic containers.     

Adaptation to cadmium in three populations of the isopod Porcellio scaber

• 1.1. First-generation laboratory animals of three populations of the isopod Porcellio scaber, collected from a reference wood, a zinc smelter area and a lead mine site, were compared with respect to effects of Cd.
• 2.2. All populations reacted differently to Cd-contaminated food: increased Cd concentrations in the food resulted in decreased consumption and growth for the reference isopods; mine isopods were not affected by Cd and for the smelter animals Cd stimulated growth at an intermediate concentration.
• 3.3. Since Cd concentrations in the isopod did not differ between populations, adaptation is probably based on an increased detoxification capacity.
• 4.4. The assimilation of Cd did not affect the Cu or Zn content of the isopods although the adapted isopods regulated their Cu content on a lower level than reference isopods.

     

Genetic trade-off between abilities to avoid attack and to mate: a cost of tonic immobility

Consistent individual differences in correlated behaviours across contexts or situations, that is, behavioural syndromes, have recently been identified as an important factor shaping the evolution of behavioural traits, because of their potential for explaining trade-offs in behavioural responses. We examined a genetic link between abilities to mate and to avoid predation from the viewpoint of two genetically correlated behavioural traits; tonic immobility (TI), which is considered to be an antipredator behaviour, and activity levels in the red flour beetle, Tribolium castaneum. Males derived from two strains artificially selected for divergent durations of TI were used in the present study: the L strain (with longer duration and higher frequency of TI) and the S strain (shorter duration and lower frequency of TI). We found that males of the L strain had higher survival rates in predatory environments than those of the S strain, and lower mating success even in predator-free environments. To our knowledge, this is the first empirical study showing a genetic trade-off between abilities to mate and to avoid predation in relation to behavioural syndromes, using individuals exhibiting different behavioural strategies.     

Metal binding compounds in hepatopancreas and haemolymph of porcellio scaber (isopoda) from contaminated and reference areas

1. In order to evaluate the role of metal-binding proteins in the tolerance mechanism of Porcellio scaber to heavy metals, a comparative study was made using isopods from three locations: a zinc-lead mine (Plombiéres), a zinc smelter (Budel) and a reference wood (Spanderswoud). The Cu, Zn and Cd concentrations and the protein composition were determined in the haemolymph and hepatopancreas from the isopods.2. A constant Cu/Zn molar ratio of about 5 was found in the haemolymph of all populations and no correlation was found between hepatopancreas and haemolymph Cu and Zn content.3. Using fast-performance liquid chromatography (FPLC), most of the haemolymph Cu and Zn appeared to be associated with a single UV absorbing peak corresponding with an apparent molecular weight of ± 70 kD; this peak is probably the monomer of hemocyanin.4. The hepatopancreas Zn and Cd concentration were elevated compared to the hepatopancreas of the smelter and mine isopods; after homogenization and centrifugation 70–80% of the metals were found in the supernatant.5. In all populations the hepatopancreas Cu-, Zn- and Cd-binding compounds eluted in separate peaks of low molecular weight, suggesting the absence of an MT-like compound in Porcellio scaber.6. The similarity of the protein profiles in haemolymph, and the similar distribution of the metals over the fractions in haemolymph and hepatopancreas suggests that inducible metal binding compounds are not involved in metal tolerance differences between populations.     

Effects of thermal and oxygen conditions during development on cell size in the common rough woodlice Porcellio scaber

During development, cells may adjust their size to balance between the tissue metabolic demand and the oxygen and resource supply: Small cells may effectively absorb oxygen and nutrients, but the relatively large area of the plasma membrane requires costly maintenance. Consequently, warm and hypoxic environments should favor ectotherms with small cells to meet increased metabolic demand by oxygen supply. To test these predictions, we compared cell size (hindgut epithelium, hepatopancreas B cells, ommatidia) in common rough woodlice (Porcellio scaber) that were developed under four developmental conditions designated by two temperatures (15 or 22°C) and two air O₂ concentrations (10% or 22%). To test whether small‐cell woodlice cope better under increased metabolic demand, the CO₂ production of each woodlouse was measured under cold, normoxic conditions and under warm, hypoxic conditions, and the magnitude of metabolic increase (MMI) was calculated. Cell sizes were highly intercorrelated, indicative of organism‐wide mechanisms of cell cycle control. Cell size differences among woodlice were largely linked with body size changes (larger cells in larger woodlice) and to a lesser degree with oxygen conditions (development of smaller cells under hypoxia), but not with temperature. Developmental conditions did not affect MMI, and contrary to predictions, large woodlice with large cells showed higher MMI than small woodlice with small cells. We also observed complex patterns of sexual difference in the size of hepatopancreatic cells and the size and number of ommatidia, which are indicative of sex differences in reproductive biology. We conclude that existing theories about the adaptiveness of cell size do not satisfactorily explain the patterns in cell size and metabolic performance observed here in P. scaber. Thus, future studies addressing physiological effects of cell size variance should simultaneously consider different organismal elements that can be involved in sustaining the metabolic demands of tissue, such as the characteristics of gas‐exchange organs and O₂‐binding proteins.     

Solar ultraviolet radiation alters alder and birch litter chemistry that in turn affects decomposers and soil respiration

Solar ultraviolet (UV)-A and UV-B radiation were excluded from branches of grey alder (Alnus incana) and white birch (Betula pubescens) trees in a field experiment. Leaf litter collected from these trees was used in microcosm experiments under laboratory conditions. The aim was to evaluate the effects of the different UV treatments on litter chemical quality (phenolic compounds, C, N and lignin) and the subsequent effects of these changes on soil fauna and decomposition processes. We measured the decomposition rate of litter, growth of woodlice (Porcellio scaber), soil microbial respiration and abundance of nematodes and enchytraeid worms. In addition, the chemical quality of woodlice feces was analyzed. The exclusion of both UV-A and UV-B had several effects on litter chemistry. Exclusion of UV-B radiation decreased the C content in litter in both tree species. In alder litter, UV exclusion affected concentration of phenolic groups variably, whereas in birch litter there were no significant differences in phenolic compounds. Moreover, further effects on microbial respiration and chemical quality of woodlice feces were apparent. In both tree species, microbial CO₂ evolution was lower in soil with litter produced under exclusion of both UV-A and UV-B radiation when compared to soil with control litter. The N content was higher in the feces of woodlice eating alder litter produced under exclusion of both UV-A and UV-B compared to the control. In addition, there were small changes in the concentration of individual phenolic compounds analyzed from woodlice feces. Our results demonstrate that both UV-A and UV-B alter litter chemistry which in turn affects decomposition processes.