Egg Ribbons Research Articles

High abundance and reproductive output of an intertidal limpet (Siphonaria japonica) in environments with high thermal predictability

The predictability of high temperatures is important for intertidal species for coping with thermal stress. To investigate the roles of high temperature and its predictability on the population abundance and reproductive output of an intertidal rocky shore limpet, Siphonaria japonica, we monitored the operative temperature, recorded the population abundance of egg ribbons and adults, and quantified the expression of heat shock protein 70 (hsp70) mRNA on two warm-temperate rocky shores with different thermal environments. Abundances of limpets and egg ribbons in the hotter but more predictable (HP) habitats were higher than those in the relatively benign and unpredictable (BU) habitats. In the HP habitats, there was a strong positive correlation between habitat temperature and population abundance. For limpets living in the HP habitats, the expression of hsp70 exhibited a smaller increase with rising body temperature than for BU limpets, indicating the existence in HP limpets of a preparatory strategy in cellular stress response against thermal stress. Our results demonstrate that the predictability of operative temperature can affect physiological responses and population dynamics. The importance of predictability should be considered in analyses of the ecological consequences of climate warming.

The "Mexican dancer" in Ecuador: molecular confirmation, embryology and planktotrophy in the sea slug Elysia diomedea.

Elysia diomedea, otherwise known as the "Mexican dancer", aries in adult size and color across its geographical distribution in Ecuador. Because of morphological variation and the absence of genetic information for this species in Ecuador, we analyzed mtDNA sequences in three populations (Ballenita, La Cabuya, and Mompiche) and confirmed that individuals from the three locations belonged to E. diomedea and that there was no population structure that could explain their morphological differences. Next, we analyzed general aspects about the reproductive biology and embryology of this species. Live slugs from the Ballenita population were maintained and reproduced ex situ. Egg ribbons and embryos were fixed and observed by brightfield and confocal microscopy. We observed a single embryo per capsule, 98 embryos per mm2 of egg ribbon, and compared the cleavage pattern of this species to that of other heterobranchs and spiralians. E. diomedea early development was characterized by a slight unequal first cleavage, occurrence of a 3-cell stage in the second cleavage, and the formation of an enlarged second quartet of micromeres. We observed clear yolk bodies in the egg capsules of some eggs ribbons at early stages of development. Both reproductive and embryological characteristics, such as presence of stomodeum in the larva, and ingestion of particles after hatching confirmed the planktotrophic veliger larvae of this species, consistent with the majority of sacoglossans from the Eastern and Northeast Pacific Oceans.

Antibacterial scalarane from Doriprismatica stellata nudibranchs (Gastropoda, Nudibranchia), egg ribbons, and their dietary sponge Spongia cf. agaricina (Demospongiae, Dictyoceratida).

Investigations on the biochemical relationship between Doriprismatica stellata (Chromodorididae, Doridoidea) nudibranchs, their egg ribbons, and the associated dietary sponge Spongia cf. agaricina (Demospongiae, Porifera) led to the isolation of the structurally new scalarane-type sesterterpene 12-deacetoxy-4-demethyl-11,24-diacetoxy-3,4-methylenedeoxoscalarin, with an unprecedented position of the cyclopropane ring annelated to the ring A. Unlike other scalaranes, which are most often functionalized at C-12 of ring C, it bears two acetoxy groups at C-11 and C-24 instead. The compound was present in all three samples, supporting the dietary relationship between chromodorid nudibranchs of the genus Doriprismatica and scalarane-containing dictyoceratid sponges of the Spongiidae family. The results also indicate that D. stellata passes the scalarane metabolite on to its egg ribbons, most likely for protective purposes. The scalarane showed antibacterial activity against the Gram-positive bacteria Arthrobacter crystallopoietes (DSM 20117) and Bacillus megaterium (DSM 32).

The alien false limpet (Siphonaria pectinata) in the Bizerte channel (northern Tunisia): spawning, development and growth under laboratory conditions

Spawning, development and growth of Siphonaria pectinata in the laboratory were studied and described in detail during a one-year study period. Egg ribbons were observed in February, March, April, June, July, August and September, with a peak in number of ribbons per individual in July. On average, individuals laid 9.0 ± 5.1 egg ribbons at a spawning frequency of one egg ribbon day−1. The number of eggs per ribbon ranged from 752 to 50,400 depending on ribbon length. Embryonic development studied in February (13–15 °C), April (15–17 °C) and July (25–27 °C), reached hatching within 8–16 days with average larval lengths of 76.7 ± 5.9, 83.0 ± 11.3 and 78.3 ± 9.0 μm, respectively. Massive mortality was registered a few days after hatching, with larval longevity depending on the study period. Larval settlement occurred within 36–38 days after hatching, but only in the spawn deposited in February. Larval growth was slow during the first three weeks (18–26 μm week−1) and then accelerated until the sixth week (40–67 μm week−1). The present study contributes knowledge on the spawning, development and growth of S. pectinata, an alien species recently spreading throughout the Tunisian coast.

Divergent thermal sensitivities among different life stages of the pulmonate limpet Siphonaria japonica

The different life-history stages of organisms may have divergent thermal limits and thus respond differently to global warming. For comprehensive understanding of the ecological impacts of global warming, it is crucial to determine thermal limits among different life stages and to understand how close an organism lives to its thermal limits at different life stages. Here, we measured the effect of temperature on hatching and the lethal temperature (LT50, lethal temperature of 50%) of larvae to explore effects of high temperature on the encapsulated and planktonic stages of the pulmonate limpet Siphonaria japonica. We measured cardiac performance to determine adult limpets’ thermal limit. At the encapsulated stage, heat shock at 34.5 °C affected larval hatching significantly. Pelagic larvae showed a high LT50 (45.03 °C), indicating a high thermal tolerance for the pelagic larval stage. For the adults, the Arrhenius break temperature and flatline temperature were 38.49 ± 1.27 and 44.27 ± 1.08 °C, respectively. The integrated study of environmental temperatures and thermal sensitivities at different life stages of S. japonica indicates that the egg ribbon and adult stages are potentially most sensitive to the future temperature increases on subtropical shores.

Maturation, reproduction and early life history of anglerfish Lophius piscatorius in Faroese waters

Maturation, reproduction and early life history of Lophius piscatorius was investigated in Faroese waters. Length at first maturity (L50) was 58 cm for males and 84 cm for females, corresponding to an age of about four years for males and seven years for females. The proportions of females and males were similar in fish less than 55 cm long, and were skewed towards more males in medium sized fish (55–75 cm). Females were predominant in the larger fish (> 85 cm). Observations of spawning males and females, egg ribbons and pelagic anglerfish larvae, suggest that the main spawning season is from February to April and the spawning area seems to be southwest of the Faroe Plateau and in the Faroe Bank area. The Faroe Plateau probably serves as a nursery ground for juvenile anglerfish. Morphological transformation from larvae to juveniles occurred when the fish were about 7–9 cm long and they settled to the bottom when they were about 11 cm long. Thus, all life stages, as well as nursery areas, spawning areas and feeding areas of anglerfish are found in Faroese waters, indicating a separate stock in the area.

Developmental consequences of association with a photosynthetic substrate for encapsulated embryos of an intertidal gastropod

Aggregation of embryos in clutches that lack internal circulation can increase the risk of hypoxia by limiting gas exchange. As a result, limits on oxygen solubility and diffusion in water can constrain the size and embryo concentration of aquatic egg clutches. Hypoxia in egg masses can slow embryo development, increase mortality, and reduce size at hatching. The risk of hypoxia for embryos, however, can be reduced by association with photosynthetic organisms. We examined whether embryo development in egg ribbons of the cephalaspidean mollusk Haminoea vesicula is significantly influenced by oviposition on eelgrass (Zostera marina). Association with the photosynthetic substrate had marked effects on development relative to association with non-photosynthetic substrates, and the direction of these effects was mediated by light conditions. Under intermediate and high light levels, association with eelgrass accelerated embryo development, while under dim light, the presence of the macrophyte increased development rate and reduced hatchling shell size. Benefits of association with eelgrass at higher light levels likely result from oxygen production by eelgrass photosynthesis, while we attribute costs under low light to oxygen depletion by eelgrass respiration. Association with Z. marina also limited microphyte growth in egg ribbons of H. vesicula. In the field, measurements of light attenuation within an eelgrass bed showed that conditions under which benefits accrue to embryos are ecologically relevant and correspond to spatial patterns of oviposition on eelgrass in the field. The choice of a photosynthetic oviposition substrate under appropriate light conditions can improve embryo fitness by accelerating embryo development without compromising hatchling size and by reducing the potential for excessive and harmful fouling by microphytes.

Plasticity of Hatching and the Duration of Planktonic Development in Marine Invertebrates

Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.

Effect of plasticity in hatching on duration as a precompetent swimming larva in the nudibranch Phestilla sibogae

Abstract. Plasticity in hatching can balance risks of benthic and pelagic development and thereby affect the extent of larval dispersal. Veligers of the nudibranch Phestilla sibogae hatched from their individual capsules if the encapsulated embryos were scattered from a torn gelatinous egg ribbon. Hatching occurred as early as day 4 at 23°–25°C. The early hatchlings lacked a propodium, swam, and were not yet competent to settle and metamorphose. Hatching may be induced by predation: crabs consumed egg ribbons, and a portunid crab, caught in the act of tearing an egg ribbon, scattered encapsulated embryos. Undisturbed egg masses hatched as late as 9–11 d at 23°–25°C, or as early as 8 d in a trial at 26°C. Late hatchlings had a well‐developed propodium, and 20–100% metamorphosed within a day of exposure to the inducer from the nudibranch's coral prey. A few metamorphosed nudibranchs were found within hatching egg masses. Thus, the veligers can hatch so late that many are competent to metamorphose or so early that the obligate planktonic period can last 4 or more days. An attack by a predator means the benthic habitat is dangerous for the embryos, and swimming is presumably the safer option. In the absence of disturbance, the veligers hatch when ready or nearly ready to settle.

Microtubular Network of the Gelatinous Egg Envelope Within the Egg Ribbon of European Perch, <I>Perca Fluviatilis</I> L.

Background. After their deposition in water, eggs of perch form characteristic, long gelatinous ribbons (strands) floating within the water column. The ultrastructure of the external gelatinious egg envelope of members of the family Percidae was believed to be amorphous. The aim of the presently reported study was to describe the ultrastructure and function of the gelatinous egg envelope composing the perch egg ribbon. Materials and methods. Fresh eggs of European perch, Perca fluviatilis L., were collected, in the form of egg ribbons, from females caught at the spawning grounds on the Odra River side canal Dziewoklicz, within the city limits of Szczecin, Poland. After fertilization eggs were fixed in 4%formaldehyde. In the laboratory, the commonly accepted techniques (dehydration, critical-point drying, sputter coating) were used to prepare samples for examination with a scanning electron microscope (SEM). The observations were photographically documented. Results. Closely below the surface of the gelatinous egg ribbon we observed a network of microtubules. These microtubules opened at the egg ribbon surface in the form of ring-like or nozzle-like pores. Conclusion. The gelatinous egg envelope of perch is a complex microtubular network that likely performs a skeletal role for the egg ribbon. Our results also suggest that the regular surface openings of the aforementioned network may play an attachment function (micro-suckers) reciprocally between eggs and between eggs and other objects, thereby facilitating the fastening the eggs to underwater vegetation.

Spawning site selection by Eurasian perch (Perca fluviatilis L.) in relation to temperature and wave exposure

Abstract – The selection of spawning depth by Eurasian perch Perca fluviatilis was investigated in an experiment using artificial substrata in Lake Constance during the spawning season of 2007. The experiment compared spawning behaviour at substrata between 0.5 and 15 m depth at two sites exposed to different regimes of ship‐generated wave action. The total abundance of egg ribbons did not differ significantly between the two sites, but the preferred spawning depth was deeper at the wave exposed site (5 m) compared to the sheltered site (2 m). While water temperatures could not account for the observations, differences in wave exposure may explain the different spawning depth preferences. At both sites, large egg ribbons were generally found in deeper water, and large egg ribbons occurred more frequently at the sheltered site. Because the egg ribbons of perch are likely to have a size‐dependent susceptibility to hydrodynamic stress, large females may be expected to select deeper spawning locations where the effects of surface waves are considerably attenuated.

Genital system anatomy and development ofOvatella myosotisby three-dimensional computer visualization

Adult anatomy as well as organogenesis of the genital system of the ellobiid pulmonate Ovatella myosotis is investigated in detail by means of serial sectioning and three-dimensional computer reconstruction and visualization. From the middle portion of the adult, which has four nidamental glands, a spermoviduct leads to a common genital aperture. From here two separate structures, the vas deferens and a groove on the body surface, lead anteriorly. The latter is termed the egg groove because it carries the egg ribbon anteriorly, a function that is recognized here for the first time in the Ellobiidae. The evolution of this structure is discussed. In development, the organ system arises from four separate anlagen: (1) the ovotestis anlage, (2) the pallial anlage giving rise to the hermaphrodite duct, fertilization pouch–spermatheca complex, nidamental glandular complex and spermoviduct, (3) the bursa copulatrix anlage and (4) the anlage of the copulatory organ, vas deferens and egg groove. This development mode strongly resembles that of the siphonariid Williamia radiata, supporting its interpretation as a plesiomorphy in Pulmonata. Similarities in development of primitive pulmonates and evolution in gastropods lead to the assumption that ontogenesis of this organ system reflects evolution to some degree.

The use of artificial spawning substrates as media to support the reproduction of Eurasian perch in Lake Piediluco

Lake Piediluco is a naturally regulated lake used for hydroelectric purposes. Management of the lake and the eutrophic conditions of its waters have had a negative impact on fish populations, particularly that of Eurasian perch (Perca fluviatilis L.). In order to increase the natural reproduction of this species, an experimental program was undertaken from 1997 to 2003 to facilitate reproduction by providing artificial spawning substrates. In Lake Piediluco perch spawn from March to May. Egg ribbons ranged in length from 30 to 180 cm and contained from 12,740 to 205,466 eggs. The fraction of degenerated eggs ranged from 0.20% to 63.30% (average 10.20%). The results demonstrate the effectiveness of artificial substrates as suitable substrates for the reproduction of perch.

Jorunnamycins A—C, New Stabilized Renieramycin‐Type Bistetrahydroisoquinolines Isolated from the Thai Nudibranch Jorunna funebris.

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Jorunnamycins A-C, New Stabilized Renieramycin-Type Bistetrahydroisoquinolines Isolated from the Thai Nudibranch Jorunna funebris

Jorunnamycins A-C (1a-c), three stabilized renieramycin-type bistetrahydroisoquinolines, were isolated from the mantles, the visceral organs, and the egg ribbons of the Thai nudibranch Jorunna funebris that was pretreated with potassium cyanide (KCN), along with five known compounds, renieramycins M (2m), N (2n), O (2o), and Q (2q) and mimosamycin (3). The structures of 1a-c were elucidated from spectroscopic data and by chemical conversion of renieramycin M (2m) into 1c via 1a. The chemical stability and the oxidative degradation generating simple isoquinoline alkaloids of a carbinolamine analog 1d, which was easily prepared by reacting 1c with silver nitrate in aqueous acetonitrile, are discussed. The results of cytotoxicity studies are also presented.

The Arctic sea butterfly Limacina helicina: lipids and life strategy

The sea butterfly Limacina helicina was collected from May to September 2001 in Kongsfjorden, Spitsbergen, to investigate population structure and body and lipid composition with regard to life cycle and reproductive strategy. Veligers and juveniles were only found in late autumn and spring, whereas females occurred from July to September. The size of the females increased until mid-August and decreased in September. Dry and lipid mass were closely related to size; dry mass increased exponentially and lipids linearly with size. The lipid content was highest in veligers (31.5% of dry mass) and juveniles (23.6%) but low in females (<10%). Phospholipids were the dominating lipid class followed by triacylglycerols. Females, veligers, and egg ribbons, all from September, were richest in phospholipids. Juveniles contained the highest amounts of triacylglycerols, whereas females had low levels in July and the beginning of August. In mid-August, levels of triacylglycerols were variable and higher. This suggests that females were in their main spawning period and the high variability in triacylglycerols points to different stages within the spawning cycle. Enhanced amounts of free fatty acids in females from July may be related to gonad development. The 16:1(n-7) fatty acid was more dominant in spring whereas 18:4(n-3) increased in summer and autumn, which reflects a change in diet from diatom-dominated food items in spring to dinoflagellates in summer/autumn. Small amounts of long-chain monounsaturated fatty acids suggest ingestion of copepods, and the fatty acid composition of veligers feeding on particulate matter. L. helicina has a one-year life cycle with peak spawning in August and over-winters as veligers that may grow to juveniles during the winter period. They metamorphose into juveniles during spring, develop to males in early summer, and mature into females in July and August.

Full of eggs and no place to lay them: hidden cost of benthic development

The scarcity of sites suitable for attaching eggs may be a hidden cost to depositing embryos in benthic aggregations. We tested this hypothesis with the bubble-shell snail Haminaea vesicula, which lives on mud or sand but requires firm substrata for attaching its eggs. In pools on a sandflat where firm substrata were scarce, the preferred substrata were but a small fraction of the total available firm substrata. Abundant drifting green algal blades comprised 1 to 11% cover but were rarely used for egg deposition. Substrata commonly used for egg deposition totaled less than 1% cover, and included attached and drifting eelgrass, drifting branched red algae, bivalve shells, and attached green algal blades. In choice experiments, the snails preferred to deposit eggs on branched red algae and eelgrass, with bivalve shells next and green algal blades last. To test the hypothesis that substratum availability limits egg deposition, we added artificial eelgrass made of duct tape to tidepools inhabited by the snails. The mean number of egg ribbons laid m -2 in the exper- imental areas was 20 to 360 times that in control areas, and the mean number of adult snails present and egg ribbons per adult snail were greater in the experimental areas. Also, more egg ribbons per adult were deposited on artificial eelgrass when it was positioned away from natural eelgrass patches, indicating that distances of a few meters affect availability of substrata for deposition. The results imply that in this habitat the snails travel to scarce substrata for egg deposition, with whatever costs in time, energy, or risk that may be associated with travel. Scarcity of suitable sites for benthic egg masses can limit an apparently safe mode of development. Habitats that regularly support adult populations can differ greatly in suitability for egg deposition, but this limitation may not be appar- ent without experimental intervention.

The structure of the egg ribbons of a planktonic and intracapsular developing siphonariid limpet (Gastropoda: Pulmonata)

Summary Egg ribbons of two sympatric species of siphonariid limpets (Siphonaria capensis and Siphonaria serrata) with different life-history strategies were studied to compare their structural and biochemical differences. The structure of the egg ribbons was examined by light, transmission and scanning electron microscopy. The organic content of the egg ribbons was determined by TCA soluble carbohydrate, NaOH soluble protein and total lipid estimation. In both species histochemical tests showed the presence of mucopolysaccharides in the egg ribbon jelly, perivitelline fluid and the developing embryo, and protein in the perivitelline fluid and the developing embryo, whereas lipid was present only in the developing embryo. The egg ribbons of both species consist of (proceeding inwards) an outer mucous cover, a mucous matrix which holds the egg capsules, an inner mucous layer terminating in a mucous strand, egg capsules and the envelope surrounding the perivitelline fluid. The structural composition of the egg mass was similar in both species although the spawn of S. serrata appeared more fibrous and had a greater amount of carbohydrate and protein than that of S. capensis. S. serrata, which has intracapsular development, also produces egg capsules with thicker walls compared to S. capensis. It is suggested that it is these differences that make the egg masses of S. serrata more robust, enabling them to survive on the shore for longer periods.

Influence of temperature and size of females on the timing of spawning of perch, Perca fluviatilis, in Lake Geneva from 1984 to 1993

The influence of temperature and the size of reproducing females on the timing of spawning of perch in Lake Geneva has been studied for 10 consecutive years (1984–1993) by means of artificial spawning substrates. The clutch of perch is an egg ribbon with a width proportional to the size of the reproducing female, so that the size structure distribution of the female population can be estimated from measurements of the width of the egg ribbons. The survey of egg-ribbon size revealed a succession of 3 cycles (period of increasing mean size followed by a sharp decrease) lasting 3, 3 and 4 years which were due to the occurrence of 3 strong year classes born in 1982, 1985 and 1988 respectively. This phenomenon can be explained by the effect of intraspecific predation exerted by strong year classes on the offspring of the 2 following years rather than by fluctuations in the success of reproduction in relation to climatic changes. In Lake Geneva, perch spawn in May. The water temperature exerted only a minor influence on the date of the beginning of the spawning period but had a greater effect on its intensity. A rise in temperature in May stimulated spawning while bad weather decreased spawning intensity. The larger perch had a tendency to spawn later than the small ones. The date of the mid-spawning period was well correlated with the yearly mean width of perch egg ribbons but no correlation could be detected between it and the water temperature.

Defensive chemicals of the Spanisch dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet

The Spanish dancer nudibranch Hexabranchus sanguineus (Rüppell et Leuckart), a large brightly colored shell-less sea slug (Gastropoda : Opisthobranchia) common to Indo-Pacific coral reefs, derives a potent chemical defense from a sponge that it eats ( Halichondria sp.). In turn, the nudibranch passes defensive compounds to its egg ribbons, which are similarly conspicuous and physically defenseless. Slices of the dorsal mantle tissue of the nudibranch were rejected in laboratory feeding assays employing two common sympatric predators: an Indo-Pacific reef fish, Thalassoma lunare (Linnaeus), and a reef hermit crab, Dardanus megistos (Herbst). The defensive metabolites, a suite of unusual oxazole-containing macrolides, were isolated from the sponge, the nudibranch, and the nudibranch egg masses at 0.14–0.38, 0.14–0.62, and 2.65% of dry weight, respectively, and were effective inhibitors of feeding by T. lunare at minimum concentrations of 0.01–0.02% dry weight of food pellet. The macrolides were concentrated in the dorsal mantle of the nudibranch, which is most vulnerable to predatory attack, and in the combined digestive gland/gonad, site of both sponge digestion and egg production. The most abundant macrolide in the sponge tissue was not present in the nudibranch or its egg masses, suggesting that chemical modification of this compound takes place upon digestion. In a reef environment dominated by visually oriented predators, the striking color pattern and behavioral responses of Hexabranchus may have arisen with a concomitant elaboration of dietarily derived chemical defenses.