Dental ontogeny of a white shark embryo

Unlike most viviparous vertebrates, lamniform sharks develop functional teeth during early gestation. This feature is considered to be related to their unique reproductive mode where the embryo grows to a large size via feeding on nutritive eggs in utero. However, the developmental process of embryonic teeth is largely uninvestigated. We conducted X‐ray microcomputed tomography to observe the dentitions of early‐, mid‐, and full‐term embryos of the white shark Carcharodon carcharias (Lamniformes, Lamnidae). These data reveal the ontogenetic change of embryonic dentition of the species for the first time. Dentition of the early‐term embryos (∼45 cm precaudal length, PCL) is distinguished from adult dentition by 1) the presence of microscopic teeth in the distalmost region of the paratoquadrate, 2) a fang‐like crown morphology, and 3) a lack of basal concavity of the tooth root. The “intermediate tooth” of early‐term embryos is almost the same size as the adjacent teeth, suggesting that lamnoid‐type heterodonty (lamnoid tooth pattern) has not yet been established. We also discovered that mid‐term embryos (∼80 cm PCL) lack functional dentition. Previous studies have shown that the maternal supply of nutritive eggs in lamnoid sharks ceases during mid‐ to late‐gestation. Thus, discontinuation of functional tooth development is likely associated with the completion of the oophagous (egg‐eating) phase. Replacement teeth in mid‐term embryos include both embryonic and adult‐type teeth, suggesting that the embryo to adult transition in dental morphology occurs during this period. J. Morphol. 278:215–227, 2017. © 2016 Wiley Periodicals,Inc.     

Dentition facilitates the release of encapsulated Ragged-tooth Shark (<Emphasis Type="Italic">Carcharias taurus)</Emphasis> embryos

The capture of four female Ragged-tooth Sharks, Carcharias taurus, in the early stages of pregnancy in the bather protective nets along the KwaZulu-Natal coastline provided an opportunity to investigate embryonic development. A total of 31 embryos, 8–225 mm total length, were found. Of these, 15 were encapsulated and 16 were found free-floating in the uterus. Six embryos, three of which were encapsulated (35–50 mm) and three free-floating (36–52 mm), were examined under both light and scanning electron microscopy. The embryos possessed tooth-like structures. Spectral analysis of these structures revealed the presence of calcium, phosphorus, fluoride and oxygen, which supports the hypothesis that they are teeth. These teeth would enable embryos to escape encapsulation. These free-floating embryos are the smallest on record, with the previous smallest being a 40 mm embryo. These findings would now amend the current literature of C. taurus embryology. These results could affect the current understanding of C. taurus reproduction and biology and may impact any current breeding programs that are attempting to increase the fecundity of these species.     

Ultrasound examination and behavior scoring of captive broadnose sevengill sharks,Notorynchus cepedianus (Peron, 1807)

Serial ultrasound examination of four mature female sevengill sharks (Notorynchus cepedianus) was carried out over 18 months. Monitoring the reproductive cycle and development of follicles and fetuses in sharks in a noninvasive manner using this technique has not been reported previously. Sharks were caught out of the “Oceanarium” tank by divers using a specially made catch‐out bag, and brought to a holding area for examination. A behavior scoring system was used to monitor the impact of regular handling on the well‐being of the animals. Ultrasound showed the growth and regression of follicles in sevengill ovaries, and allowed an approximation of the reproductive stage of these sharks. Monitoring behavior at five time points during the procedure showed that regular handling of sharks for clinical studies could be done with minimal impact on animal welfare. The ability to follow reproductive events in elasmobranches using ultrasonography is an important step in the application of assisted reproductive technology in these species. Assisted reproductive technology, such as monitoring female reproductive cycles and artificial insemination, could potentially be used to maintain genetic diversity and compliment aquaria‐based breeding programs for endangered species such as the gray nurse shark (Carcharias taurus). Zoo Biol 26:383–395, 2007. © 2007 Wiley‐Liss, Inc.     

Teeth of Embryos in Lamniform Sharks (Chondrichthyes: Elasmobranchii)

The dentitions of lamniform sharks possess a unique heterodonty, the lamnoid tooth pattern. However, in embryos, there are 'embryonic' and 'adult' dentitions. The teeth in the embryonic dentition are peg-like and appear to be attached to the jaw in an acrodont fashion. The adult dentition is characterized by the presence of replacement tooth series with the lamnoid tooth pattern. The embryonic–adult transition in dentitions appears at around 30–60cm TL. Tooth replacement generally begins before birth in embryos with adult dentitions. The adult dentition becomes functional just before or after parturition. An embryo of one species (Lamna nasus) shows a tooth directly on the symphysis of the upper jaws, marking the first record of a medial tooth for the order Lamniformes.     

Polymorphic microsatellite markers for studies of the conservation and reproductive genetics of imperilled sand tiger sharks (Carcharias taurus)

We report on the isolation of eight microsatellites from the sand tiger shark, Carcharias taurus, using an enrichment protocol. All loci, with the exception of Cta45–183, were in Hardy–Weinberg equilibrium. Loci exhibited three to 15 alleles, and observed and expected heterozygosities of 0.095–1.000 and 0.284–0.924, respectively. An additional marker (Iox‐12) developed from a shortfin mako library was variable in sand tigers. These markers will be used to examine population genetics and mating patterns of this imperilled species.     

Intrauterine and post-ovipositional embryonic development of Amerotyphlops brongersmianus (Vanzolini, 1976) (Serpentes: Typhlopidae) from northeastern Argentina

The reproductive biology and embryonic development of Typhlopidae have rarely been explored. This family of snakes includes mostly oviparous species with uterine egg retention, but the morphology and development of embryos remain unknown. This work aimed to describe the embryonic development of Amerotyphlops brongersmianus from the northeast of Argentina. For this purpose, embryos from intrauterine eggs of gravid females and eight post-ovipositional eggs incubated in the laboratory were analyzed. Embryonic stages, corresponding to the early, mid and advanced development, and a hatchling were described. The main organs and systems form during the period of intrauterine embryonic retention. Comparing to other snakes, differences in the development of cranial structures such as encephalic vesicles and mandibular and maxillary processes were identified. After oviposition the development and differentiation of the tissues and organs completes, the body scales develop, the characteristic pattern of pigmentation establishes and the embryo grows and consumes the yolk. On average, the incubation period lasts 55 days. Differences in the stage of development at oviposition among females of different populations were observed. Embryonic retention could extend up to advanced stages of development.     

Terranova galeocerdonis (Thwaite, 1927) (Nematoda: Anisakidae) from Carcharias taurus (Chondrichthyes: Odontaspididae) off Argentina, with comments on some related species

The purpose of this study was to study and redescribe Terranova galeocerdonis (Thwaite, 1927) from Carcharias taurus off Argentina. Its fourth larval stage was described, measured and illustrated for the first time. The host and geographical range of this species is extended into the southwestern Atlantic Ocean. When the present material was compared with T. rochalimai (Pereira, 1935) and T. ginglymostomae Olsen, 1952, it was considered that both morphological and morphometrical differences between the three species did not justify differentiation at the specific level. As a result, T. rochalimai and T. ginglymostomae are considered to be junior synonyms of T. galeocerdonis.     

A review of hybridization in marine angelfishes (Perciformes: Pomacanthidae)

Synopsis Although hybridization of terrestrial and freshwater organisms has been well-studied, very little work has focused on hybridization among coral reef fish species. In the present paper, eleven examples of probable hybrids between marine angelfishes (Pomacanthidae) are reviewed. Evidence is presented which strongly suggests that the nominal speciesApolemichthys armitagei is invalid and that specimens previously identified as this species represent hybrids betweenA. trimaculatus andA. xanthurus. Of the remaining ten probable pomacanthid hybrids, five are inCentropyge (C. eibli x C. flavissimus, C. eibli x C. vrolikii, C. flavissimus x C. vrolikii, C. loricu0lus x C. potteri, andC. multifasciatus x C. venustus); one inHolacanthus (H. bermudensis x H. ciliaris), and four inPomacanthus (P. arcuatus x P. paru, P. chrysurus x P. maculosus, P. maculosus x P. semicirculatus, andP. sexstriatus x P. xanthometapon). An additional five examples of possible pomacanthid hybrids are described, two inCentropyge, two inChaetodontoplus and one inPomacanthus. Examination of hybrids may provide clues on reproductive behavior, dispersal capabilities, and phylogenetic relationships of species. More studies on hybridization in coral reef fish species, particularly those involving molecular techniques, are needed.     

The first reproductive parameters and evidence of multiple paternity in one new spiny dogfish species,Squalus albicaudus (Squaliformes,Squalidae)

Understanding elasmobranch reproductive biology is necessary for species conservation. Multiple paternity (MP) has been reported for elasmobranchs, and this study investigates the reproductive aspects and mating system (paternity genetic analyses) for Squalus albicaudus. Thirteen pregnant females were analysed concerning reproductive parameters, and the mating system was assessed for nine females and their litters. The study found a mean fecundity of 2.84 pups per litter without correlation between total female length and the number of embryos per litter. One litter showed evidence of MP, indicating the presence of polyandrous behaviour of the species.     

Reproduction and development ofSebastes in the context of the evolution of piscine viviparity

Synopsis Selected aspects of the reproduction and development ofSebastes and other rockfishes are reviewed in the context of piscine viviparity. Among the eight subfamilies of the Scorpaenidae, viviparity is confined to the subfamily Sebastinae; gestation is lumenal and the embryos usually develop to term within the egg envelope. Transitional states from oviparity to viviparity are evident in different species within the family. A scenario for the evolutionary origin of viviparity in rockfishes is derived from an analysis of scorpaeniform reproductive biology. Although viviparity is best developed in the genusSebastes, it is still in a primitive, unspecialized state. Rockfish viviparity is essentially lecithotrophic, i.e. embryonic nutrition is dependent on the energy reserves laid down during oogenesis. In other groups of viviparous fishes, lecithotrophy has been shown to be better suited energetically to seasonally unpredictable habitats, whereas matrotrophy requires a predictable food supply. During the evolution of an essentially primitive form of lecithotrophic viviparity in rockfishes, the advantages of high fecundity associated with oviparity were retained while an enormous increase in the survival rate of the developing embryos was acquired. The basic lecithotrophic pattern of oviparous development was not changed since it offered selective advantages both in terms of energetics and as a basis for retaining a large brood size.     

Laboratory studies on the life cycle of Leydigia acanthocercoides Fisher (1854) (Cladocera: Chydoridae)

The biology of Leydigia acanthocercoides has been studied under laboratory conditions with reference to longevity, instar duration, growth, fecundity and embryonic development at a temperature range of 28–30 °C. It has three preadult and thirteen adult instars. Under the given laboratory conditions this species produces 20 eggs during a life span of 23 days. The number of eggs produced is uniformly constant in all adult instars. The growth rate seems to be exponential in the early phase of the life cycle as in other Cladocera. The general pattern of embryonic development of L. acanthocercoides is similar to those of other tropical cladocerans though differences in the duration of total developmental period have been recorded.Part of Ph.D. thesis.     

Use of field‐portable ultrasonography reveals differences in developmental phenology and maternal egg provisioning in two sympatric viviparous snakes

A thorough understanding of the life cycles underlying the demography of wild species is limited by the difficulty of observing hidden life‐history traits, such as embryonic development. Major aspects of embryonic development, such as the rate and timing of development, and maternal–fetal interactions can be critical features of early‐life fitness and may impact population trends via effects on individual survival. While information on development in wild snakes and lizards is particularly limited, the repeated evolution of viviparity and diversity of reproductive mode in this clade make it a valuable subject of study. We used field‐portable ultrasonography to investigate embryonic development in two sympatric garter snake species, Thamnophis sirtalis and Thamnophis elegans in the Sierra Nevada mountains of California. This approach allowed us to examine previously hidden reproductive traits including the timing and annual variation in development and differences in parental investment in young. Both species are viviparous, occupy similar ecological niches, and experience the same annual environmental conditions. We found that T. sirtalis embryos were more developmentally advanced than T. elegans embryos during June of three consecutive years. We also found that eggs increased in volume more substantially across developmental stages in T. elegans than in T. sirtalis, indicating differences in maternal provisioning of embryos via placental transfer of water. These findings shed light on interspecific differences in parental investment and timing of development within the same environmental context and demonstrate the value of field ultrasonography for pursuing questions relating to the evolution of reproductive modes, and the ecology of development.     

Considerations on the diet composition and feeding rate of dermersal sharks in 15 European public aquaria

To get an overview of the feeding practices applied to dermersal sharks in captivity, a questionnaire was sent to 15 European public aquaria. The most common dermersal shark species kept in the participating aquaria are Carcharhinus plumbeus (n=9), Carcharias taurus (n=7), and C. melanopterus (n=6). Body weight (BW) was calculated using captive estimated body length (BL) and actual weight data obtained from commercial fisheries. The estimated BW for C. plumbeus in all participating aquaria is higher than the calculated BW. The feeding rate (FR) for adult C. plumbeus varied widely within participating aquaria (2.3–11.5% BW_cal/week or 32–112 kcal/kg BW_cal/week). The FR for adult C. plumbeus was lower (1.2–7.9% BW_est/week or 17–99 kcal/kg BW_est/week) using the estimated BW. Adult Carcharias taurus were fed at 1.3–5.0% BW_cal/week or 70–170 kcal/kg BW_cal/week. Negaprion brevirostris was fed at 5.0% BW_est/week or 57 kcal/BW_est/week. The relationship between FR and estimated BW is expressed as FR=54.5 e^?0.033BW. In this study, the feeding frequency for C. plumbeus varied between 1–7 times a week, with an average of 3.3 times a week. Diet in all aquaria consisted of both lean and fatty fish, and sometimes squid or crustaceans. Supplementation of vitamins is common practice in 80% of the surveyed aquaria, although a wide variety of quantity and quality was observed. Ten aquaria (66%) add iodine, as potassium iodide (0.4–12.5 mg KI/kg BW/week) or calcium‐iodate (322–1,500 mg/kg food/week), to their food. Zoo Biol 22:203–226, 2003. © 2003 Wiley‐Liss, Inc.     

To change or not to change sex: A comparison between twoOphryotrocha species (Polychaeta)

Summary The polychaeteOphryotrocha puerilis is a male-to-female sex-changer, whereasO. labronica has separate sexes throughout life. In other respects the two species are remarkably similar: they occur in the same habitat, they look the same, they eat the same things, and in someO. labronica populations sex-changers can actually be found. The size-advantage hypothesis predicts that inO. puerilis males should not benefit reproductively from a size increase as much as males inO. labronica: henceO. puerilis but notO. labronica males should change to the female sex at a certain size. I experimentally compared reproductive success at different body sizes between the two species. In isolated male-female pairs reproductive rate increased significantly with female body size but not with male body size, and this pattern was the same in both species. Hence male fecundityper se cannot account for the difference in reproductive type between the two species. In other experiments I investigated if larger males gained access to more females because they were superior competitors for mates or were preferred by females, compared to small males. InO. puerilis the combined effect of these two factors conferred no size advantage to the males, whereas inO. labronica larger males acquired more females than did smaller males. Hence interactions among males and females, in accordance with the size-advantage hypothesis, can explain why sex change is maintained inO. puerilis, and why separate sexes are maintained inO. labronica.     

Unusual pattern of embryogenesis of Caryophyllia inornata (scleractinia,caryophylliidae) in the mediterranean sea: Maybe agamic reproduction?

While knowledge of the reproductive biology of tropical scleractinian corals is extensive, information from temperate zones is limited. The aim of this study is to describe the reproductive biology of Caryophyllia inornata, a temperate species, and to increase the understanding of the reproductive strategies of Mediterranean corals. Samples of C. inornata were collected during SCUBA surveys at Elba island. Sexually active individuals displayed either male or female germ cells, showing a gonochoric sexuality. C. inornata exhibited an unusual pattern of embryogenesis. Embryos appeared throughout the whole year in males and in sexually inactive individuals, and they did not show a seasonal pattern of development, as usually expected for sexual reproduction. This observation suggests the possibility of asexual origin. These embryogenetic sexually inactive individuals were larger in size than the embryogenetic sexually active ones, and they might be senile polyps that preserve the ability to produce embryos only by agamic reproduction. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

The relative influence of temperature and humidity on cutaneous function in Bos indicus and Bos taurus females

The relative importance of dry- and wet-bulb temperatures on cutaneous function inBos indicus andBos taurus females under humid tropical climatic conditions was evaluated. The parameters investigated were sweating rate and skin temperature, while the species utilised were zebu White Fulani (Bos indicus) and German Brown and German Black and White (Bos taurus).The sweating rate, irrespective of breed, differed with the site of sampling and was more influenced by dry-bulb (59%) than by wet-bulb temperature (41%). Skin temperature responded more to wet-bulb temperature in White Fulani and German Black and White cattle, but not in German Brown cattle.It is concluded that the response of the animals, with respect to sweating, was similar but that the efficiency of sweating, judged by the lowering of skin temperature, was higher inBos indicus than inBos taurus. This, in part, may explain the higher degree of comfort demonstrated byBos indicus under tropical conditions.     

Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus <Emphasis Type="Italic">Cirsium</Emphasis> (Asteraceae)

Previous studies have examined an association between reproductive success and pollination biology of rare versus widespread species through pair-wise comparisons of native and invasive congeners or rare and common congeners. To determine the importance of reproductive success and pollination biology for an invasive thistle, Cirsium vulgare, we compared it in its invaded range to five, co-occurring native Cirsium species that range from rare to common. Native study species include C. fontinale var. fontinale, C. andrewsii, C. brevistylum, C. occidentale, and C. quercetorum. We compared all species’ reproductive success, insect visitation rate and composition, autonomous self-pollination, and level of pollen limitation in multiple populations. Species differed in their reproductive success; the invasive C. vulgare produced more flower heads per plant than most native species. C. vulgare attracted more visitors than its congeners. In addition, reproductive success and insect visitation significantly varied between populations within species, mainly due to aphid infestation in one population of C. occidentale. Unlike the rare species (C. fontinale and andrewsii), C. vulgare did not require a pollinator for high-levels of seed production. The remaining native species set fewer seeds than C. vulgare without a pollinator. However, differences in insect visitation and autonomous self-pollination did not lead to differences in pollen limitation across species or between populations. This result suggests that factors other than pollination biology determine the difference in reproductive success of these species. However, high levels of autonomous self-pollination and generalist insect visitation may allow the invasive C. vulgare to easily establish new populations from low numbers of propagules. Our study provides one contrast that should build towards a larger comparative analysis to examine general patterns in the relationship between reproductive success, pollination biology, rare and invasive species, and our ability to predict biological invasions in introduced species.     

Reproductive biology of twoPrunus species (Rosaceae) in the Northwest Iberian Peninsula

We studied the reproductive biology ofPrunus spinosa andPrunus mahaleb (Prunoideae, Rosaceae) in the northwest Iberian Peninsula. The two species flowered at the same time (peaking on March 9 and 11, respectively in 1990) but differ significantly in their fruit maturation times. Nectar volume peaked in the early morning in both species, and was ten times greater inP. spinosa than inP. mahaleb. Neither species shows apomixis, nor does fruit-set occur if pollinators are excluded. In both species self-pollination resulted in fewer fruits than open pollination. The principal pollinators belong to theApidae family (79% and 63% of visits toP. spinosa andP. mahaleb, respectively). Results are compared with those for other rosaceous plants with fleshy fruits.     

Fecundity and reproductive output of the caridean shrimp Periclimenes paivai associated with scyphozoan jellyfish

Periclimenes paivai is notable for its symbiotic lifestyle with jellyfish. The objective of this study was to investigate the fecundity and reproductive output of females, and specifically to determine whether females protected in their host have a greater reproductive success than other shrimp species. All anatomical parts of the medusae were analyzed and the P. paivai individuals were separated. Among 83 females analyzed, 65 presented embryos in the first developmental stage, and 18 were in the final stage of development. The mean fecundity was 229.08 ± 120.04 in initial-stage embryos and 191 ± 114.76 in final-stage embryos. We observed a positive relationship between the embryo number and the female size; however, the embryo number was not related to the embryonic stage, which indicates that females did not lose their embryos during the incubation period. The weight of brood mass during production is closely related to the female weight according to the results of linear regression, as fecundity increased with female size. In its symbiosis, P. paivai can increase the amount of energy used to produce embryos (mean reproductive output = 10.38%) and can elevate the reproductive success.