The contribution of the facultative feeding period to echinoid larval development and size at metamorphosis: a comparative approach

Planktotrophic invertebrate larvae have two dissociable stages during development, a facultative feeding period, whose length is determined by the amount of maternal provisioning in the egg, and an obligate feeding period, whose length is determined by the quantity of exogenous energy needed to reach metamorphic competence. Here we set out to experimentally test the impact of feeding during the facultative feeding period at two food concentrations (limiting and nonlimiting) on larval development time and juvenile quality. We used two closely related subtropical sand dollar species that differ in the quantity of maternal investment for these comparisons: Leodia sexiesperforata (large egg, long facultative feeding period) and Mellita tenuis (small egg, short facultative feeding period). We found that feeding during the facultative period accelerates development to metamorphosis only in M. tenuis and only at the high food ration. Feeding during the facultative feeding period had no effect on development time for M. tenuis at a food limiting concentration and for L. sexiesperforata at either food concentration. Furthermore, we found feeding during the facultative period to significantly increase quantity of carbohydrates and lipids at metamorphosis only for M. tenuis in nonlimiting food concentration. Thus, our data reveal a two-fold benefit of the facultative feeding period for a poorly provisioned species under high food conditions but little effect on a well-provisioned species. We discuss our results in reference to McEdward's [McEdward, L.R., 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am. Nat. 150, 48-72] facultative feeding model.     

Egg components, egg size, and hatchling size in leatherback turtles

Relationships between egg size, egg components, and neonate size have been investigated across a wide range of oviparous taxa. Differences in egg traits among taxa reflect not only phylogenetic differences, but also interactions between biotic (i.e., maternal resource allocation) and abiotic (i.e. nest environment conditions) factors. We examined relationships between egg mass, egg composition, and hatchling size in leatherback turtles (Dermochelys coriacea) because of the unique egg and reproductive characteristics of this species and of sea turtles in general. Albumen comprised 63.0%+/-2.8% (mean+/-S.D.) of egg mass and explained most of the variation in egg mass, whereas yolk comprised only 33.0%+/-2.7%. Additionally, leatherback albumen dry mass was approximately 16% of albumen wet mass. Whereas hatchling mass increased significantly with egg mass (n = 218 clutches), hatchling mass increased by only approximately 2 g for each 10 g increase in egg mass and was approximately 10-20 g greater than yolk mass. Taken together, our results indicate that albumen might play a particularly significant role in leatherback embryonic development, and that leatherback eggs are both capable of water uptake from the nest substrate and also possess a large reservoir of water in the albumen. Relationships between egg mass and egg components, such as variation in egg mass being largely explained by variation in albumen mass and egg mass containing a relatively high proportion of albumen solids, are more similar to bird eggs than to eggs of other non-avian reptiles. However, hatchling mass correlates more with yolk mass than with albumen mass, unlike patterns observed in bird eggs of similar composition.     

The relationship among egg size,density and food level on larval development in the wood frog (Rana sylvatica)

Summary Although inter- and intraspecific variation in egg size among amphibians has been well documented, the relationship between egg size and fitness remains unclear. Recent attempts to correlate egg size intraspecifically with larval developmental patterns have been equivocal. In this study the development of larvae derived from large eggs and small eggs, from a single population in Maryland were compared under a range of food levels and larval population densities. Both food level and density had significant effects on the length of the larval period and size at metamorphosis. However, the response among larvae derived from different egg sizes was not additive. At low densities and high food levels, larvae from small eggs had longer larval periods and a larger size at metamorphosis than larvae derived from large eggs. In contrast, at high densities larvae from small eggs had longer developmental periods but were smaller at metamorphosis than larvae from large eggs. In addition, larvae from small eggs were more sensitive to density irrespective of food level. These results suggest that optimal egg size is correlated with environmental factors, which may explain the maintenance of both geographic and within population variation in egg size commonly observed in amphibians.     

Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching

Recent literature suggests that heterotrophic protists could improve the biochemical constituents of poor quality algae for subsequent use by higher trophic levels, a phenomenon dubbed “trophic upgrading”. We conducted experiments to test trophic upgrading effects on the omnivorous calanoid copepod Acartia tonsa. Two heterotrophic protists, Oxyrrhis marina and Gymnodinium dominans, were grown on three algal species of different nutritional qualities: Dunaliella tertiolecta, Isochrysis galbana and Rhodomonas salina. In parallel incubations, the copepods were fed the heterotrophic protists or the algae that the protists grew on. We measured the ingestion rate, egg production rate and egg hatching success of the copepods in each treatment. Comparison of the egg production efficiency (EPE; egg carbon production/carbon ingestion×100%) between parallel diet treatments allowed us to calculate the trophic upgrading index (TUI; ratio of EPE-heterotrophic protist to EPE-alga). The copepods ingested similar amount, or 20-30% more algae than heterotrophic protists. Daily rations ranged 50-122% of body C per day. Copepods feeding on O. marina that grew on D. tertiolecta had higher egg production rate and egg hatching success than copepods feeding on D. tertiolecta directly, and the resultant TUI between the two treatments was 19.7. Similarly, the copepod egg production was improved by G. dominans that grew on D. tertiolecta and the resultant TUI was 23.3. TUI was near 1 between I. galbana treatment and the parallel heterotrophic protist treatments, indicating no or little trophic upgrading effects on the copepod's egg production. However, egg hatching success was significantly lower with G. dominans growing on I. galbana. O. marina that grew on R. salina induced a lower EPE relative to the alga itself, yielding a TUI of less than 1. Biochemical data showed that the heterotrophic protists contained eicosapentanoic acid (EPA) and docosahexanoic acid (DHA) even when they fed on alga that lacked these essential fatty acids, which may explain some of the observed trophic upgrading effects and species-specific differences in our experiments. However, our data also suggested that dietary EPA and DHA could not be the sole factors regulating the copepod's reproductive output, and that egg production and egg hatching appeared to have different nutritional requirements and respond differently to the copepod's diets.     

Developmental plasticity in larval development in the echinometrid sea urchin Evechinus chloroticus with varying food ration

Developmental plasticity in the morphology of planktotrophic echinoid larvae has been studied primarily in temperate sea urchins from the Northern Hemisphere. These studies have shown that echinoplutei with reduced food ration generally respond by increasing the length of the larval arms, and thus the length of the ciliated band, and delaying formation of the rudiment. Using the endemic New Zealand sea urchin Evechinus chloroticus we tested for the presence of developmental plasticity in larvae fed a high or low algal food ration (6000 or 600 Dunaliella cells/ml), or with no algal food. Our results show that developmental plasticity in larval form is seen in a Southern Hemisphere representative of the Family Echinometridae, but the general pattern of longer arms with low food ration was only seen in the earliest part of development. Larvae in the High food treatment were largest in all dimensions and formed rudiments within 23 days of fertilization. Larvae fed a low algal ration or no algal food stalled at the four-arm echinopluteus stage, and were significantly smaller in size, and differed in shape, when compared in a multivariate analysis to the High food treatment. We suggest that the response of echinoplutei to low levels of particulate food is a species-specific trait, depending in part on the level of dependence of the larvae on exogenous food. Previous studies in Lytechinus variegatus, and the present study with E. chloroticus, suggest that in species where development stalls at the four-arm stage, the pattern of longer larval arms with low food ration will only be seen during the initial early period of larval growth. Additionally our results show that there can be significant variation in larval morphology between replicate jars in the same feeding treatment, suggesting that future research on developmental plasticity should also consider differences in larval morphology between culture containers.     

Expression of 'segmentation' genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans

Polychaete annelids and arthropods are both segmented protostome invertebrates. To investigate whether the segmented body plan of these two phyla share a common molecular ground pattern, we report the developmental expression of orthologues of the arthropod segment polarity genes engrailed (en), hedgehog (hh), and wingless (wg/Wnt1) in larval and juvenile stages of the polychaete annelid Capitella sp. I and en in a second polychaete, Hydroides elegans. Temporally, neither Wnt1 nor hh are detected in the segmented region of the larval body until after morphological segmentation is apparent. Expression of CapI-Wnt1 is limited to a ring of ectoderm marking the future anus during larval segmentation. CapI-hh is expressed in a ring of the hindgut internal to that of CapI-Wnt1, as well as in a subset of ventral nerve cord neurons, anterior gut tissue, and mesoderm. In both H. elegans and Capitella sp. I, en is expressed in a spatially and temporally dynamic manner in segmentally iterated structures as well as a population of cells that migrate internally from ectoderm to mesoderm, possibly representing a population of ecto-mesodermal precursors. Significantly, the expression patterns we report for wg, en, and hh orthologues in Capitella sp. I and for en in larval development of H. elegans are not comparable to the highly conserved ectodermal segment polarity pattern observed in arthropods at any life history stage, consistent with distinct origins of segmentation between annelids and arthropods.     

Morphogenesis and proliferation of the larval brain glia in Drosophila

Glial cells subserve a number of essential functions during development and function of the Drosophila brain, including the control of neuroblast proliferation, neuronal positioning and axonal pathfinding. Three major classes of glial cells have been identified. Surface glia surround the brain externally. Neuropile glia ensheath the neuropile and form septa within the neuropile that define distinct neuropile compartments. Cortex glia form a scaffold around neuronal cell bodies in the cortex. In this paper we have used global glial markers and GFP-labeled clones to describe the morphology, development and proliferation pattern of the three types of glial cells in the larval brain. We show that both surface glia and cortex glia contribute to the glial layer surrounding the brain. Cortex glia also form a significant part of the glial layer surrounding the neuropile. Glial cell numbers increase slowly during the first half of larval development but show a rapid incline in the third larval instar. This increase results from mitosis of differentiated glia, but, more significantly, from the proliferation of neuroblasts.     

The effect of food limitation on gonad development and egg production of the planktonic copepod Calanus finmarchicus

Calanus finmarchicus, one of the dominant copepods species of the North Atlantic, often encounters low food concentration or quality during the reproductive period; however, our knowledge on the effect of these conditions on reproduction processes is scarce. The present study combines experiments with histological observations to describe the response of C. finmarchicus to limited food focussing on (1) oocyte maturation processes, (2) gonad morphology, (3) egg production rates as a function of spawning frequency and clutch size, and (4) the fuelling of egg production by measuring carbon and nitrogen content of the females. In the laboratory, C. finmarchicus females were exposed to 0, 10, 50, 150 or >300 μg C l⁻¹ for several days. To account for food quality and season, reproductive activity was compared in April and July 1999 between females feeding on diatoms or dinoflagellates. The effect of feeding history was studied in February with females fed and starving prior to the experiment. Feeding conditions had severe effects on oocyte maturation process. Hence, egg production varied significantly with food concentration and quality, season and feeding history due to variation in both clutch size and spawning frequency. Clutch size differed by a factor of 2-4 between food limited and well fed females, and is thus an important parameter for modelling egg production. Changes in clutch size were related to changes of the number of maturing oocytes in the females gonads indicating that the latter can be used to precise the prediction of egg production from preserved samples. The proportion of females carrying at least some mature oocytes was relatively high at low food availability. Apparently, these females used internal body reserves as the carbon and nitrogen content decreased significantly under these conditions. These results indicate that C. finmarchicus embarks on the strategy to enable reproduction in all or many females of a population at low rates when feeding conditions are unfavourable.     

Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird

The importance of avian egg components in the determination of hatchling size and quality has yet to be fully evaluated. In the first experiment, 20% of the albumen and/or the yolk was removed from chicken eggs to determine the impact of each egg component on metabolism and various size measures in near-term embryos. Results show that metabolic rate, dry body mass, and internal organ mass are largely independent of egg composition. Removal of albumen resulted in a decrease in wet body mass corresponding to decreases in water content in the body and the yolk sac, and decreased tibiotarsus length. Removal of yolk resulted in no change in body mass, but decreases in both wet and dry yolk sac mass. In a second experiment, removal of 15% of either egg component led to reductions in hatchling mass similar to those observed in whole near-term embryos. Albumen, as the primary source of water in the egg, is the primary determinant of hatchling size and may influence hatchling success through size-related limiting factors. Differences in yolk content may influence neonatal quality as a nutritional supplement, but seem not to result in greater tissue formation during embryonic development. Accepted: 2 September 1997     

New insights into the larval development of Macandrevia cranium (Müller, 1776) (Brachiopoda: Rhynchonelliformea)

The terebratulid Macandrevia cranium (Müller, 1776) is a representative of articulate brachiopods. However, little is known about its embryology and larval development. In order to obtain reproducible results we used a strict protocol of artificial fertilization under controlled temperature conditions as a basis for our morphological study. Sampling of embryos or developing larvae at frequent intervals led to the most comprehensive collection of preserved developmental stages, ranging from early zygotes to late three-lobed stage larvae. SEM studies of all these stages showed that the development of M. cranium is similar to that of other terebratulid brachiopods. This includes the presence of four bundles of larval setae in three-lobed stage larvae. Our results contradict earlier observations on the development of M. cranium and show that this species exhibits more typical features of articulate brachiopod development than previously thought.     

Larval feeding substrate and species significantly influence the effect of a juvenile hormone analog on sexual development/performance in four tropical tephritid flies

The juvenile hormone (JH) analog methoprene reduces the amount of time it takes laboratory-reared Anastrepha suspensa (Caribbean fruit fly) males to reach sexual maturity by almost half. Here, we examined if methoprene exerted a similar effect on four other tropical Anastrepha species (Anastrepha ludens, Anastrepha obliqua, Anastrepha serpentina and Anastrepha striata) reared on natural hosts and exhibiting contrasting life histories. In the case of A. ludens, we worked with two populations that derived from Casimiroa greggii (ancestral host, larvae feed on seeds) and Citrus paradisi (exotic host, larvae feed on pulp). We found that the effects of methoprene, when they occurred, varied according to species and, in the case of A. ludens, according to larval host. For example, in the case of the two A. ludens populations the effect of methoprene on first appearance of male calling behavior and number of copulations was only apparent in flies derived from C. greggii. In contrast, males derived from C. paradisi called and mated almost twice as often and females started to lay eggs almost 1 day earlier than individuals derived from C. greggii, but in this case there was no significant effect of treatment (methoprene) only a significant host effect. There were also significant host and host by treatment interactions with respect to egg clutch size. A. ludens females derived from C. paradisi laid significantly more eggs per clutch and total number of eggs than females derived from C. greggii. With respect to the multiple species comparisons, the treatment effect was consistent for A. ludens, occasional in A. serpentina (e.g., calling by males, clutch size), and not apparent in the cases of A. obliqua and A. striata. Interestingly, with respect to clutch size, in the cases of A. ludens and A. serpentina, the treatment effect followed opposite directions: positive in the case of A. ludens and negative in the case of A. serpentina. We center our discussion on two hypotheses (differential physiology and larval-food), and also interpret our results in light of the life history differences exhibited by the different species we compared.     

Seed development in Malpighiaceae species with an emphasis on the relationships between nutritive tissues

Malpighiaceae ovules have a well-developed nucellus; previous observations indicate that during seed development, the endosperm does not proliferate, thus, remaining scarce. This study aimed at identifying the nutritive tissues during seed development in Malpighiaceae, focusing especially on the endosperm. We analysed the seed development of Janusia mediterranea, J. occhionii, Mascagnia cordifolia, and Tetrapterys chamaecerasifolia, which were collected and processed by traditional methods for light microscopy. Ovules are subcampylotropous, crassinucellate and unitegmic in Janusia and bitegmic in M. cordifolia and T. chamaecerasifolia. The nucellus is well developed and protrudes through the micropyle, touching the funicular obturator. During development, a pachychalaza is formed, and the integuments coalesce in bitegmic species. Through a series of nucellar cell divisions, the perisperm is formed. In Janusia species, the endosperm is not produced. In M. cordifolia and T. chamaecerasifolia, the endosperm is nuclear, but it is scarce and ephemeral. The mature seed is exalbuminous, and the perisperm is consumed, and thus, the mature embryo is total. The absence of endosperm in Janusia is newly observed for the family and indicates functional transfer for the abundant perisperm.     

Murine immune responses to a novel schistosome egg antigen, SmEP25

Pathology in schistosomiasis consists of granuloma formation around parasite eggs. There is considerable variation in the severity of disease in individuals with schistosomiasis, which may result from differential responses to egg antigens. The egg-induced immunopathology is mediated by CD4+ T helper cells sensitised to egg antigens. In this study, cellular responses to a 25-kDa fraction of egg proteins identified a novel T-cell antigen, SmEP25. The native SmEP25 elicited significant proliferative responses as well as gamma interferon (IFN-gamma), IL-2, IL-4, and IL-5 secretion in CD4+ cells from 8.5-week infected CBA and C57BL/6 mice. In C57BL/6 mice, proliferative responses to SmEP25 were relatively stronger than those directed against the major egg antigen Sm-p40, whereas in CBA mice the reverse was found. SmEP25 elicited stronger Th2 type response than Sm-p40 in both mouse strains. By comparison, recombinant SmEP25 elicited a smaller, Th1-polarised response, with significant IFN-gamma, low levels of IL-5 and essentially no IL-4. B-cell responses to SmEP25 coincided with the start of parasite egg production and SmEP25 protein was restricted to parasite eggs. The systematic identification of T-cell-sensitising egg components will lead to a better understanding of the processes involved in granuloma formation.     

Experimentally reducing clutch size reveals a fixed upper limit to egg size in snakes, evidence from the king ratsnake, Elaphe carinata

Snakes are free of the pelvic girdle's constraint on maximum offspring size, and therefore present an opportunity to investigate the upper limit to offspring size without the limit imposed by the pelvic girdle dimension. We used the king ratsnake (Elaphe carinata) as a model animal to examine whether follicle ablation may result in enlargement of egg size in snakes and, if so, whether there is a fixed upper limit to egg size. Females with small sized yolking follicles were assigned to three manipulated, one sham-manipulated and one control treatments in mid-May, and two, four or six yolking follicles in the manipulated females were then ablated. Females undergoing follicle ablation produced fewer, but larger as well as more elongated, eggs than control females primarily by increasing egg length. This finding suggests that follicle ablation may result in enlargement of egg size in E. carinata. Mean values for egg width remained almost unchanged across the five treatments, suggesting that egg width is more likely to be shaped by the morphological feature of the oviduct. Clutch mass dropped dramatically in four- and six-follicle ablated females. The function describing the relationship between size and number of eggs reveals that egg size increases with decreasing clutch size at an ever-decreasing rate, with the tangent slope of the function for the six-follicle ablation treatment being -0.04. According to the function describing instantaneous variation in tangent slope, the maximum value of tangent slope should converge towards zero. This result provides evidence that there is a fixed upper limit to egg size in E. carinata.     

Impacts of egg and larval size on survival and growth of Atlantic cod under different feeding conditions

Large eggs (1·38 mm) of Atlantic cod reared in the laboratory produced large larvae. However, large larvae had low survival rates. Results also indicated that the first few days' of growth of cod larvae mainly resulted in an increase in mass. Exogenous feeding tended to result in faster growth than endogenous feeding. In the delayed feeding groups (larvae not fed until 67 degree-days), larvae from large eggs grew faster than those from small eggs (1·28 mm) after feeding commenced, while there was no significant difference in growth rate within feeding groups. Compensatory growth was detected in the delayed feeding groups.     

Change in significance of feeding during larval development in the yellow-spotted longicorn beetle, Psacothea hilaris

Larvae of the west-Japan type yellow-spotted longicorn beetle, Psacothea hilaris (Coleoptera: Cerambycidae), show a long-day type photoperiodic response at 25 degrees C; under long-day conditions, larvae pupate after the fourth or fifth instar, while under short-day conditions, they undergo a few nonstationary supernumerary molts and eventually enter diapause. In the present study, the effect of food on the development and photoperiodic response of the larvae was examined with special reference to molting and pupation. Although the pupal body size was greatly affected by the food quality and the length of feeding, the critical day length for induction of metamorphosis at 25 degrees C was always between 13.5 and 14 h. Exposure to starvation of larvae reared on the standard diet revealed that the capability to pupate is acquired after a few days of feeding in the fourth instar. In the larvae that had acquired the capability to pupate, premature pupation was induced by exposure to starvation, indicating that feeding becomes dispensable long before it is normally terminated.     

Effects of egg size, parental origin and feeding conditions on growth of larval and juvenile cod Gadus morhua

An experimental study was performed to disentangle parental and environmental effects on the growth of Atlantic cod Gadus morhua larvae and juveniles. Eggs were collected during the spawning season from spawning pairs (families) kept separately in specially designed spawning compartments. Newly hatched larvae were released simultaneously into two mesocosms of 2500 and 4400 m³. Larval growth was monitored by sampling over a 10 week period, after which juveniles were transferred to on-growing tanks, where they were tagged and kept for up to 2 years. Maternal origin was determined by individual microsatellite genotyping of the larvae ( n = 3949, 24 families) and juveniles ( n = 600). The results showed significant positive correlations between egg size and larval size during the whole mesocosm period. Correlations, however, weakened with time and were no longer significant at the first tank-rearing sampling at an age of 9 months. Significant family-specific differences in growth were observed. The coefficient of variation ( c.v. ) was calculated in order to examine variation in standard length of larvae during the mesocosm period. Inter-family c.v. was on average 69% of intra-family c.v. Differences in zooplankton densities between the two mesocosms were reflected in larval growth, condition factor and c.v. Low food abundance appeared to reduce c.v. and favour growth of larvae that showed relatively slow growth at high food abundance. It is suggested that genetically determined variation in growth potential is maintained by environmental variability.     

Prefeeding larval development time is not correlated with egg size in regular echinoids (Strongylocentrotus species)

Summary

We compared prefeeding development times, from fertilized egg to prism larva, for Strongylocentrotus embryos from four clutches of eggs (each from a different species) differing in size. Development times did not vary consistently with egg diameter, and trends among eggs of different sizes varied with stage of development. In some cases, development times for eggs of intermediate diameter (S. franciscanus) were longer than those for larger or smaller eggs. Although mean egg diameters in clutches ranged from 84 μm (S. purpuratus) to 162 μm (S. pallidus), differences in development time to the last embryonic stage (prism) were very small. We conclude that the inverse relationship between parental investment in offspring and premetamorphic development time in echinoids depends only on the functional consequences of reduced size of feeding larval stages: effects of egg size on prefeeding development time are not evident.     

Temperature-mediated plasticity in egg and body size in egg size-selected lines of a butterfly

We examine genotype–environment interactions by using lines of the butterfly Bicyclus anynana artificially selected for differences in egg size in a full factorial design with two developmental and two oviposition temperatures. In accordance with the temperature–size rule, egg size and pupal mass increased by 4–5 and 8%, respectively, at lower temperatures. Genotype–environment interactions for both traits suggest that plasticity is largely independent of the trait value, and that there is potential for evolutionary change. These findings cast further doubt on the notion that temperature-mediated plasticity might be purely a physiological constraint.