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.     

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.     

Reproduction and sex reversal of the solitary vermetid gastropod<Emphasis Type="Italic"> Serpulorbis arenarius</Emphasis>

The reproductive biology of the Mediterranean vermetid gastropod Serpulorbis arenarius, a subtidal sessile solitary species that lives in shady rocky communities, was studied at two localities south-east of the Iberian Peninsula. Its population density is usually low, with specimens sometimes sparsely distributed. Its shell often appears to be covered by epibiotic organisms. The sex ratio is biased toward males (63%) in the populations of SE Spain, and the results point towards hermaphroditism with alternating sexuality. The results obtained suggest that all specimens are first males, change to females under some as yet unknown condition and, after the ovogenesis cycle has been completed, revert to the original sexual state (male). The possible adaptive forces that favour hermaphroditism in this species are discussed, and we hypothesise that the seizure of a spermatophore by males may stimulate sex change to female. Brooding females (51% of females studied) were found from March to December. In males, histological study of testes revealed that spermatogenesis seems to occur throughout the year. Females brooded between 5 and 28 (=15) egg capsules, which were attached by stalks to the inner surface of the shell. It is noteworthy that the gonads of two of the specimens brooding egg capsules were developing testes. The newly laid egg capsules were filled with an organic intracapsular matrix, in which 40–153 (=94) eggs were embedded. The mean diameter of the uncleaved ova was 352.5 µm. The organic intracapsular matrix and some nurse eggs were used as an extra-embryonic food source. Hatching occurred at an advanced veliger stage, immediately followed by metamorphosis. Therefore, the larval development of S. arenarius is of a lecithotrophic intracapsular type, with a short, free-swimming/crawling phase.Communicated by O. Kinne, Oldendorf/Luhe     

Factors affecting the allocation of paternal care in waterbugs (Belostoma flumineum Say)

Summary Male giant waterbugs (Belostoma flumineum Say) brood eggs oviposited on their dorsa by conspecific females. Laboratory observations indicate that viable egg pads are occasionally discarded before hatching. Theory predicts that such behavior should occur only if the costs incurred by brooding exceed the benefits of hatching the egg pad. We studied the effects of egg pad size, time invested in brooding, and egg viability upon the continuation of paternal care in the giant waterbug. We found that smaller egg pads are less likely to hatch than larger ones, and males appear to be less likely to discard egg pads as temporal investment increases. However, the inviability of eggs did not appear to affect the probability of an egg pad being discarded. Males of this species appear to have evolved a decision-making process involving the continuation of paternal care. Offprint requests to: K.C. Kruse     

Possible mutualism between females of the subsocial membracid Polyglypta dispar (Homoptera)

Summary Female Polyglypta dispar membracids facultatively guard egg masses or oviposit into masses guarded by other females. Defending females repel at least some enemies of both eggs and nymphs. Eggs of guarding females may be partially protected from parasitism by the presence of additional eggs laid by other females. Females sometimes desert egg masses or groups of nymphs, and undefended masses are sometimes adopted by other females. Some individuals remain on or near the plant where they grew up, and littermates sometimes oviposit into the same egg mass. Some copulating pairs are littermates, while others are not. Females with larger numbers of mature and nearly mature eggs in their ovaries are less likely to defend egg masses, and females desert smaller groups of nymphs more often.     

Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting

The probability of successful dispersal by sessile benthic invertebrates is thought to strongly influence their geographic distribution and population genetics. Generally, species with long-lived planktonic larvae are expected to exhibit wider distribution patterns than those species which brood their young, due to their presumably greater potential for dispersal. In some cases, however, brooding species exhibit broad distributions and show evidence of genetic exchange with geographically distant populations. One potential factor that has been invoked as an expianation is dispersal by floating and rafting of adults and egg masses. Several studies have shown that it is possible for sessile adults to disperse on the order of several to many thousand kilometers by rafting on debris in ocean currents. With very few exceptions, however, direct evidence of rafting in the open ocean has been lacking. We present evidence of long-distance (1300 to 2000 km) dispersal of a brooding pelecypod,Gaimardia trapesina (Lamarck, 1819), in the Southern Ocean in the vicinity of Cape Horn, the Falkland Islands, and the antarctic island South Georgia (54°S; 37°W). Data on survival and fecundity rates ofG. trapesina and the prevalence of kelp rafts collected during the austral winter of 1993 indicate that dispersal by rafting can occur over ecologically relevant time scales and could potentially serve as a significant means of genetic exchange between populations.     

“Egg dumping” in lace bugs (Gargaphia solani,Hemiptera: Tingidae)

Summary Data are presented which document that females of the subsocial lace bug, Gargaphia solani lay eggs in the nests of conspecifics whenever the opportunity arises. Because of an inverse relationship between time invested in maternal care and fecundity, maternal behavior in G. solani is an ecologically expensive trait that is adaptive only in the face of heavy predation on eggs and nymphs. By facultatively utilizing the maternal defensive behavior of conspecifics, it is possible for egg donors to protect their progeny from predators without limiting fecundity. Whenever possible, females oviposit in recently established egg masses of conspecifics. While guarding their own eggs, egg recipients inadvertently protect the eggs of egg donors. Egg donors need not establish and guard their own masses as long as there are females with egg masses in the vicinity. Instead, egg donors are free to lay as many eggs as physiologically possible by avoiding long periods of maternal care.Published with the approval of the Director of the Delaware Agricultural Experiment Station as Miscellaneous Paper No. 1048, Contribution No. 544 of the Department of Entomology and Applied Ecology, University of Delaware, Newark, Delaware, USA     

Brooding behaviour and reproductive success in two species of free-living simultaneous hermaphrodites

Although polyclads are amongst the most structurally simple of the triploblastic metazoans, they adopt a wide range of reproductive strategies. Parental care behaviour in this group is yet to be quantified for any species. We assessed the significance of brooding behaviour to the reproductive success of two free-living marine flatworms. Echinoplana celerrima and Stylochus pygmaeus were collected from the field and placed in pairs in containers of filtered seawater where they laid batches of eggs. Both parents were then removed from half of the containers and the brooding behaviour and hatching success of eggs were quantified. There were interspecific differences in brooding behaviour. Egg masses were covered by one E. celerrima parent for 12 ± 2% of time, whereas egg masses of S. pygmaeus were covered by one or both parents simultaneously for 85 ± 8% of time. Egg batches were abandoned by both species immediately prior to the onset of hatching (10–12 days). Hatching success was generally high (~90%) and brooding did not enhance the hatching success of eggs. We assessed the significance of parental care to hatching success of E. celerrima egg masses in the presence of three potential egg predators; in the presence of other organisms. E. celerrima devoted less time to brooding; however, hatching success was not affected. The amount of time spent brooding eggs differed greatly between the two polyclad species but was not essential to their reproductive success under benign conditions. Parental care may be of adaptive value under more stressful environmental conditions commonly experienced in estuarine environments such as lowered salinity, increased hypoxia or turbidity. Covering egg batches may play an additional role of advertising sexual status and a willingness to care for eggs.     

Apparent resource competition among embryos in the brood pouch of a male pipefish

Embryo success was studied in the paternally brooding pipefish Syngnathus typhle. During brooding, which lasts about a month, males provide embryos in their brood pouch with nutrients and oxygen via a placenta-like structure. Egg size depends on female size. In aquaria, males were mated with differently sized females to give the following treatments: M, mixed-egg-size broods of approximately half large and half small eggs; L, single-egg-size broods of large eggs; S, single-egg-size broods of small eggs; and F, field mated males. All males were kept in aquaria for a full brooding period. For each egg-size category, the number of newborn was compared with the number of eggs the male initially fertilized in his brood pouch. Within mixed-egg-size broods, a higher proportion of large eggs survived and large eggs resulted in heavier newborn than small eggs. Indeed, small eggs from a mixed-egg-size brood had significantly lower relative success (proportion of embryos surviving to birth) than those from a brood entirely composed of small eggs. The implication is that embryos compete for resources within the brood pouch, and that competitive success depends on egg size. Given that females produce eggs corresponding in size to their body size, and that females are known to compete indirectly for access to mates (i.e., the sex-roles are reversed), this intrabrood competition could be seen as an extension of female-female competition, but alternative explanations are discussed. Received: 28 April 1995/Accepted after revision: 28 October 1995     

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.     

An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusitriton oregonensis (Gastropoda)

Oxygen supply inside egg masses has been reported as a constraint of embryo development. Many species that enclose their eggs in jelly masses or ovicapsules have strategies to avoid or reduce intracapsular hypoxia. In some amphibian species, a decrease in the wall thickness of the egg capsule over time produces an increase in oxygen conductance of the wall, reducing the problem of intracapsular oxygen limitation. Previous studies of gastropods have reported a decrease in the thickness of the capsules during development. However, there are no studies relating capsule thinning to the oxygen limitation problem in this group. This study links the thinning of egg capsules with oxygen diffusion as a possible mechanism to reduce or avoid hypoxia inside the capsules of the gastropod Fusitriton oregonensis. Capsule thickness, capsule area, oxygen partial pressure inside and outside the capsule, and oxygen consumption of the embryos at early and late developmental stages were measured. The conductance and the diffusion coefficients of the capsule were estimated using these measurements. Results showed that (1) capsule thickness decreased throughout development by about 50%, (2) oxygen consumption of embryos increased from early to late stages, (3) oxygen partial pressure inside the capsule did not change during development, (4) conductance coefficient increased with time, and (5) estimation of diffusion coefficient was lower than amphibian egg jelly, shark capsules, egg fishes, and eggs of giant cuttlefish. The reduction in the thickness of the capsule wall and the associated increase in its conductance during embryonic development may reduce oxygen constraints, especially at late developmental stages.     

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     

Predation by the nemertean Carcinonemertes errans on eggs of the Dungeness crab Cancer magister

The nemertean Carcinonemertes errans is an important predator on the eggs of its host, the Dungeness crab Cancer magister. Each nemertean consumes an average of approximately 70 crab eggs during the host brooding period. The nemerteans, which apparently consume no other food during the host brooding period, convert crab egg tissue to worm tissue with an efficiency of 28.9% on a caloric basis. Epidemic levels of Carcinonemertes errans on the central California Dungeness crab population have resulted in the direct mortality of an average of 55% of the eggs produced by that population over the last 5 years, making C. errans probably the most numerically significant predator on these crabs.     

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.     

Brooding of the sub-Antarctic heart urchin, <Emphasis Type="Italic">Abatus cavernosus</Emphasis> (Spatangoida: Schizasteridae), in southern Patagonia

The reproductive cycle of the sub-Antarctic spatangoid sea urchin, Abatus cavernosus, was examined during a 2-year period in southern Patagonia, Argentina. The population studied is the northernmost known coastal population in the austral oceans, and is influenced by a greater annual range of seawater temperature than other Abatus species. The sex ratio of the overall A. cavernosus population did not differ significantly from 1:1, but was not homogeneous across size classes. A clearly defined annual reproductive cycle was found. Spawning occurred from May to July and was synchronous between sexes. Females were observed to be brooding within a 9-month period, from May to February. Juveniles were released during the austral summer, from January to February. The length at which 50% of the females were brooding occurred at a test length of 25.9 mm. A. cavernosus had a large egg size (mean diameter = 1.4 mm) and low fecundity (maximum = 57 eggs per female) compared to closely related species. The number of eggs within each brood pouch was highest in larger anterior brood pouch, which is close to two gonopores, as opposed to the other anterior and two smaller posterior pouches. Significant interannual variation was observed in gonad cycles, fecundity, and embryo development such as: brood size decreased during 2001; adjusted gonad dry weight and fecundity were higher during 2003. Hypotheses concerning the gonadal and brooding cycles and fecundity of sub-Antarctic and Antarctic Schizasteridae are discussed. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Reproductive isolation between intertidal and subtidal<Emphasis Type="Italic"> Scoloplos armiger</Emphasis> (Polychaeta,Orbiniidae) indicates sibling species in the North Sea

Two distinct modes of development in the common polychaete Scoloplos armiger (O. F. Müller, 1776) occur in the North Sea region: holobenthic development in egg cocoons and pelagic larvae hatching from suspended eggs. In the northern Wadden Sea near the island of Sylt, we observed that egg cocoons are produced intertidally while pelagic larvae originate from the adjacent subtidal zone. A previous genetic comparison between these subtidal and intertidal populations revealed distinct gene pools, suggesting that reproductive differences are not phenotypic but heritable. In this study, crossbreeding experiments show that intertidal and subtidal populations are reproductively isolated. Couples with males and females from different habitats had no offspring. Production of egg cocoons is determined by female origin from the intertidal zone. Pelagic larvae occurred only in couples with subtidal females and subtidal males. Intertidal males have spermatozoa with heads twice as long as those from subtidal males and a significantly shorter flagellum. We suspect that deviating sperm morphology may cause the reproductive breakdown at the fertilization stage. Juveniles hatching from cocoons have shorter anal cirri compared to juveniles that metamorphosed from pelagic larvae. We conclude there to be two sympatric sibling species in S. armiger: 'type I' in intertidal areas, which have egg cocoons, no pelagic larvae, elongated sperm heads, shortened sperm flagella and anal cirri; and a subtidal 'type S', lacking egg cocoons but with pelagic larvae, short sperm heads, long sperm flagella and anal cirri.Communicated by O. Kinne, Oldendorf/Luhe     

The reproductive biology of Hymenaster membranaceus from the Rockall Trough,North-East Atlantic Ocean,with notes on H. gennaeus

Samples of the deep-sea spinulosan asteroid Hymenaster membranaceus Wyville Thomson were collected in a timeseries of 19 bottom trawls spanning the period April 1978 to October 1981 from a 2200 m-deep station in the northern Rockall Trough. The reproductive biology of this species was studied from histological sections of the gonad, and compared with that of H. gennaeus H. L. Clark which was collected in the same hauls. At first sexual development, oogonia develop in nests surrounded by small accessory cells. Previtellogenic oocytes remain in the periphery but, at maturity, oocytes ranging up to 1 100 m fill the ovary. A variety of accessory cells pack the lumen and may be nutritive or degenerative. It appears that a small number of oocytes are spawned intermittently, but there is no evidence of overproduction and break-down of superfluous oocytes. A few large oocytes become senescent and undergo internal break-down, releasing periodic acid Schiff-positive material into the lumen. Size-frequencies of oocytes indicate that eggs may be spawned as a continuous slow release, and there is no evidence of reproductive synchrony between or within samples. On reaching maturity, males appear always to be ready to release spermatozoa. Spawning is probably stimulated by egg release during chance encounters with mature females. There is no evidence for brooding, and from the large size and yolky nature of the egg direct lecithotrophic development at or near the seabed is inferred. A limited histological study of H. gennaeus indicates that egg production is very similar, but the two species differ in the nature of the accessory cells and amorphous material filling the lumen.     

Local mate competition in the solitary parasitoid wasp <Emphasis Type="Italic">Ooencyrtus kuvanae</Emphasis>

Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.     

Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females

Females mating with multiple males may obtain direct benefits such as nuptial gifts or paternal care or indirect (i.e. genetic) benefits resulting in higher-quality offspring. While direct benefits are easily identified, it is difficult to determine indirect benefits, and it is hence largely unclear how they are obtained. This is particularly true in species with external fertilisation, where females seem to have little control over fertilisation. In cichlids, most maternal mouthbrooders show sequential multiple mating, where females visit several males for egg deposition. Genetic data revealed that multiple paternity of eggs and young in the mouth of females is common, but behavioural data of female spawning decisions are missing. Here, we test four hypotheses to explain female multiple mating in the maternally mouthbrooding cichlid, Ophthalmotilapia ventralis: (1) fertilisation insurance, (2) genetic bet-hedging, (3) female choice and (4) ‘sperm shopping’ (i.e. induction of sperm competition resulting in sexually selected sperm). Detailed observations of spawning behaviour in the field combined with histological analyses of the male reproductive organs suggest that fertilisation insurance, genetic bet-hedging and pre-mating female choice are unlikely to explain the sequential female multiple mating in O. ventralis. Instead, cryptic female choice by sperm shopping, i.e. post-mating sexual selection, is most compatible with our data and might be the major ultimate cause of multiple mating in females of this species and of mouthbrooding cichlids with maternal care in general. Our study provides new insight into ultimate causes of sequential polyandry in species with external fertilisation, as hitherto post-mating sexual selection by cryptic female choice has been assumed to be incompatible with external fertilisation mechanisms except by components of the ovarian fluid.     

Observations on Octopus joubini: Some aspects of reproductive biology and growth

Observations were made on the brooding behavior of 10 laboratory reared female Octopus joubini, including egg laying, care of the eggs, feeding during brooding, and survival of the female from the onset of egg laying. Data concerning the numbers of eggs laid by each female and hatching (duration, frequency, correlation of duration to water temperature, etc.) are given. The newly hatched octopuses (whose ages were determined within 24 h) were fed Uca spp. to determine their growth rate from hatching to 4 months of age. In addition, some specimens were presented with a variety of foods that were easily accessible in the laboratory or field in an effort to find a food suitable for mass culture.Contribution No. 1830 from the University of Miami, Rosenstiel School of Marine and Atmospheric Science.