Sensitivity to photoperiod of the terrestrial isopod Armadillidium vulgare (Latreille) during photoperiodic induction of sexual rest

Summary

The characterization of photoperiodic induction of sexual rest in Armadillidium vulgare females (a cosmopolitan species) shows that the photoperiodic curves relating to the cessation of reproduction are representative of long-days type species. Experiments made on photophase maintenance or reduction show that females are sensitive not only to such reduction but also to its magnitude. Furthermore, the photophase value is relative and depends on previous conditions experienced by the female and there is evidence for the existence of a circannual endogenous cycle in A. vulgare.     

Reproductive phenology of a natural population of Armadillidium pelagicum Arcangeli, 1955 (Isopoda, Oniscidea)

Armadillidium pelagicum, the most abundant species of the genus in Tunisia is endemic to the North of Tunisia and the circumsicilian islands. In the laboratory and under the natural conditions of temperature and photoperiod, virgin females of A. pelagicum exhibit a spontaneous ovarian maturation, followed by a parturial moult. Nevertheless, the onset of reproduction is greatly accelerated by the presence of a male. In fact, mating shortened the lag time (from the beginning of experiment to the parturial moult) by reducing the number of normal moult preceding the first parturial moult and the duration of the preparturial intermoult. In this species, only one mating is enough to ensure the fertility for several egg layings. Otherwise, it has been shown that A. pelagicum has a reproductive period rather than a reproductive activity and that mating females have a longer reproductive period than virgins. Like several species of terrestrial Isopods, the duration of the gestation period is temperature-dependent.     

Photoperiodism and seasonal breeding in aquatic and terrestrial Eumalacostraca

Summary

Seasonal reproduction in Crustacea is synchronized by environmental cues (e.g., temperature and photoperiod). Two types of responses occur: (1) in reptant decapods, short photoperiods and low temperatures are necessary to induce vitellogenesis; (2) in natant decapods and in most peracarids, both high temperatures and long photoperiods promote the onset of reproduction. In this context studies on the biological clocks involved in photoperiodic time measurement were performed on two crustaceans: the ditch shrimp Palaemonetes varians and the woodlouse Armadillidium vulgare, which is distributed worldwide outside polar and intertropical areas. The most important feature of the photoperiodic response curves was the same mean lag time in response to photophase length ≤ 12 h: short photophases delayed breeding but did not prevent it (i.e., “short-day effect”). On the contrary, long photophases promoted the onset of reproduction (i.e., “long-day effect”) differently in P. varians and A. vulgare. In A. vulgare strains the shape of the photoperiodic response curve depended on latitudinal origin. Results of “resonance” experiments provided evidence of involvement of an endogenous circadian component in the photoperiodic clocks of the two species according to the internal coincidence model developed for insects. Seeing that relations between reproduction and moulting were different in the two species, we proposed the hypothesis of an evolutionary change in the transition from the sea to the continental environment.     

Female genitalia,reproductive cycle and sperm storage in Armadillidium vulgare (Crustacea,Isopoda, Oniscidea)

Light and electron microscopic studies that we have published in the past have reported many aspects of the reproductive process in Armadillidium vulgare with particular emphasis on the reconstruction of female genitalia. Together this body of work provides an almost complete, albeit fragmented picture of these processes and include many data on sperm storage and sperm translocation. Females of A. vulgare have a pair of cuticular genitalia in the lumen of the oviduct. For insemination, these genitalia can receive the copulatory organs of males formed by the elongated tips of the first two pleon endopods. During transitions between reproductive (parturial) and non-reproductive (normal, non-parturial) moult cycles the genitalia undergo intriguing structural changes resulting in two types of genitalia. Throughout their reproductive lifetime, either type is reconstructed after each moult depending on the reproductive phase of the female. In this review, we integrate the events that occur during a reproductive cycle with particular emphasis on the genitalia reconstruction and sperm storage, and discuss functional aspects of the genitalia. Thereby, we provide a case model that can be useful for further studies on genitalia diversity and female reproductive strategies in terrestrial isopods.     

The effect of external marking on the behaviour of the common pill woodlouse Armadillidium vulgare

Zoologists distinguish individual animals using marking techniques. Generally they test the potential influence of marking on survival only; the influence on behaviour is usually neglected. We evaluated the influence of two external marking techniques (nail polish and queen-bee marker) on the behaviour of common pill woodlouse, Armadillidium vulgare. The behaviour was examined from two points of view: (1) activity during 24 hours and (2) specific expressions of behaviour (exploring, feeding, resting and hiding) over a 24 hour period. We compared behaviour among woodlice marked with nail polish and queen-bee marker with the unmarked control group during a nine-day experiment. Although we did not find any influence of marking on survival, there was an evident influence on behaviour in most cases. Generally, in the groups of marked individuals of Armadillidium vulgare there were large differences observed against the control group in the overall activity. Activity of marked individuals was significantly reduced and they preferred hiding. The influence of polish and marker on the overall frequencies of behavioural categories was evident, mainly in feeding, resting and hiding. The influence on the frequency of exploring was significant in the polish marked group only.     

The structure and function of the hepatopancreas of a terrestrial isopod, Armadillidium vulgare

The fine structure of the hepatopancreas of the isopod, Armadillidium vulgare was studied in intact and in experimentally treated animals. The gross anatomy of the hepatopancreas of this species is simpler than that of decapods, but microscopically the cells are similar in both. Accordingly, the function of this organ is probably the same in decapods and Armadillidium. Some phylogenetic considerations are also presented. In a previous paper Miyawaki et al. (1984), presented experimental results which indicated that the hepatopancreas of the crayfish, Procambarus clarki, had an important role in the absorption of digested food materials. These results confirmed earlier reports by Yonge (1924) and van Weel (1955) on the decapods, Nephrops norvegicus and Atya spinides, respectively. In the present study, we wished to determine whether the isopod hepatopancreas has a function like that of the decapods. A terrestrial isopod, Armadillidium vulgare collected on the University campus, and reared in the laboratory at room temperature was used. The methods of study were similar to those employed in the study with Procambarus clarki (Miyawaki et al., 1984).     

Photoperiodic control of the termination of breeding and the induction ofmoult in House Sparrows Passer domesticus

Two photoperiodic mechanisms controlling gonadal regression in birds have been identified: absolute photorefractoriness, typical of species with short breeding seasons, where gonadal regression occurs spontaneously during long days, and relative photorefractoriness, where a decrease in daylength is required to induce regression. An experiment was designed to test whether these simply represent extremes of one underlying mechanism. Three groups of male House Sparrows Passer domesticus were transferred from a short photoperiod, 8 h of light: 16 h of darkness per day (8L:16D) to long photoperiods of either 18L:6D, 16L:8D or 13L:11D. Gonadal maturation rates were similar in all three groups; gonadal regression and moult began latest in the 13L:11D group. Four additional groups of sparrows were transferred from 8L:16D to 18L:6D and then transferred to either 13L: 11D or 16L:8D prior to, or shortly after, the onset of gonadal regression. The decrease in daylength prior to regression had no effect on the timing of regression but did advance the onset of moult. Decrease in daylength after the onset of regression increased the rate of regression and the rate of moult. Because a decrease in daylength did not affect the timing of regression, the data do not support the hypothesis that absolute and relative photorefractoriness represent extremes of a single underlying photoperiodic control mechanism. The adaptive significance of the effects of decreasing daylength on the rate of regression and moult is discussed.     

Repellents in the Japanese cedar,Cryptomeria japonica,against the pill-bug,Armadillidium vulgare

Sandaracopimarinol and (1S,6R)-2,7(14),10-bisabolatrien-1-ol-4-one were isolated and identified from Cryptomeria japonica as repellents against Armadillidium vulgare which is well known as an unpleasant pest in the house and as vegetable pest in Japan. These compounds strongly repelled A. vulgare when they were combined, although each compound alone did not show any activity.     

A comparative study in Porcellio laevis (Lat.) and Armadillidium vulgare (Lat.): response to temperature, photoperiod and oxygen concentration.

Relationship of body weight, imposed fasting, temperature, light intensity, and oxygen concentration to oxygen consumption in Porcellio laevis and Armadillidium vulgare has been investigated in a series of laboratory experiments. It was observed that (1) the metabolic response in the two species to temperature change was a uniform increase of oxygen consumption with increasing temperature from 15 degrees C to 60 degrees C. Beyond 30 degrees C, the oxygen consumption in each species fell, and the thermal death point was reached at about 40 degrees C. (2) The response to decreasing oxygen concentrations was a corresponding decrease in oxygen consumption. Armadillidium vulgare was a partial regulator while Porcellio laevis was able to conform its internal state to the changing oxygen levels. (3) In each species there was a decrease in metabolic rate with increasing body weight. (4) On the basis of their general activity level and oxygen consumption rate, Porcellio appeared to be a nocturnal species, while Armadillidium had a day active metabolism.     

Evidence for a new feminizing Wolbachia strain in the isopod Armadillidium vulgare: evolutionary implications

Wolbachia are intracellular maternally inherited alpha-Proteobacteria infecting a wide range of arthropods. In the common pill bug Armadillidium vulgare, the known Wolbachia strain is responsible for feminization of genetic males. We have investigated Wolbachia diversity in 20 populations of A. vulgare from west and east Europe, north Africa and north America. A new Wolbachia strain (wVulM) was identified through the variability of the wsp gene, distantly related to that previously known (wVulC) in this host species. No individual with multiple infections was detected. Inoculation experiments indicated that the new wVulM bacterial strain also induces feminization in A. vulgare. However, the wVulC strain showed a higher transmission rate than the wVulM strain and was the most geographically widespread Wolbachia in A. vulgare populations. Mitochondrial 16SrDNA gene sequencing was conducted in Wolbachia-infected individuals, revealing the occurrence of four host lineages. The comparison of bacterial strains and their respective host mitochondrial phylogenies failed to show concordance, indicating horizontal transmission of the Wolbachia strains within populations of A. vulgare.     

Plasticity of moult and breeding schedules in migratory European Stonechats Saxicola rubicola

Timing is crucial in seasonal environments. Passerine birds typically use a combination of physiological mechanisms and environmental cues to ensure that breeding, moult and migration occur without major temporal overlap and under the most favourable conditions. However, late in the breeding season some individuals initiate additional clutches , whereas others initiate moult. Such alternative strategies are thought to reflect trade‐offs between reproductive benefits and timely investment in maintenance and survival. The degree of seasonal plasticity differs between species, depending on the mechanisms that govern their annual routine. Migrants are generally under pressure to complete breeding and moult before the autumn departure and often show little plasticity. We studied seasonal plasticity of breeding and moult schedules in the European Stonechat Saxicola rubicola. This species, an obligate short‐distance migrant in Central Europe, sometimes initiates late clutches after typically at least two earlier breeding attempts. Based on life‐history theory and on observations in captivity, which revealed photoperiodic regulation of breeding and moult, we predicted relatively little seasonal plasticity in Stonechats. We further predicted that reproductive gains of late breeders should be offset by reduced survival. These predictions were tested on long‐term field data, using Underhill–Zucchini models to estimate moult. Late breeding occurred in c. 40% of pairs and increased their reproductive success by a third. Both sexes modified moult timing but in different ways. Late breeding females postponed moult approximately until chick independence without compensating for delay by faster moult. Males started moult on time and overlapped it with breeding, associated with markedly slowed plumage change. Sex differences in moult score increased with lay date, but due to their respective modifications, both sexes delayed moult completion. Nonetheless, we could not detect any evidence for survival costs of late breeding. Breeding and moult of European Stonechats appear relatively flexible, despite migratory schedules and photoperiodic programs for seasonal timing. Individuals can modify seasonal behaviour in late summer, presumably depending on their condition, and may profit considerably from extended breeding.     

Why renew fresh feathers? Advantages and conditions for the evolution of complete post‐juvenile moult

Juveniles of several passerine species renew all of their fresh juvenile feathers immediately after fledging (complete post‐juvenile moult), in contrast to the majority, which perform a partial post‐juvenile moult. To understand the adaptive roles of this phenomenon we compared the quality of juvenile plumage in species that perform a complete post‐juvenile moult with that of species which perform a partial post‐juvenile moult; we similarly compared juveniles and adults in each of these groups. The quality of feathers was measured by mass of primaries, colour, and length. In species which perform a complete post‐juvenile moult the plumage quality of second‐year individuals, in their first breeding season, is similar to the plumage quality of adults, unlike those species that perform a partial post‐juvenile moult. In species which perform complete post‐juvenile moult, the quality of the feathers grown in the nest is lower than the quality of adult post‐breeding feathers. In contrast, in species which perform partial post‐juvenile moult the quality of the feathers grown in the nest is similar to that of adult post‐breeding feathers. We found that a complete post‐juvenile moult strategy is much more common 1) in residents and short‐distance migrants than in long‐distance migrants, 2) in southern latitudes, 3) in species with medium body mass and 4) in omnivores and granivores. Our results indicate two adaptive roles of the complete post‐juvenile moult strategy: 1) achieving high quality plumage in the first year which may increase individual survival probability and fitness and 2) allocating fewer resources to nestling plumage and more to nestling development, which enables the nestlings to leave the nest earlier, thus reducing the probability of encountering nest predators. We suggest that the complete post‐juvenile moult, immediately after fledging, is an optimal strategy in favourable habitats and under low time constraints, as in some tropical ecosystems.     

Novel structures in secreting the androgenic gland hormone

The secretory granules in the androgenic gland of the terrestrial isopod Armadillidium vulgare, which have been indistinct for long time because of vulnerable structures, were revealed by using the rapid-freezing and freeze-substitution method. The fine structure of the androgenic gland is conspicuous by the distribution of numerous particular organelles in the cytoplasm consisting of the endoplasmic reticulum and the Golgi complex, and by having a number of highly organized structures developed between the androgenic gland cells. The structures connect to the intercellular space, which is seen as intercellular canaliculi for exporting the androgenic gland hormone. The plasma membranes near the particular structure of the intercellular canaliculi in the androgenic gland are often specialized to form cellular junctions. The secretory granules including the electron-dense materials, which are supposed to be peptides of androgenic gland hormone, are distributed beside the particular structure of the intercellular canaliculi. Some of the granules are seen to fuse with the plasma membranes. This observation suggests that, in the Armadillidium vulgare, the secretory granules containing androgenic gland hormone are transferred to the extracellular space through the intercellular canaliculi particularly developed for exporting the peptide hormone. This is the first evidence to show the secretory mechanism of the androgenic gland hormone in the Isopoda.     

Early exposure to a bacterial endotoxin advances the onset of moult in the European starling

In animals, events occurring early in life can have profound effects on subsequent life‐history events. Early developmental stresses often produce negative long‐lasting impacts, although positive effects of mild stressors have also been documented. Most studies of birds have investigated the effects of events occurring at early developmental stages on the timing of migration or reproduction, but little is known on the long‐term effects of these early events on moulting and plumage quality. We exposed European starling Sturnus vulgaris nestlings to an immune challenge to assess the effects of a developmental stress on the timing of the first (post‐juvenile) and second (post‐breeding) complete annual moult, the length of the flight feathers, and the length and colouration of ornamental throat feathers. The nestlings were transferred to indoor aviaries before fledgling and kept in captivity until the end of post‐breeding moult. Individuals treated with Escherichia coli lypopolysaccharide (LPS) started both moult cycles earlier compared to control siblings. Moult duration was unaffected by the immune challenge, but an advanced moult onset resulted in a longer moult duration. Moreover, female (but not male) throat feather colouration of LPS‐injected individuals showed a reduced UV chroma. We argue that an early activation of the immune system caused by LPS may allow nestlings to better cope with post‐fledging stresses and lead to an earlier moult onset. The effect of early LPS exposure was remarkably persistent, as it was still visible more than one year after the treatment, and highlighted the importance of early developmental stresses in shaping subsequent major life‐history traits, including the timing of moult in birds.     

Seasonal changes in moult,body mass and reproductive condition in siskins Carduelis spinus exposed to daylength regimes simulating different latitudes

Birds use change in daylength during the year to time events during their annual cycles. Individual Eurasian siskins Carduelis spinus can breed and winter in widely separated areas in different years. Birds at different latitudes will experience different changes in photoperiod. So how does latitude affect photoperiodic control? Our aim in this study was to find whether Siskins caught from the wild in Britain and exposed to different photoperiodic regimes, typical of widely separated latitudes, would differ in the subsequent timing and duration of their moults and associated processes. Siskins were caught in late February and early March, and initially kept outside on natural photoperiods. From the spring equinox (21 March), they were divided into three groups kept under photoperiodic regimes that simulated latitudes 40°, 55° and 70°N respectively. All three groups showed highly significant subsequent changes in body mass, fat scores and cloacal protuberance size. Moult of the primary feathers started during June – August (mean 9 July), and lasted 61–99 days (mean 75 days). Birds that started to moult late in the season had shorter moult durations. All individuals showed lower mass and fat levels during moult than before or after moult. Crucially, there were no significant differences in the timing of these events between the three photoperiodic groups. Apparently these birds did not use prevailing absolute photoperiod or the prevailing rate of change in photoperiod to time moult‐related seasonal events, but used instead some other feature of the annual photoperiod cycle or some form of interval timer linked to photoperiod.     

Non‐moulted primary coverts correlate with rapid primary moulting

Time constraint is a main factor which affects the moult strategies in passerines, mainly during the first year of life. The variability of moult strategies between species is associated with the extent of the moult. In the first year of life, the extent of the moult is highly variable between species and individuals. In most passerine species, juveniles only renew some of their feathers, but the factors that govern which feathers are renewed and which are retained have been largely overlooked. Here we examine the common pattern of non‐moulted primary coverts (PC) in passerines during the first‐year moult cycle (post‐juvenile and first‐year pre‐breeding moults). On the interspecific level we found that among 63 species of passerines, PCs are the least commonly moulted feather tract. For five species (Hirundo rustica, Pycnonotus xanthopygos, Prinia gracilis, Acrocephalus stentoreus and Passer moabiticus) which perform a complete post‐juvenile moult, we found that the PC moult occurs over a longer period than greater coverts (GCs) and is sequential (non‐simultaneous). At the intraspecific level, we found that the main difference between a partial and complete moult in Prinia gracilis is the moulting or non‐moulting of the PCs. We also demonstrate that for Prinia gracilis 1) juveniles which do not moult their PCs, moult their primaries at a higher speed than those which moult their PCs and 2) area/mass ratio of PCs is lower than of GCs. These two findings may explain why many passerines skip PC renewal during the first year of life. Because the PC moult lasts a long time, forgoing this moult enables long term resource savings that allow for dealing with time constraints. Our results highlight the adaptive advantages of non‐moulted PCs in cases of time constraints.     

The life-cycle of the flatfish nematode Cucullanus heterochrous

Mature specimens of Cucullanus heterochrous Rudolphi, 1802 (Nematoda: Cucullanidae) were obtained from the intestine of the flounder, Platichthys flesus, from Danish waters. Eggs embryonate in seawater but do not hatch. Fully developed larvae pressed out of eggs are 430 microm long with amphids and dereids and enclosed within the cuticle of a previous larval stage. Infective larvae are believed to be in their third stage. Experimental studies showed that the polychaetes, Nereis spp., Scoloplos armiger, Brada villosa and Capitella sp., may act as intermediate hosts. In N. diversicolor the larvae increase their length to 1 mm within four weeks (15 degrees C) without moulting. Experimental infections showed that larvated eggs are not infective to fish, whereas >550 microm long larvae from polychaetes survived in 4-24 cm long flounders and plaice, Pleuronectes platessa. Third-stage larvae 550 microm to 1.1 mm long were found in the submucosa of the intestine one week post infection. At a length of about 800 microm to 1.4 mm they moult to fourth-stage larvae. Fourth-stage larvae, immature and mature worms occur in the intestine and rectum. Fourth-stage larvae and adults survived experimental transfer from one flounder to another. Similar developmental stages survived for two weeks in the intestine of experimentally infected cod, Gadus morhua.     

Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare.

Two maternally inherited sex ratio distorters (SRD) impose female-biased sex ratios on the wood louse Armadillidium vulgare by feminizing putative males. These SRD are (i) an intracytoplasmic bacterium of the genus Wolbachia, and (ii) another non-Mendelian element of unknown nature: the f element. Mitochondrial DNA variation was investigated in A. vulgare field populations to trace the evolution of host-SRD relationships and to investigate the effect of SRD on host cytoplasmic polymorphism. The Wolbachia endosymbionts showed no polymorphism in their ITS2 sequence and were associated with two closely related mitochondrial types. This situation probably reflects a single infection event followed by a slight differentiation of mitochondria. There was no association between the f element and a given mitochondrial type, which may confirm the fact that this element can be partially paternally transmitted. The spreading of a maternally inherited SRD in a population should reduce the mitochondrial diversity by a hitchhiking process. In A. vulgare, however, a within-population mtDNA polymorphism was often found, because of the deficient spread of Wolbachia and the partial paternal inheritance of the f element. The analysis of molecular variance indicated that A. vulgare populations are genetically structured, but without isolation by distance.     

Factors influencing the evolution of moult in the non‐breeding season: insights from the family Motacillidae

The number of moults per annual cycle and their final spatial pattern (i.e. topography) show high interspecific variation in the order Passeriformes. Factors behind this variability remain obscure, especially for variability in spatial pattern among species. Here, we explored the relative influence of ten ecological, ontogenetic, social and sexual factors on the evolution of autumn moult (feather replacement largely undertaken by migratory species, which is not necessarily an independent episode within their moult cycle) and prealternate moult among Northern Hemisphere species of the family Motacillidae using phylogenetically controlled analyses, ancestral state reconstruction and analyses of correlated evolution. The results strongly support the presence of prealternate moult and absence of autumn moult as ancestral states in this family. A high rate of change between related species indicates phylogenetic independence among prealternate moult patterns and examined factors. Migration distance and gregariousness are the most important factors influencing prealternate moult evolution, and point toward natural selection and sociality as the most important evolutionary drivers of prealternate moult in Motacillidae. Breeding latitude, seasonal plumage change, winter plumage conspicuousness, sexual dichromatism, plumage maturation and extent of preformative moult show a minor influence, and suggest that ontogeny and sexual selection may have played a limited role in shaping prealternate moult in Motacillidae.