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.     

Characterization of polymorphic microsatellite loci in the terrestrial isopod Armadillidium vulgare

The common pill bug, Armadillidium vulgare, is known to harbour two distinct strains of the feminizing proteobacteria Wolbachia. In order to study the effect of the presence of Wolbachia on the evolution of A. vulgare populations, we developed and characterized a set of nine polymorphic microsatellite loci from two microsatellite‐enriched genomic libraries. We screened 48 individuals from three French populations and found high genetic variation. Locus‐specific allelic diversity ranged from four to 28 and observed heterozygosity from 0.40 to 1.00, which indicates that these markers can be used to conduct population genetic studies in A. vulgare.     

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.     

Seasonal Reproduction in the Terrestrial Isopod Armadillidium vulgare (Latreille): Geographical Variability and Genetic Control of the Response to Photoperiod and Temperature

Summary

Armadillidium vulgare females of ten geographical origins were reared under various photoperiodic regimes. Long days stimulated reproduction in all the strains, but, whatever the conditions, females originating from high latitudes began to breed later than ones from low latitudes and, under natural photoperiod of Poitiers, the lag time was increased, more or less linearly, by 2 days per degree of latitude. The ability to remain in reproduction, after a first brood, was also related to the latitudinal origin of the strain. The onset of reproduction in the Sucre strain (Bolivia) was very late in respect to the latitude of the original site; the high altitude of Sucre may explain the divergence from the common rule. Reproduction characteristics of each strain persist in the females born and reared in the laboratory for several generations. This stability makes it possible to study the genetic determination of the photoperiodic responses. One genie system probably controls induction and maintenance of reproduction. This system involves maternal sex linked gene(s) (carried by W heterochromosome) and also autosomal genes with additive effects.     

Morphological and Biochemical Characterization of the Cream Markings in the Integument of the Female Isopod,Armadillidium vulgare

Cream markings aligned along the dorsal region of the female isopod, A. vulgare, were investigated with light and a fluorescence microscope and an electron microscope. Biochemical studies were also carried out. The cream markings were observed in the dorsal integument as a group of cream-colored chromatophores that emit a yellow fluorescence. These chromatophores, which are distinguishable from ommochrome chromatophores, contained numerous granules in the cytoplasm, and these granules (0.6–3.0 μm in length by 0.4–1.5 μm in width) were electron-lucent and spheroidal in shape with a concentric arrangement of membranes. Based on various biochemical analyses, the principal component of the yellow pigment isolated from the cream markings was identified as sepiapterin. These facts revealed that the cream markings are the chromatophores that contain pteridine granules. The males have no cream markings like those of the females, since the cream-colored chromatophores are externally hidden by the ommochrome chromatophore layer. The content of sepiapterin in the males was about two times greater than that in the females. This quantitative difference in sepiapterin content between males and females suggests that the pteridine formation in this pigment cell may be regulated by hormones associated with sex determination.     

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

Exotic 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.     

Morphological and hormonal parameters in two species of macaques: impact of seasonal breeding

To compare physiological and developmental differences between two cogeneric species that differ by seasonal vs. aseasonal breeding, values for morphological measurements, testicular volume, serum testosterone, estradiol, and dehydroepiandrosterone-sulfate levels were obtained from 53 rhesus during the early breeding season, as well as 41 pig-tailed macaque males maintained at the Tulane Primate Center. The two species exhibited similar body size, testosterone, and estradiol levels, but differed substantially in testicular volume (3.00 +/- 1.7 vs. 1.72 +/- 1.3 cc), abdominal skinfold measures (15.7 +/- 9.2 vs. 9.0 +/- 7.7 mm), and DHEA-S levels (18.0 +/- 11.7 vs. 7.6 +/- 5.4 microg/dl). Significant interaction effects for species by age group were found for weight, tricep circumference, length, and estradiol level. In addition, length was more closely related to testicular volume among rhesus compared to pig-tailed macaques, suggesting different developmental patterns between the species. Predictors of hormonal levels differed between the two species. In the rhesus, estradiol levels were related to testicular volume and testosterone levels while there were no anthropometric predictors of testosterone or DHEA-S. For the pig-tailed macaques, testicular volume was related to tricep circumference, testosterone to triceps skinfold and testicular volume, and estradiol to weight. It is argued that rhesus have larger testes for body size and more abdominal fat deposits during the early breeding season relative to pig-tailed macaques reflecting the increased demands of sperm competition in a seasonally breeding species. Hormonal differences associated with the difference in breeding system appear to be primarily related to adrenal rather than testicular activity.     

Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata)

Japanese macaques inhabit a relatively cold environment and females of this species could have developed strategies of energy economy to face the sometimes-harsh seasonal conditions of temperate climates, as well as reproductive costs, and thus regulate their energy balance. Here, we explore the relationship between nutritional status, body composition, seasonality, and reproductive status using isotope-labeled water, anthropometric measurements, and leptin assays from 14 captive female Japanese macaques. Our results indicated that body mass provided the best predictor of fat-free mass and fat mass. These females varied in estimated percent body fat between 8 and 25% (18% on average at the beginning of the mating season and 13% during the birth season). Higher body mass and body fat content were observed at the beginning of the mating season, which supports the hypothesis that individual females need to attain a sufficient physical condition to cover energy costs associated with mating activity, and to survive under severe ecological conditions in winter with high thermoregulatory costs. We found a relationship between conception rates and energetic condition or body fat, with females that conceived during one mating season being fatter after the end of their previous mating season. Together, these results suggest that, even in captive settings with constant food availability, seasonal breeding entails relatively high energy costs, and that females with higher energy status could invest more in reproductive activities and could afford to reproduce more rapidly.     

Male-male competition and repeated evolution of terrestrial breeding in Atlantic Coastal Forest frogs*

Terrestrial breeding is a derived condition in frogs, with multiple transitions from an aquatic ancestor. Shifts in reproductive mode often involve changes in habitat use, and these are typically associated with diversification in body plans, with repeated transitions imposing similar selective pressures. We examine the diversification of reproductive modes, male and female body sizes, and sexual size dimorphism (SSD) in the Neotropical frog genera Cycloramphus and Zachaenus, both endemic to the Atlantic rainforest of Brazil. Species in this clade either breed in rocky streams (saxicolous) or in terrestrial environments, allowing us to investigate reproductive habitat shifts. We constructed a multilocus molecular phylogeny and inferred evolutionary histories of reproductive habitats, body sizes, and SSD. The common ancestor was small, saxicolous, and had low SSD. Terrestrial breeding evolved independently three times and we found a significant association between reproductive habitat and SSD, with shifts to terrestrial breeding evolving in correlation with decreases in male body size, but not female body size. Terrestrial breeding increases the availability of breeding sites and results in concealment of amplexus, egg-laying, and parental care, therefore reducing male-male competition at all stages of reproduction. We conclude that correlated evolution of terrestrial reproduction and small males is due to release from intense male-male competition that is typical of exposed saxicolous breeding.     

Field and laboratory investigations of factors controlling schizogamous reproduction in the polychaete,Autolytus

Schizogamous reproduction by stolon formation in a presumably hybrid population of Autolytus prolifer × A. brachycephalus from the Oosterschelde (The Netherlands) was investigated. Field observations proved that this population does not reproduce all year. During winter, about 50% of the worms were at early stages of stolonization, but no mature stolons at all were developed. Individuals with mature stolons, and also juveniles with less than 20 setigers, were collected in May. Nurses with long stolon chains and numerous reproductive stolons appeared during summer. Nurses collected in winter had higher numbers of stock setigers than those captured in summer; this reduction of the number of setigers mainly results from repeated incorporation of stock setigers into stolons. The influence on stolonization of nutrition, photoperiod and temperature was investigated in the laboratory. Ample food supply is an indispensable prerequisite for stolonization; starved individuals produced small regenerates, but never formed stolons. In well-fed specimens of both juvenile worms and nurses deprived of their stolons, simulated winter conditions (short-day photoperiod at 10°C) prevented stolonization, whereas approximation of summer conditions (long-day photoperiod at 15°C) induced or reinitiated stolon formation.

The results and observations on stolonization at other combinations of different photoperiods and temperatures show that the diurnal photoperiod is a dominant factor in the control of stolonization in these Autolytus spp.. This is the first experimental proof of photoperiodism within the polychaete family, Syllidae.     

Interactions potentially affecting the seasonal abundance of selected aquatic invertebrates in a rice field habitat

Variables associated with the seasonal abundance of members of a prey complex consisting of Chironomidae, Corixidae and Crustacea, and of a predator guild including Belostomatidae, Dytiscidae, Hydrophilidae and Notonectidae sampled from California rice fields were evaluated by multiple regression analysis. Variables included water temperature, rice plant stand and potential predator-prey interactions. Regression equations using water temperature and rice plant stand as independent variables described the seasonal abundance of both the prey complex (F = 5.619; P = 0.025) and the predator guild (F = 9.037; P = 0.005). Predator-prey interactions further modified many of the seasonal patterns of the organisms observed.     

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax)

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21–174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm³) was twice that recorded in June (351 mm³). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.     

Olfactory receptors in aquatic and terrestrial vertebrates

In species representing different levels of vertebrate evolution, olfactory receptor genes have been identified by molecular cloning techniques. Comparing the deduced amino-acid sequences revealed that the olfactory receptor gene family of Rana esculenta resembles that of Xenopus laevis, indicating that amphibians in general may comprise two classes of olfactory receptors. Whereas teleost fish, including the goldfish Carassius auratus, possess only class I receptors, the `living fossil' Latimeria chalumnae is endowed with both receptor classes; interestingly, most of the class II genes turned out to be pseudogenes. Exploring receptor genes in aquatic mammals led to the discovery of a large array of only class II receptor genes in the dolphin Stenella Coeruleoalba; however, all of these genes were found to be non-functional pseudogenes. These results support the notion that class I receptors may be specialized for detecting water-soluble odorants and class II receptors for recognizing volatile odorants. Comparing the structural features of both receptor classes from various species revealed that they differ mainly in their extracellular loop 3, which may contribute to ligand specificity. Comparing the number and diversity of olfactory receptor genes in different species provides insight into the origin and the evolution of this unique gene family. Accepted: 29 July 1998     

Variable infant care contributions in cooperatively breeding groups of wild saddleback tamarins

Among non-human primates, alloparental infant care is most extensive in callitrichines, and is thought to be particularly costly for tamarins whose helpers may suffer increased energy expenditure, weight loss, and reduced feeding time and mobility. The costs and benefits of infant care likely vary among group members yet very few wild studies have investigated variable infant care contributions. We studied infant care over an 8-month period in four wild groups of saddleback tamarins in Bolivia to evaluate: (a) what forms of infant care are provided, by whom, and when, (b) how individuals adjust their behavior (activity, vigilance, height) while caring for infants, and (c) whether individuals differ in their infant care contributions. We found that infant carrying, food sharing, and grooming varied among groups, and immigrant males—those who joined the group after infants were conceived—participated less in infant care compared to resident males. Adult tamarins fed less, rested more, and increased vigilance while carrying infants. Although we did not detect changes in overall activity budgets between prepartum and postpartum periods, tamarins spent more time scanning their environments postpartum, potentially reflecting increased predation risk to both carriers and infants during this period. Our study provides the first quantitative data on the timing and amount of infant carrying, grooming, and food transfer contributed by all individuals within and among multiple wild groups, filling a critical knowledge gap about the factors affecting infant care, and highlighting evolutionary hypotheses for cooperative breeding in tamarins.     

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.     

Skeleton weight allometry in aquatic and terrestrial vertebrates

The relation of skeleton weight to body weight with increasing size is compared for aquatic and terrestrial vertebrates. Due to the buoyancy of water, the skeleton weights of aquatic vertebrates (fishes and whales) vary in nearly direct proportion (exponent 1.0) to body weight; while the skeletons of terrestrial vertebrates occupy an increasingly greater proportion of total body weight as size increases (exponent greater than i. i) due to the necessity of supporting their weight on land.     

Being evergreen in an aquatic habitat with attenuated seasonal contrasts – a major competitive advantage?

This study experimentally compares growth of four aquatic macrophytes species (Sparganium emersum Rehm., Hippuris vulgaris L., Groenlandia densa (L.) Fourr., Luronium natans (L.) Raf.) with different modes of winter persistence in a thermally buffered habitat. The question is whether the above-ground persistence of photosynthetic structures during winter can compensate for low growth rates of evergreens when they compete with fast growing, non-evergreen species. The experiment was carried out in experimental boxes installed in a former river channel fed by stenothermic ground-water. Species were planted pairwise in experimental boxes in autumn, monitoring was carried out in the following year: degree of evergreenness was evaluated through number of ramets present prior to the main growing season, competitive ability of species was assessed during the growing season through cover measurements at three dates. Degree of evergreenness varied considerably between species, ranging from increase of ramet numbers during winter in Luronium over preservation of ramet numbers in Groenlandia and Hippuris to nearly complete winter die-back in Sparganium. Luronium presented the highest cover during the entire growing season. Only by the end of summer did Sparganium attain a similar cover through a high growth rate. Despite large differences in cover, growth appeared largely unaffected by the kind of treatment partner a species was confronted with. Nevertheless, this study demonstrates that being evergreen can compensate for a low growth rate during the main growing season when it is associated to extensive growth outside this main growing season.     

Unaltered hematocrit values and differential hemocyte counts in acanthocephalan-infected Armadillidium vulgare

Three cell types were present in Armadillidium vulgare hemolymph. Hyaline cells, 8.2 to 12.0 μm in size with a few fine granules in the cytoplasm, comprised 42% of the cells. Twelve percent of the cells were nonexplosive granulocytes, 8.8 to 15.0 μm, with many cytoplasmic granules of medium size. A third cell type, an explosive 7.2- to 12.0-μm granulocyte with coarse cytoplasmic granules, comprised 46% of the cells. Within 48 hr after adult specimens of A. vulgare were fed eggs of the acanthocephalan, Plagiorhynchus cylindraceus, isopod hemocytes aggregated in the intestinal epithelium surrounding penetrating acanthors. Encapsulation and death of the parasite routinely followed. No significant difference in hematocrit values or in differential hemocyte counts occurred between infected and uninfected control isopods.     

Obligate association of an oligolectic bee and a seasonal aquatic herb in semi‐arid north‐eastern Brazil

Hydrocleys martii (Limnocharitaceae) is an annual aquatic herb common in ephemeral isolated ponds in semi‐arid northe‐astern Brazil. We studied pollination of H. martii, emphasizing reproductive success and association with oligolectic pollinators. The yellow flowers bear a central cone of staminodes that encloses the fertile stamens and four free carpels. The self‐incompatible species depends on pollinators to set fruits. In 25 temporary water bodies in five Brazilian states, Protodiscelis palpalis bees (Colletidae, Paracolletinae) were the unique effective pollinators of H. martii and, in 18 of these, the sole flower visitors. Females of this narrowly oligolectic species show adapted behaviour to access the pollen chamber in the flower centre. Females removed more than 80% of the 480 000 pollen grains in only 2 h from the flowers but maintained a high visitation frequency almost until flower senescence. In this highly specialized plant‐pollinator system, on average, 1.6% of the pollen grains reached the stigmatic surface and 9.6% remained uncollectible in the flowers. In the absence of P. palpalis, flowers set almost no seeds, indicating reproductive dependence on the oligolectic species. This pioneer pollination study of a species of Limnocharitaceae provides evidence of a close relationship of the family to species of Protodiscelis, their specific pollinators. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 355–368.