Reproductive biology of a deep-sea brittle star Amphiura carchara (Echinodermata: Ophiuroidea)

 New information on the brooding reproduction of Amphiura carchara, and previous studies of several deep-sea congeners, contradict the prevailing notion that direct development is exceptional among deep-sea echinoderms. Over 500 specimens of A. carchara from 2,850 to 4,100-m depths off the coast of California, USA, were studied. The species was found to be gonochoric, although most brooding species of ophiuroids are hermaphroditic. Females each brooded up to 72 embryos at a time, with up to 10 in a single bursa. The embryos of individual adults were often at different stages of development, but those brooded in a single bursa tended to be at the same stage. Thus, the species has characteristics that breach the distinctions between sequential and simultaneous brooding exhibited by shallow-water ophiuroids. The embryos developed from yolky eggs that are large for an ophiuroid, with the mean largest oocytes 0.45 mm, and ranging to 1.28 mm in diameter. Almost all late-stage embryos were positioned with their mouth and arms pressed against the wall of the bursa, possibly to facilitate the uptake of nutrients from the parent. Thus, A. carchara may be matrotrophic. The largest embryos examined had a rudimentary disk skeleton, and arms with four joints and a terminal plate. Emerging juveniles probably differ in disk diameter. The species appears to brood year round, although differences in gonad size, the incidence of brooding, and the relative numbers of early developmental stages in summer and winter samples indicated that there are seasonal trends in reproduction. Received: 14 February 2000 / Accepted: 3 July 2000     

Prodissoconch morphology is environmentally modified in the brooding bivalve Lasaea subviridis

Embryonic shell sculpture of intertidal and laboratory brooded individuals of the direct developer Lasaea subviridis was studied using scanning electron microscopy. Intertidally brooded individuals develop a distinct prodissoconch I (PI) and prodissoconch II (PII) of unusual morphologies. The PI is relatively small (50–100 m in length), oval in outline, lacks a radial sculpture and is restricted to the initial pitted zone of the prejuvenile shell. A larger PII is formed (510–680 m in length) and it is dominated by pronouced commarginal striae but also includes a belt of radial ridges extending from the PI/PII boundary. Laboratory brooded individuals kept constantly submerged do not develop the pronounced commarginal striae characteristic of PII. This implies that PII formation in L. subviridis is not a direct result of the brooding habit, and can be modified by environmental factors, which possibly include low-tide exposure. There is no single feature of external prodissoconch morphology that unambiguously indicates a direct development mode combined with mantle cavity brood protection. General guidelines are presented to help recognize this developmental mode, based on prodissoconch morphology. In comparing prodissoconch morphologies of brooding bivalves, the habitats as well as the phylogenies of species should be considered, especially in comparisons of intertidal and subtidal species.     

Comparing biochemical changes and energetic costs in gastropods with different developmental modes: <Emphasis Type="Italic">Crepipatella dilatata</Emphasis> and <Emphasis Type="Italic">C. fecunda</Emphasis>

The Chilean gastropods Crepipatella dilatata and C. fecunda have different development modes: brooding and direct development in C. dilatata and brooding and planktotrophic development in C. fecunda. Unlike many other congeneric invertebrate species pairs, recent genetic evidence suggests that C. fecunda may have evolved from C. dilatata. To explore the changes involved in this unusual evolutionary path, this study examined the biochemical, energetic, and morphological characters during early development of both species. Mean egg size was slightly smaller for the direct-developing species C. dilatata, and initial energy content was lower—by about 27%—for eggs of that species. In both species, protein content in the eggs was the principal biochemical component. Although females of C. fecunda produce 180 times more eggs than C. dilatata, females of C. dilatata invest 20 times more energy in each of their offspring, through nurse eggs; their embryos have approximately eight times more energy at hatching and about 5 times more energy when they enter the benthos, despite a long planktonic feeding period in the larvae of C. fecunda. Evolutionary switching between modes of development in these species is reflected in shifts in maternal energy investment.     

Gill morphogenesis in the oyster Ostrea chilensis

Despite the importance of the gills in the acquisition of food by suspension-feeding bivalve mollusks, there is almost no information on gill organogenesis. By means of a series of stereoscan electron micrographs, this paper describes gill development in the Chilean oyster, Ostrea chilensis, from the brooded larval stages to 1-month-old spat. A single gill rudiment was observed on each side of the mantle at a shell length of 320 μm, and the rudiments increased in number and size until the end of the brooding period. During metamorphosis the gill filaments increased in number from 5 or 6 to between 7 and 9. The loss of the velum and the absence of functional gill filaments during metamorphosis are consistent with previous observations of weight loss during this critical period of the life history, because the newly settled juvenile lacks the ability to remove particles from suspension. The end of metamorphosis (100% of spat with dissoconch edge) was reached 36 h after larval settlement, when the gill filaments began to grow cilia, which increased in density and differentiated as the spat developed and acquired the capability of suspension-feeding, accounting for the increase in body weight previously recorded during this stage. The larval rudiments gave rise to the inner demibranchs. The outer demibranchs were observed 10 days after settlement, located between the inner demibranch and the mantle. In 1-month-old spat, the gill did not show differentiation between primary and secondary filaments, indicating that the heterorhabdic condition characteristic of adult oysters had yet to be attained. Received: 11 December 1998 / Accepted: 21 August 2000     

Reproduction of the invasive slipper limpet, Crepidula fornicata, in the Bay of Brest, France

The reproduction of Crepidula fornicata was studied in the Bay of Brest in order to characterise the first step of the reproductive cycle of this invasive species. The survey was carried out from 2000 to 2003 and different parameters were measured, namely, the percentage of the different sexual stages, the straight length of the shell and the percentage of brooding females using a survey of the embryonic development and the fecundity. The juvenile frequency increases generally from mid-June or mid-August, depending on the year. In 2001 and 2003, a first peak was observed as early as May, but it was followed by a rapid disappearance of the individuals. The sex-ratio female/male increased from 0.22 to 0.46 between 2001 and 2003. The sex change between intermediates and females took place mainly in summer and was well marked in 2001 and 2003. The survey of the embryonic development in the egg capsules brooded by the females provided an annual phenology of the laying and hatching processes. The laying period extends from February to September with three to four major periods of egg-laying per year and corresponding hatching periods about 1 month later. Each female lays two to four times per year on average. The first egg-laying concerned fewer females than subsequent ones, except in 2003, and exhibited a higher fecundity. The annual mean of the number of eggs for each stage was not significantly different, thus indicating no significant mortality rate during embryonic development. For the C. fornicata population in the Bay of Brest, several reproductive characteristics tend to highlight its invasive capacity: (1) a long reproductive period, (2) reproduction in a ‘multi-trials’ process equivalent to a spreading out of the risks and (3) a relatively high fecundity.     

Reproductive habits and life cycle of the small clam Kingiella chilenica (Bivalvia: Cyamiidae) in an estuarine sand flat from the south of Chile

A population of the small clam Kingiella chilenica Soot Ryen 1959 was studied from March 1986 to December 1988 in an intertidal flat at Queule River, in the south of Chile. The life cycle and life history pattern of the bivalve were established contrasting population structure and dynamics to its reproductive habits. Individuals are gonochoristic and semelparous, presenting a typical annual life cycle. The species is a sequential brooder whose embryos undergo direct development. After the brooding season (summer through autumn), the adults disappear gradually (autumn through winter). Recruited juveniles overwinter during a relatively long period, undergoing rapid growth during the spring to attain the adult stage during the summer. The number of brooded embryos increases in proportion to adult length cubed. Life history traits of this bivalve are compared to those reported for other small brooder clams. Some basic tendencies become apparent when traits for semelparous versus iteroparous species are contrasted. As in other semelparous sequential brooders (Transennella tantilla, Gaimardia bahamondei), the relationship between brood size and shell length obseved in K. chilenica does not fit the allometry hypothesis for marine brooding invertebrtes that allometric constraints on the brooding space limit the fecundity of larger individuals. Also contrary to theoretical predictions, small body size does not limit the diversity of a clam's developmental patterns. Possible explanations for this finding are discussed.     

Combined effects of dissolved oxygen concentration and water temperature on embryonic development and larval shell secretion in the marine snail <Emphasis Type="Italic">Chorus</Emphasis><Emphasis Type="Italic">giganteus</Emphasis> (Gastropoda: Muricidae)

The present study was undertaken to determine the effects of both extracapsular oxygen concentration and temperature on embryonic development in Chorus giganteus. In normoxia increasing water temperature from 12°C to 18°C reduced by 15 days the median time required for the capsules to hatch. Hypoxia (oxygen content at 50% of air saturation) generated a low development rate and totally prevented both shell secretion and larval hatching from the egg capsule. Experimental transfer at weekly intervals, from normoxia to hypoxia and vice versa, induced a decrease and increase in the embryonic ash content, respectively, but did not affect the number of hatched larvae. Such an effect was more pronounced at 12°C than at 15°C or 18°C. The embryonic inability to produce a shell under hypoxia is likely to be a result of the low intracapsular oxygen concentration (IPO₂) generated as the combined effect of a low extracapsular oxygen concentration (environmental) added to the intracapsular embryonic oxygen demands, which lowers the IPO₂ still further. Under such conditions, a decrease in intracapsular pH is likely to take place, and, if so, embryos might divert carbonates away from shell calcification to balance such changes in pH.     

Variable within-brood maternal provisioning in newly extruded embryos of Homarus gammarus

Offspring quality of decapod crustaceans has been widely studied, with special emphasis on the sources of variability determining embryonic and larval quality. Nevertheless, maternal provisioning has commonly been overlooked as a potential source of offspring within-brood variability. In the present study, the existence of variable maternal provisioning was assessed through the analysis of the fatty acid (FA) profile of newly extruded embryos from different regions of the brooding chamber of Homarus gammarus. Significant differences in the FA profile of embryos sampled from different pleopods and sides of the brooding chamber were recorded. Significant deviations of the overall mean of each surveyed female were also observed for essential FA, particularly 20:4n-6, 20:5n-3 and 22:6n-3. Lipid energy available to fuel embryogenesis also varied among embryos sampled from different regions of the brooding chamber. Results suggest variable female investment at oocyte production, which may be amplified during the incubation period of developing embryos by differential lipid catabolism. For the first time, maternal provisioning is evidenced as an additional source for within-brood variability in the FA profile of embryos.     

Developmental and genetic evidence for the existence of three morphologically cryptic species of<Emphasis Type="Italic"> Crepidula</Emphasis> in northern Chile

The taxonomy of Crepidula has been based principally on shell morphology, but shell characteristics in this genus may be strongly influenced by the substrates they inhabit and are thus of limited use in classification. Four species in this genus are currently recognized from the Chilean coast, of which two, Crepidula dilatata and C. fecunda, are sympatric. These species are morphologically cryptic and differ only in their larval development: C. dilatata has indirect development with a planktonic phase, and C. fecunda direct development within egg capsules. The other two species, C. coquimbensis and C. philippiana, are species that occur within gastropod shells inhabited by hermit crabs and differ from the other species in internal morphology of the shell, developmental features, and geographic distribution. Analyses of nine morphological characters, eight developmental characters, and 26 enzymatic loci were carried out on four Crepidula populations in the Coquimbo region of northern Chile. Four populations of Crepidula were identified based on morphological, developmental, and protein electrophoresis features. Our results suggest the presence of C. coquimbensis plus three morphologically cryptic species including C. dilatata, C. fecunda, and a new previously unrecognized cryptic species. All four populations showed differences in larval development pattern. C. fecunda have indirect development, with free-swimming larvae. The remaining three species have intracapsular metamorphosis, but different modes of larval nutrition. C. dilatata have nurse eggs that are consumed by mechanical destruction; C. coquimbensis engulf nutritional embryos; and the new species eat nutritive embryos by rotation. Protein electrophoresis data support the specific condition of each group with different larval development and endorse the use of developmental differences in taxonomy of Crepidula. Genetic distance shows that C. dilatata and C. fecunda are closely related, and that C. coquimbensis is closer to them than to the new cryptic species.     

Growth and reproduction in the Antarctic brooding bivalve Adacnarca nitens (Philobryidae) from the Ross Sea

We present information on the reproductive biology, population structure, and growth of the brooding Antarctic bivalve Adacnarca nitens Pelseneer 1903, from the Ross Sea, Antarctica. Individuals ranging from 0.85 to 6.00 mm were found attached to a hydrozoan colony. This species shows low fecundity and large egg size, common to other brooding species. The minimum size at which oogenesis was detected was 2.3 mm and the minimum size at which brooding was evident was 3.9 mm. Embryos of a full range of developmental stages were brooded simultaneously in females. The population showed a log–normal distribution and results suggest non-periodic reproduction with continuous embryonic development. The reproductive traits of A. nitens are discussed in the context of circum-Antarctic species distribution and limitations to dispersal in brooding benthic invertebrates.     

Nutrition and development of brooded embryos in the brittlestar Amphipholis squamata: do endosymbiotic bacteria play a role?

To identify sources of nutrition potentially available to the yolk-deficient embryos of the brooding brittlestar Amphipholis squamata Della Chiaje, (= Axiognathus squamata, Thomas 1966), specimens were collected intertidally at all seasons (1986 through 1987) from Odiorne Point, Rye, New Hampshire and from Appledore Island, Isles of Shoals, Maine, USA. Ultrastructural, autoradiographic and immunohistochemical studies were made of adults and brooded embryos. Adult and embryonic tissues have morphological adaptations which support healthy, symbiotic bacteria (5 to 9 x 10⁶ colony forming units/adult brittlestar), while autoradiographic studies indicate direct uptake of labeled amino acids by eukaryotic host tissues and bacteria. Cell envelopes of subcuticular bacteria suggest that they are Gram negative and may belong in the genus Vibrio. Based on immunohistochemical localization, it appears that a single type of bacterium is present in large numbers under the cuticles of embryos and adults of A. squamata. This is the first study of the relationship between an echinoderm and a bacterium which includes isolation and immunohistochemical verification of the identity of the bacterial symbiont.     

Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi

Two ill-explored hypotheses might explain host castration by parasitic pea crabs. The ‘energy drain’ hypothesis states that castration is caused by host-derived nutrient consumption of parasites that ultimately diminishes host-energy intake. The ‘steric interference’ hypothesis states that castration occurs when parasites physically inhibit host reproduction. This study evaluated whether Calyptraeotheres garthi, a pea crab from the southwestern Atlantic, is a parasitic castrator and explored whether the two hypotheses above explain castration in the limpet Crepidula cachimilla. None of three studied limpet species brooded embryos during the reproductive season when infested by mature female pea crabs. Also, limpets of C. cachimilla infested by C. garthi did not reproduce during a 90-day experimental period while crab-free limpets did spawn embryos during this period. Limpets resumed reproduction soon after pea crabs were experimentally removed from their brooding chamber. Thus, C. garthi does castrate limpets, and castration is reversible. Pea crabs ‘steal’ food from limpets, and infested limpets did not modify their feeding behavior to counteract nutrient loss. Thus, infested limpets are expected to ingest less food which provides partial support for the ‘energy drain’ hypothesis. However, the limpet’s body condition increased or was not affected by pea crabs during the breeding season which argues against the same hypothesis. Furthermore, that limpets promptly recovered reproductive activity once pea crabs were experimentally removed, that castration was not induced by the smallest pea crabs in the population (that fill only partially the brooding chamber), and that parasitized limpets did exhibit fully mature ovaries, support the ‘steric interference’ hypothesis explaining parasitic castration.     

Differential timing of larval starvation effects on filtration rate and growth in juvenile Crepidula onyx

This study demonstrates that the timing of larval starvation did not only determine the larval quality (shell length, lipid content, and RNA:DNA ratio) and the juvenile performance (growth and filtration rates), but also determine how the latent effects of larval starvation were mediated in Crepidula onyx. The juveniles developed from larvae that had experienced starvation in the first two days of larval life had reduced growth and lower filtration rates than those developed from larvae that had not been starved. Lower filtration rates explained the observed latent effects of early larval starvation on reduced juvenile growth. Starvation late in larval life caused a reduction in shell length, lipid content, and RNA:DNA ratio of larvae at metamorphosis; juveniles developed from these larvae performed poorly in terms of growth in shell length and total organic carbon content because of “depletion of energy reserves” at metamorphosis. Results of this study indicate that even exposure to the same kind of larval stress (starvation) for the same period of time (2 days) can cause different juvenile responses through different mechanisms if larvae are exposed to the stress at different stages of the larval life.     

Temperature and salinity interactively impact early juvenile development: a bottleneck in barnacle ontogeny

When juvenile mortality or juvenile growth is impacted by temperature and salinity, these factors have a substantial effect on recruitment success and population dynamics in benthic ecosystems. Using freshly settled cyprids of Amphibalanus improvisus, we investigated the combined effects of temperature (12, 20 and 28 °C) and salinity (5, 15 and 30 psu) on early juvenile stage performance. Mortality as well as size (basal diameter, dry weight, and ash-free dry weight) was monitored for a period of 40 days. Mortality was high (42–63 %) during the first week following attachment, regardless of the temperature and salinity treatments. Subsequently, mortality and size were interactively influenced by temperature and salinity. Highest mortality and lowest size of juveniles occurred at lowest temperature (12 °C) and salinity (5 psu). Apparently, low temperature (12 °C) narrowed the barnacles’ salinity tolerance. Juvenile barnacles constructed more shell material compared to body mass at high temperature and high salinity, while a reverse situation was observed at low temperature and low salinity. Our results demonstrate that environmental changes can directly and/or indirectly alter patterns of survivorship and size. Warming and desalination as predicted for the Baltic Sea in the course of climate change may, however, act antagonistically and compensate each other’s isolated effect on barnacles.     

Reproduction in Anthelia glauca (Octocorallia: Xeniidae). I. Gametogenesis and larval brooding

Anthelia glauca Lamarck, 1816 is a gonochoric, external-brooding soft coral found in KwaZulu-Natal. It is reproductively active in the summer months. The development of gametes produced in late summer is arrested in winter. Several stages of gametes are found at the base of the polyps, and female polyps produce several cycles of larvae over an extended breeding period of 4 to 5 months. Larvae are brooded in a unique pharyngeal brooding pouch not yet described in other coral species. The brood pouch consists of an expansion of the pharynx with constrictions proximal and distal to the embryos and larvae. Our data suggest that egg transfer and fertilization occur at full moon and the mature larvae are released after new moon. Zooxanthellae are absent in A. glauca oocytes, but zooxanthella infestation commences at the immature larval stage. Received: 15 July 1997 / Accepted: 12 March 1998     

Oxygen-dependent asynchrony of embryonic development in embryo masses of brachyuran crabs

Among brooding species, passive and active means to provide oxygen to embryos can be observed. Among passive oxygen providers, lower oxygen availability in the center than at the periphery of embryo masses seems to delay development of inner embryos. We investigated the differences in patterns of oxygen supply to the periphery and the center of embryo masses in two active oxygen providers, the brachyuran crabs Cancer setosus and Homalaspis plana, and evaluated the consequences on: (1) the proportion of time that early- and late-stage embryos were exposed to low or high oxygen partial pressure (PO₂), (2) oxygen consumption of the embryos from the center (inner) and the periphery (outer) of the embryo mass at those PO₂ levels that the embryos experience throughout development, and (3) development of inner and outer embryos. We found that oxygen availability in the embryo masses of brachyuran crabs exhibited dramatic contrasts between the periphery and the center during early development and that these differences decreased throughout embryonic development. These dissimilar patterns of oxygen availability produced differences in the proportion of the time that the embryos were exposed to high and low PO₂ levels throughout development. PO₂ affected oxygen consumption of the inner and outer embryos in the same fashion, but the oxygen demand of inner embryos was lower. Furthermore, development of inner embryos was delayed, in comparison to outer embryos of the same female. We suggest that the asynchrony in the development of inner embryos, in comparison to outer embryos, is due to oxygen limitation, since oxygen availability affects embryonic oxygen consumption. The differences between development of inner and outer embryos is relatively small, when compared to other marine invertebrates, probably because female crabs are able to adjust oxygen supply to the embryos according their needs, while passive oxygen providers are not. However, active oxygen provision may affect investment in reproduction. Our results could have important implications both on studies of larval development and survival and in understanding the life-history tradeoffs of aquatic invertebrates.     

Sexual reproduction in solitary corals: Overlapping oogenic and brooding cycles,and benthic planulas in Balanophyllia elegans

The temperate solitary coral Balanophyllia elegans Verrill, 1864 was collected monthly between January 1977 and August 1978 off the California coast. B. elegans reproduces only sexually, is gonochoric, and broods its embryos. Males are ripe only in late summer, but oocytes and embryos (ca. 40 per female) are found throughout the year. The presence of oocytes and embryos throughout the year may be the result of very long, overlapping oocyte growth and embryonic developmental times. Large, crawling, benthic planulas are released mainly in the winter. The skeletal design of the corallum of B. elegans accommodates the brooding of unusually large embryos; this design may be indicative of brooding large embryos in other species of corals, particularly dendrophyllids.     

Brooding and development of <Emphasis Type="Italic">Anasterias minuta</Emphasis> (Asteroidea: Forcipulata) in Patagonia,Argentina

Brooding, embryonic and larval development, and the influence of environmental and biological factors in tidepool habitats were studied in the sea star, Anasterias minuta, at various sites along ~220 km of the Patagonian coast. This species has a benthic, lecithotrophic development that includes eight distinct developmental stages. A larval organ, the connection cord, is developed from a small preoral lobe at early stages of development and becomes larger and thinner at advanced stages. Fecundity and average egg size increased with female body size. The regression of log egg number to log sea-star size and weight at different sites had a slope significantly less than 3.0, resulting in negative allometry and indicating that brood capacity was limited in large females. Development was generally synchronous among sites, but varied within each brood at advanced stages, with more developed brooded larvae located at the periphery of the brood mass. Brooding was synchronous among various populations at different years and spatial scales, and extended over a period of 8 months. The highest proportion of brooding females occurred during May and June (austral winter). Juveniles were released mainly during September. The likelihood of finding brooding sea stars decreased with increasing sea water temperature, tidal height, and wave exposure, and increased with increasing body size. Both body size of brooding females and brooding rate were higher in the infralittoral fringe than at midlittoral levels. A revision of the current model of brooding behavior and development among forcipulate sea stars is given.     

Origin,morphology and fate of the nonmineralized shell of Coryphella salmonacea,an opisthobranch gastropod

Little is known about initial shell formation in molluscs or about the possible functions of the embryonic shell field invagination (SFI). The present paper describes formation and loss of an unusual shell in embryos of the nudibranch Coryphella salmonacea (Couthouy, 1838), collected in February–March, 1981–1984. The first organic shell material was attached to shell field cells just outside the SFI at two weeks after fertilization (5°C). As viewed with transmission electron microscopy, the organic shell in section consisted of two electron dense layers having a total thickness of 16 nm. The shell continued to grow through at least the fifth week of encapsulated development. In the eighth week, the shell still covered the visceral mass; there was no evidence that mantle tissue reflexed and covered the shell or that shell materials were resorbed by the mantle. The shell and sometimes the operculum were discarded within the embryonic capsule prior to hatching at the end of Week 8. The cup-like shell is unusual in that it was shed as a wrinkled organic sheet which apparently lacked mineralization. Fully-developed shells were non-birefringent and did not produce calcium peaks when examined by electron microprobe. Both the location of the first organic shell material outside the SFI and the apparent absence of shell mineralization in the presence of an SFI are consistent with the hypothesis that the SFI is nonsecretory. C. salmonacea is probably in the evolutionary process of losing its shell, a structure of little or no function during encapsulated, nonplanktonic development.Contribution No. 130 of the Marine Science Laboratory, Northeastern University