Placental ontogeny of the Tasmanian scincid lizard, Niveoscincus ocellatus (Reptilia: Squamata)

A prominent scenario for the evolution of reptilian placentation infers that placentotrophy arose by gradual modification of a simple vascular chorioallantoic placenta to a complex structure with a specialized region for nutrient transfer. The structure of the chorioallantoic placenta of Niveoscincus ocellatus, apparently described originally from a single embryonic stage, was interpreted as a transitional evolutionary type that provided support for the model. Recently, N. ocellatus has been found to be as placentotrophic as species with complex chorioallantoic placentae containing a specialized region called a placentome. We studied placental development in N. ocellatus and confirmed that the chorioallantoic placenta lacks specializations found in species with a placentome. We also found that this species has a specialized omphaloplacenta. The chorioallantoic placenta is confined to the region adjacent to the embryo by a membrane, similar to that found in some other viviparous skinks, that divides the egg into embryonic and abembryonic hemispheres. We term this structure the "inter-omphalopleuric" membrane. The position of this membrane in N. ocellatus is closer to the embryonic pole of the egg than to the abembryonic pole and thus the surface area of the omphaloplacenta is greater than that of the chorioallantoic placenta. In addition, the omphaloplacenta is regionally diversified and more complex histologically than the chorioallantoic placenta. An impressive and unusual feature of the omphaloplacenta of N. ocellatus is the development of extensive overlapping folds in the embryonic component of mid-gestation embryos. The histological complexity and extensive folding of the omphaloplacenta make this a likely site of placental transfer of nutrients in this species.     

Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus

The majority of research into the timing of gonad differentiation (and sex determination) in reptiles has focused on oviparous species. This is largely because: (1) most reptiles are oviparous; (2) it is easier to manipulate embryonic developmental conditions (e.g., temperature) of eggs than oviductal embryos and (3) modes of sex determination in oviparous taxa were thought to be more diverse since viviparity and environmental sex determination (ESD)/temperature-dependent sex determination (TSD) were considered incompatible. However, recent evidence suggests the two may well be compatible biological attributes, opening potential new lines of enquiry into the evolution and maintenance of sex determination. Unfortunately, the baseline information on embryonic development in viviparous species is lacking and information on gonad differentiation and sexual organ development is almost non-existent. Here we present an embryonic morphological development table (10 stages), the sequence of gonad differentiation and sexual organ development for the viviparous spotted snow skink (Niveoscincus ocellatus). Gonad differentiation in this species is similar to other reptilian species. Initially, the gonads are indifferent and both male and female accessory ducts are present. During stage 2, in the middle third of development, differentiation begins as the inner medulla regresses and the cortex thickens signaling ovary development, while the opposite occurs in testis formation. At this point, the Müllerian (female reproductive) duct regresses in males until it is lost (stage 6), while females retain both ducts until after birth. In the later stages of testis development, interstitial tissue forms in the medulla corresponding to maximum development of the hemipenes in males and the corresponding regression in the females.     

Facultative sex allocation in snow skink lizards (Niveoscincus microlepidotus)

Mathematical models suggest that reproducing females may benefit by facultatively adjusting their relative investment into sons vs. daughters, in response to population‐wide shifts in operational sex ratio (OSR). Our field studies on viviparous alpine skinks (Niveoscincus microlepidotus) document such a case, whereby among‐ and within‐year shifts in OSR were followed by shifts in sex allocation. When adult males were relatively scarce, females produced male‐biased litters and larger sons than daughters. The reverse was true when adult males were relatively more common. That is, females that were courted and mated by few males produced mainly sons (and these were larger than daughters), whereas females that were courted and mated by many males produced mainly daughters (and these were larger than sons). Maternal body size and condition also covaried with sex allocation, and the shifting pattern of sexual size dimorphism at birth may reflect these correlated effects rather than a discrete component of an evolved sex‐allocation strategy.     

Utilisation of nutrients by embryos of the enigmatic Australian viviparous skink Niveoscincus coventryi

The Eugongylus species group of Australian lygosomine skinks provides an unparalleled opportunity to study the evolution of placentotrophy. Viviparity and placentotrophy have evolved in two lineages, currently recognised as the genera Pseudemoia and Niveoscincus. The genus Niveoscincus is important because it is the only lineage of squamates in which variation in placental morphology and in the pattern of embryonic nutrition is known. Niveoscincus coventryi has the least complex placental morphology among species currently assigned to the genus. We quantified the net uptake of nutrients across the placenta of N. coventryi for comparison with other species in the genus and with other viviparous and oviparous lizards. The pattern of embryonic nutrition of N. coventryi is similar to other viviparous lizards with simple placentae in that there is no net uptake of dry matter during development but there is a net uptake of water, calcium, potassium, and sodium. There is no net uptake of lipid, nitrogen (an index of protein), or magnesium. We conclude that N. coventryi is predominantly lecithotrophic. Further, if N. coventryi is the sister taxon to Tasmanian Niveoscincus, then the distribution of patterns of embryonic nutrition among members of this clade suggests that the evolution of placentotrophy occurred during radiation of this lineage in Tasmania.     

The effect of thyroxine on the oxygen consumption of the ocellated skink, Chalcides ocellatus (Forskal)

Acutely administered thyroxine caused significant increase in the whole body rate of oxygen consumption of C. ocellatus at temperatures between 4 and 25 degrees C. No significant increase in the oxygen consumption was observed over the voluntary body temperature range of 30-40 degrees C.     

Contribution of aerobic and anaerobic scope to the total metabolic scope of the desert skink,Chalcides ocellatus (Forskal)

• 1.1. Measurements of aerobic scope (resting and active oxygen consumption rates) and anaerobic scope (resting and active production of lactate rates in the whole body homogenates) were carried out on the desert skink, Chalcides ocellatus at temperatures between 10 and 40°C.
• 2.2. The aerobic scope was maximal around the preferred body temperature with a low thermal temperature dependence above the preferred levels.
• 3.3. During initial stages of forced activity, C. ocellatus employed anaerobic metabolism as its major energy source.

     

Late stage deferral of parturition in the viviparous lizard Niveoscincus ocellatus (Gray 1845): implications for offspring quality and survival

The ability of viviparous lizards to defer parturition after completion of embryonic development is a potentially key strategy for enhancing offspring fitness. Using the spotted snow skink, Niveoscincus ocellatus , we investigated the ability of females to defer birth if placed into cold conditions at the same time, for 1, 2 or 3 weeks at the end of gestation. The ability to defer birth was compared between two populations at each end of the species' altitudinal range. We hypothesized that females from the high elevation population would be less likely to defer parturition under extended periods of poor conditions, thus ensuring that young were not born too late in the season. In all but the 3-week treatment group from the high elevation population, females were able to defer birth when placed under cold conditions: for all groups, there was no treatment effect on offspring phenotype at birth, dispersal distance or survivorship after release. However, there was a significant negative effect of treatment on offspring growth measured after release, with the results differing between the populations. Females from the high elevation population were less able to defer birth under long periods (3 weeks) of cold conditions, and this was accompanied by a decrease in viability of the offspring.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 735–746.     

Sex determination system of the rosy bitterling, Rhodeus ocellatus ocellatus

The rosy bitterling, Rhodeus ocellatus ocellatus, is the only fish species known in which artificial triploids are always male, regardless of the kind of polyploidization technique used. In order to elucidate the genetic sex determination system of the rosy bitterling, two kinds of gynogenesis were carried out: retention of the second polar body (GRSPB) and suppression of the first cleavage (GSFC). The sex ratio of progeny was nearly 7:1 (:) for both GRSPB and GSFC, while those of control and parental fish were almost 1:1. In backcrosses of female progeny by GRSPB and normal diploid males, male progeny were observed at low frequency (one or two individuals in each experiment), except in one experiment where the appearance rate of males was about 50%. From results of gynogenesis and backcrosses, the following conclusions can be made. The genetic sex determination system of the rosy bitterling is a heterogametic female system (ZW). Survival rate of superfemales (WW), produced by gynogenesis, is much lower than that of males (ZW).There is a possibility that crossovers between sex determining genes and a centromere occur in the first meiosis. With repect to the mechanism of unisexuality (male) of artificial triploids of the rosy bitterling, only males (ZZZ and ZZW) are presumed viable, while females (ZWW) are probably inviable.     

Oochoristica chalcidesi n. sp. (Eucestoda: Linstowiidae) from the ocellated skink, Chalcides ocellatus (Forskal, 1775) in the United Arab Emirates

Five out of ten ocellated skinks (Chalcides ocellatus) examined in Dubai between 2007 and 2010 were infected with cestodes of the genus Oochoristica. Out of the 36 collected tapeworms seven specimens were used to describe a new species. Oochoristica chalcidesi n. sp. belongs to the group of species with 25 to 35 testes arranged in two clusters. The lobes of the ovary are subdivided into 4-5 lobules in a similar way as O. ubelakeri described from Agama atra in Namibia. Both species differ in the presence of a neck, a lower number of mature segments in O. chalcidesi n. sp. and a different position of the cirrus pouch in relation to the ovary, as well as in the distribution of uterine capsulae in gravid segments.     

Female-biased natal and breeding dispersal in an alpine lizard, Niveoscincus microlepidotus

We measured two aspects of dispersal in the alpine Australian scincid lizard, Niveoscincus micolepidotus : (1) natal dispersal, i.e. shift in home range over the lizard's first year of life, and (2) breeding dispersal, i.e. shifts of home ranges between breeding attempts as adults. On average, displacements were surprisingly small. Female neonates dispersed about twice as far as did males in the same cohort (means of 12 m vs. 6 m). A female's natal dispersal distance was not correlated with her body size or our estimate of physiological performance (sprint speed). However, larger, faster-running male neonates dispersed further than did smaller, slower males. As was the case for neonates, adult females moved significantly further between breeding seasons than did adult males (14.2 m vs. 9.6 m). Because of a female's long gestation period (more than 1 year), two groups of females occur simultaneously in the population, non-ovulated (i.e. with yolking folicles) and pregnant females (i.e. approaching parturition). Females that were not yet ovulated showed a markedly stronger dispersal in response to high reproductive effort (i.e. clutch size in relation to body condition) than did pregnant females. In adult males, body size was negatively correlated with dispersal distance, suggesting that although males have overlapping territories, they exhibit an increasing level of site tenacity with age and/or size. Thus, selection for the relatively more pronounced site tenacity in adult males may have resulted in the more marked philopatric behaviour compared to females also as neonates.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 277–283.     

Spermatozoa in triploids of the rosy bitterling Rhodeus ocellatus ocellatus

Artificially induced triploid male Rhodeus ocellatus ocellatus showed typical nuptial colorations, irrespective of spermiation. In milt from triploids, abnormal spermatozoa (malformation of the head and mitochondrion, excessive formation of the head, mitochondrion and flagellum, and no flagellum) occurred at 78°4% frequency. Spermatozoa with multiflagella were most common, often with a saccate-like organ. Many triploid spermatozoa moved actively as long as those of diploids (10·92±0·91 min=mean±S.D., P >0·05), but did not advance like diploids, spinning around until movement ceased. The sperm density in triploids was < 2% of that from diploids. In triploid testes, deformed and variously sized spermatids were often observed, and normal spermatids and spermatozoa were seldom recognized. The DNA content of triploid spermatozoa varied greatly, compared with that of diploids. Peak of sperm DNA content differed slightly between two triploid samples with two peaks at 1·5 n and 1·9 n ( P <0·0001 in both), respectively. Triploids had the greatest average sperm head diameter of 2·25±0·67 μm (mean±S.D.), while that of diploids was 1·83±0·15 μm ( P =0·002). In the fertilization test using the eggs of diploids ( n =1500, 30 trials), only one egg developed. The embryo chromosome number was 60 (2·5 n) and the ploidy of spermatozoa contributing to fertilization appears to be 1·5 n. The extremely low fertility of triploid R. o. ocellatus spermatozoa seems to be caused by the reduced motility and large head size of spermatozoa, and the low sperm density of the milt. The ploidy of spermatozoa that are successful in fertilization is likely to be related to the distribution pattern in the DNA content of cells.     

Ownership influences the outcome of male-male contests in the scincid lizard, Niveoscincus microlepidotus

Male snow skinks (Niveoscincus microlepidotus) in the Tasmanian highlands have broadly overlapping home ranges, and fight vigorously(often with substantial damage to one or both participants)upon encountering another adult male. We observed 32 male-malecontests, involving at least 49 different males, during a five-yearfield study near the summit of Mount Wellington. Bouts involvingsimilar-sized lizards typically continued for longer than boutsinvolving a greater size disparity between the combatants. Resident males won 72% of all bouts, despite a lack of any significantdifference between residents and intruders in body sizes, relativehead sizes or body condition. Thus, prior residency of a siteappears to be the major determinant of success in male-malerivalry.     

Costs of egg caring in the skink, Mabuya longicaudata

Why do most animal species not provide parental care to their eggs or progeny? The “cost” hypothesis suggests that parental care can reduce food intake, probable survivorship, and/or subsequent fecundity of the reproductive female, and parental care is not adaptive unless it is balanced by considerable fitness trade-offs. Therefore, parental care would be expected to evolve most often in species in which such costs are minor or insignificant. Although parental care has been reported in more than 140 species of reptiles, few records unambiguously demonstrate the cost of parental care. In the current study, I report the “costs” of maternal activities and survivorship, as well as egg attendance times, and within- and between-seasonal body size variations, of females of Mabuya longicaudata after engaging in parental care. I used those data to test whether parental care necessarily entailed large costs to mother lizards. The proportion of nests guarded decreased with time after eggs were laid, with most females remaining at the nest for at least 1 week, but then some beginning to leave. The loss of mass by females over the first week of egg guarding was on average balanced by a gain in mass during subsequent foraging bouts. The snout–vent length (SVL), body mass (BM), recapture (survival) rates, fecundity, timing of a second clutch, and clutch frequencies of females that exhibited long-term parental care (more than 28 days; mean, 31.6 ± 2.2 days) did not significantly differ from that of females that showed short-term parental care (9～16 days; mean, 12.5 ± 2.3 days). Thus, my data indicate that intense parental care over a long period does not necessarily entail major energy costs for the mother in terms of SVL, BM, recapture (survival) rates, or fecundity.     

Transparent-Scaled Variant of the Rosy Bitterling, Rhodeus ocellatus ocellatus (Teleostei: Cyprinidae)

Transparent-scaled variant (TSV) of the rosy bitterling Rhodeus ocellatus ocellatus (Kner) was observed on both morphology and heredity. Compared with the normal-scaled type (NST), TSV is characterized by the blackish coloration in both eyes and peritoneum, and the luminescent one over the whole body. Histologically, the density of guanophores containing reflecting platelets was conspicuously low, especially in scale, iris, choroid and peritoneum, while the increase in the number of goblet cells (mucous cells) was recognized all over the dermal/epidermal regions. The heredity of TSV was recessive and supposed to be controlled by a single pair of genes unrelated to sex, judging from the result of crossbreeding experiments between NST and TSV. In growth and reproduction, no difference was seen between these two phenotypes. Transparent-scaled variant of the rosy bitterling can be competent for a genetic marker in experimental and developmental biology.     

Life history,morphology and crossability of Chondrus ocellatus forma ocellatus and C. ocellatus forma crispoides (Gigartinales,Rhodophyta) from the north-western Pacific

The morphology, life histories and crossability in culture are described for the marine red algae Chondrus ocellatus Holmes forma ocellatus from Japan, China and Korea and C. ocellatus f. crispoides Mikami (Gigartinaceae, Rhodophyta) from Japan. In culture, all isolates of both formae showed a Polysiphonia-type life history typical of the family Gigartinaceae. Plants of C. ocellatus f. ocellatus from Korea and China and some strains from Japan formed gametangia under long-day conditions (LD) at 15°C; however, two other Japanese strains required short-day conditions (SD) at 15°C for gametogenesis, indicating a photoperiodic response. Plants of C. ocellatus f. crispoides did not require SD for gamete formation. In all strains, tetrasporophytes of both formae produced tetrasporangia under LD. Isolates of C. ocellatus f. ocellatus from Japan, China and Korea were found to be completely sexually compatible regardless of photoperiodic characteristics, and the responses to daylength shown by progeny of LD and SD strains suggested Mendelian inheritance of a daylength factor. Chondrus ocellatus f. ocellatus was sexually incompatible with C. nipponicus Yendo, a morphologically similar species from Japan, but C. ocellatus f. crispoides was partially interfertile with both C. ocellatus f. ocellatus and C. nipponicus, indicating that the three entities are closely related. In view of the apparently higher breeding compatibility between C. nipponicus and C. ocellatus f. crispoides, and the fact that these two entities are more similar morphologically and reproductively, it is proposed, provisionally, to refer C. ocellatus forma crispoides to C. nipponicus.