Gametic, morphometric, and physiological variables influencing clutch size in the Chilean oyster, Ostrea chilensis (Philippi, 1845)

A number of marine bivalve taxa, including species of the genus Ostrea, have adopted brooding of the young in the mantle cavity as a reproductive mechanism. In spite of the importance of brooding in the reproductive success of such species, little is known about the most important variables influencing the process, including those limiting clutch size. This study addresses the regulation of brood size in the hermaphroditic oyster Ostrea chilensis. During spawning, oysters released all their oocytes into the mantle cavity. No residual oocytes remained in the gonad, so a second spawning during the same brooding season was not possible. There was a weak correlation between the number of embryos incubated during the early phase of brooding and the dry tissue weight of the brooding oyster, and between the number incubated and the shell length of the brooding adult during the later phases of brooding. The number of embryos was also correlated with the area of the labial palps of the brooder during the later stages, suggesting that the loss of veligers observed at this time may be at least partially attributable to a limitation of space around the palps, which manipulate the larvae and with which the larvae are closely associated. The oxygen consumption rate of brooders incubating a normal clutch of embryos was not significantly different from that of oysters in which clutch size had been experimentally reduced by 50%. Experimental increase of the normal clutch size by 100% significantly increased the oxygen consumption of the brooder, suggesting that there is a physiological as well as a spatial limit to brood size. Thus the number of embryos brooded by an oyster is initially dependent on its production of oocytes and secondarily by the high metabolic costs of incubating large numbers of embryos. As development proceeds, space available for brooding apparently becomes a limiting factor as the larvae grow. The fate of the excess larvae is not known at present, but any larvae released prematurely cannot be competent to settle, since development is synchronous and there is a complete release of all pediveligers at the end of the brooding period.     

Brooding in echinoderms: How can modern experimental techniques add to our historical perspective?

Echinoderms are among the most abundant and ecologically successful groups of marine animals on earth. Their unique adaptations have enabled them to inhabit diverse environments ranging from various substrates in shallow water habitats to the benthos of the deepest seas. Although members of the Echinodermata generally share common characteristics including radial symmetry, a unique water vascular system, and decentralized cephalization, they have evolved a variety of life history strategies that enable them to reproduce successfully across a wide range of habitats. These reproductive strategies range from a complete lack of parental care (broadcasting) to internal and external brooding of the eggs, embryos, and juvenile phases. Although brooding is relatively rare in echinoderms, it is of interest as a “deviant” or “derived” form of reproduction that has been the subject of much study and debate. The aim of the present review is to examine how and why brooding occurs from a historical perspective, and then explore how modern experimental techniques are providing novel approaches to answering fundamental questions related to brooding in this very successful group of benthic marine invertebrates.     

Exclusive Male Egg Care and Determinants of Brooding Success in a Millipede

The evolution of exclusive male parental care is a major and controversial issue in behavioural ecology. Although arthropods practicing paternal care are thought to be key taxa for investigating this issue, few studies have attempted to clarify the selection factors associated with male behaviour and fitness consequences in arthropods. In the millipede Brachycybe nodulosa, males curl their bodies around egg masses on the undersides of decaying logs. Male‐removal experiments in the laboratory strongly suggest that males defend the eggs against fungal infection. Orphaned eggs were soon covered by hyphae and no eggs hatched, whereas almost all eggs brooded by males successfully hatched. The egg‐brooding males showed no aggressive responses when disturbed. Only some mature males bred in the field. Furthermore, the number of eggs brooded varied greatly among the males. Selected generalized linear models revealed that males with a wide seventh body segment, which possesses gonopods (genital legs), tended to succeed in brooding; and males with a wider body also obtained more eggs. Colony attributes had no significant effects on male brooding. We discuss the possible sexual selection mechanisms that could accomplish this pattern of brooding success among male B. nodulosa.     

Postural Shifts During Egg‐Brooding and Their Impact on Egg Water Balance in Children’s Pythons (Antaresia childreni)

Parental care typically consists of distinct behavioral components that are balanced to address the multiple needs of offspring. Female pythons exhibit post‐oviposition parental care in which they coil around their parchment‐shelled eggs throughout incubation (40–80 d). Subtle postural shifts during egg‐brooding facilitate embryonic gas exchange but may entail hydric costs to the clutch. This study used a simple behavioral model to (1) further quantify the costs and benefits of specific parental behaviors to developing offspring and (2) determine the influence that developmental stage and relative clutch mass have on parental behavior. Although previous research has demonstrated that egg‐brooding as a whole reduces clutch water loss, we hypothesized that egg‐brooding female pythons specifically adopt a tightly coiled posture to conserve embryonic water, but must make postural adjustments to enhance gas exchange between the clutch and nest environments at the cost of increased clutch water loss. We measured rates of water loss in brooding Children’s pythons (Antaresia childreni) and their respective clutches (i.e., brooding units) and monitored changes in brooding posture. We conducted serial trials to elucidate the effect of developmental stage on postural adjustments and water loss. Results demonstrated that the proportion of time females spent in a tightly coiled posture was inversely related to mean water loss from the brooding unit. Analyses indicated that slight adjustments in posture led to bursts in brooding unit water loss. Indeed, brooding unit water loss during postural adjustments was significantly higher than during tight coiling. These findings imply that python egg‐brooding provides an adjustable diffusive barrier that leads to discontinuous gas exchange, which minimizes clutch water loss. Because females with larger relative clutch masses spent more time tightly coiled, egg‐brooding female pythons may use a ‘water first’ strategy in which they intentionally conserve clutch water at the cost of reduced embryonic respiratory gas exchange.     

Reproductive strategy of the semelparous clam Gaimardia bahamondei (Bivalvia,Gaimardiidae)

Abstract. Semelparity is one of the most drastic reproductive strategies found among marine invertebrates. It is frequently found in species whose members have small adult sizes and brood embryos internally. In this study, we describe the reproductive strategy of the bivalve Gaimardia bahamondei to explore the possible causes of the association between semelparity and internal brooding. Males of this species exhibit continuous gonadal activity throughout the breeding season. Apparently continuous spawning of sperm is associated with an abundance of captured sperm in the adfrontal region of the gill filaments of both males and females. Females are capable of brooding three cohorts of embryos simultaneously while also producing three new cohorts of oocytes. This suggests that females are able to generate at least six cohorts of embryos during the breeding season. Embryos are brooded in the suprabranchial chamber and are individually surrounded by a membrane with a projecting peduncle; embryos are anchored by this peduncle to the adfrontal region of the gill filaments. Members of the youngest cohort differ in size, color, and shell ornamentation from members of the two older cohorts. There is no difference between members of the two older cohorts in size, but there is with respect to coloring and shell ornamentation. The importance of the embryonic cohorts in terms of their percentage of the total number of embryos varied among brooding females, suggesting among‐female variation in the timing of release of the oldest cohort of embryos. Members of this cohort break loose from the gills, lose their surrounding membrane, and fall into the ventral region of the suprabranchial chamber, from which they are evacuated to the exterior. Continuous sperm production in males and the production of at least six cohorts of embryos in females suggest that the costs of reproduction are high, which may partly explain the semelparity identified in this species.     

Phylogeographic analysis of the brooding brittle star Amphipholis squamata (Echinodermata) along the coast of New Zealand reveals high cryptic genetic variation and cryptic dispersal potential

Abstract.— Direct development in benthic marine invertebrates is usually associated with narrow geographical range, low rates of colonization, and low levels of gene flow. Paradoxically, the small brittle star Amphipholis squamata broods its larvae to a crawl-away juvenile stage, yet has a cosmopolitan distribution. Using sequence and restriction-fragment-length-polymorphisms (RFLP) analyses of nuclear and mitochondrial DNA from 16 coastal populations throughout New Zealand, we tested whether the species is indeed a poor disperser, as may be expected from its brooding habit. We predicted that local and regional populations would be genetically structured according to isolation by distance. We also suspected that this ubiquitous "species" is composed of a variety of cryptic taxa in different geographic areas, as has been discovered in an increasing number of marine invertebrates. We found evidence of four genetically divergent and reproductively isolated lineages that can exist in syntopy. Lineages vary in abundance, haplotype diversity, and geographic distribution. The partitioning of genetic variation within the most common lineage, as well as the geographic distribution of the four lineages, suggest a north/south split. This pattern is consistent with known New Zealand marine biogeographic zones and appears to be linked to the regime of oceanic circulation, which is characterized by subtropical, southward-moving water masses in the north, and sub-Antarctic, northward-moving water in the south. We conclude that the dispersal ability of A. squamata is regionally restricted but with sporadic long-distance dispersal, which serves to increase local genetic variation. Our results support the idea that dispersal occurs through passive transport by drifting or rafting on macroalgae, which A. squamata commonly inhabits, and emphasize that poor dispersal ability is not necessarily a corollary of direct development.     

Patterns of Parental Investment and Sexual Selection in Teleost Fishes: Do They Support Bateman's Principles?

Bateman demonstrated differences in variance for fertility andmating success between the sexes, with males usually havinga greater variance than females. Thus in general, male reproductivesuccess increases with number of mates acquired. These resultshave been referred to as "Bateman's principles" and taken togetherwith other parameters (e.g., relative parental investment) havebeen proposed to estimate a component of sexual selection. Forthis review I examine patterns of parental care and sexual selectionin teleost fishes (substrate brooding and with internal fertilization).I present data for the pumpkinseed sunfish Lepomis gibbosus,in which I estimated cost of paternal care and compared directmeasures of the intensity of selection on possible sexuallyselected traits to measures of sexual selection based on Bateman'sprinciples. Despite high levels of paternal care in substrate brooding fishes,sexual selection tends to act more strongly on males than onfemales, which suggests that maternal investment is higher thanpaternal investment and that parental care does not limit thereproductive rate for males. In pumpkinseed sunfish, selectionfavors parents with high levels of defense that may excludepredators more effectively and, as suggested by Bateman's measures,alternative reproductive strategies may decrease the opportunityfor sexual selection within the parental strategy. In teleostfishes with internal fertilization, patterns of parental investmentand intensity of sexual selection seem to support Bateman'sprinciples, but further studies using these systems and thesemeasures of selection will improve the understanding of factorsaffecting the intensity of sexual selection and its relationto mating systems.     

Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes.

Many marine invertebrates deposit benthic egg masses that are potentially vulnerable to microbial infection. To help counter this threat these species may have evolved some form of chemical protection for their encapsulated embryos. In this study the egg masses from 7 marine mollusks were tested for antibacterial activity against 4 marine pathogens: Enterococcus sericolicida, Vibrio anguillarum, Vibrio alginolyticus, and Vibrio harveyi. Extracts from all of these egg masses were found to inhibit the growth of at least 1 marine bacterium at concentrations that approximate the natural concentration of extract in the egg masses. The egg masses of 39 mollusks and 4 polychaetes were then tested for antibacterial activity against 3 human pathogenic bacteria; Escherichia coli, Staphylococcus aureus, and Pseudomonas aeruginosa. Activity was detected in the egg masses from 34 species, including 2 polychaetes and mollusks from two classes and 18 families. Antibacterial activity in molluskan egg masses was found to extend across the marine, estuarine, freshwater, and terrestrial environments. Both gelatinous egg masses and tough egg capsules were found to inhibit microbial growth, suggesting that physical protection alone may not be sufficient to protect the eggs. Antimicrobial activity was observed in the fresh egg masses but not in the well-developed egg masses of a subset of species. The results of this study indicate that a wide range of invertebrates use chemical defense to protect their early stage embryos against bacterial infection.     

The dynamics of male brooding,mating patterns,and sex roles in pipefishes and seahorses (family Syngnathidae)

Modern theory predicts that relative parental investment of the sexes in their young is a key factor responsible for sexual selection. Seahorses and pipefishes (family Syngnathidae) are extraordinary among fishes in their remarkable adaptations for paternal care and frequent occurrences of sex-role reversals (i.e., female-female competition for mates), offering exceptional opportunities to test predictions of sexual selection theory. During mating, the female transfers eggs into or onto specialized egg-brooding structures that are located on either the male's abdomen or its tail, where they are osmoregulated, aerated, and nourished by specially adapted structures. All syngnathid males exhibit this form of parental care but the brooding structures vary, ranging from the simple ventral gluing areas of some pipefishes to the completely enclosed pouches found in seahorses. We present a molecular phylogeny that indicates that the diversification of pouch types is positively correlated with the major evolutionary radiation of the group, suggesting that this extreme development and diversification of paternal care may have been an important evolutionary innovation of the Syngnathidae. Based on recent studies that show that the complexity of brooding structures reflects the degree of paternal investment in several syngnathid species, we predicted sex-role reversals to be more common among species with more complex brooding structures. In contrast to this prediction, however, both parsimony- and likelihood-based reconstructions of the evolution of sex-role reversal in pipefishes and seahorses suggest multiple shifts in sex roles in the group, independent from the degree of brood pouch development. At the same time, our data demonstrate that sex-role reversal is positively associated with polygamous mating patterns, whereas most nonreversed species mate monogamously, suggesting that selection for polygamy or monogamy in pipefishes and seahorses may strongly influence sex roles in the wild.     

Evidence for matrotrophy in the viviparous sea cucumber Leptosynapta clarki: A role for the genital haemal sinus?

Summary

Viviparity, where the embryos develop in the female reproductive system, is a rare form of reproduction in marine invertebrates, being described in only 14 species of echinoderm. In the intraovarian brooding sea cucumber, Leptosynapta clarki Heding 1928 (cf., Sewell et al. 1995), we used direct evidence (changes in energetic content) to show that significant additional nutrients are provided to the embryos during viviparous development (matrotrophy). In the transition from a structure used to produce gametes to a long-term brooding structure there are visual, histological and transmission electron microscopy (TEM) changes in the structure of the ovarian wall. Changes occur primarily in the cells of the visceral peritoneum and involve an increase in size of the connective tissue/genital haemal sinus (CT/GHS). In the latter part of the brooding period the visceral peritoneum returns to a flattened form, and new oocytes develop along the tubule wall. Similar changes in the intraovarian brooding sea cucumber Oneirophanta mutabilis affinis lead us to suggest that there is a role for the genital haemal sinus in providing nutrition during the brooding period in viviparous echinoderms. Future research is suggested to focus on changes in the ovarian wall structure during the different phases of reproduction (gamete production/brooding) in these species.     

Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the Tertiary of southern Australia

Abstract Taxonomic revision and cladistic analysis of a morphological dataset for Australian Tertiary temnopleurids resolve the phylogeny of the group and allow the testing of a series of hypotheses about the evolution of larval development and consequences of changes in development. Australian Tertiary temnopleurids encompass all three major developmental types found in marine invertebrates (planktotrophy, lecithotrophy, and brooding). Planktotrophy is plesiomorphic for this clade, and nonplanktotrophic larval development evolved independently at least three times during the Tertiary. The change to a nonplanktotrophic mode of larval development is unidirectional with no evidence of reversal. In addition, there is no evidence of an ordered transformation series from planktotrophy through planktonic lecithotrophy to brooding. In common with previous studies of other invertebrate groups, analysis of the raw data suggests that nonplanktotrophic taxa within this clade have significantly shorter species longevities, more restricted geographic ranges and higher speciation rates than taxa with planktotrophic development. However, analysis using phylogenetically independent contrasts is unable to confirm that the stratigraphic and geographic patterns are unbiased by the phylogenetic relationships of the included taxa.     

δ18O‐derived incubation temperatures of oviraptorosaur eggs

In order to determine the incubation temperature of eggs laid by non‐avian dinosaurs, we analysed the oxygen isotope compositions of both eggshell carbonate (δ¹⁸O_c) and embryo bone phosphate (δ¹⁸O_p) from seven oviraptorosaur eggs with preserved in ovo embryo bones. These eggs come from the Upper Cretaceous Nanxiong Formation of Jiangxi Province, China. Oviraptorosaur theropods were selected because of their known brooding behaviour as evidenced by preserved adult specimens fossilized in brooding posture on their clutch. Incubation temperature of these embryos was estimated based on the following considerations: eggshell δ¹⁸O_c value reflects the oxygen isotope composition of egg water fluid; embryo bones precipitate from the same egg fluid; and oxygen isotope fractionation between phosphate and water is controlled by the egg temperature. A time‐dependent model predicting the δ¹⁸O_p evolution of the embryo skeleton during incubation as a function of egg temperature was built, and measured δ¹⁸O_c and δ¹⁸O_p values used as boundary conditions. According to the model outputs, oviraptorosaurs incubated their eggs within a 35–40°C range, similar to extant birds and compatible with the known active brooding behaviour of these theropod dinosaurs. Provided that both eggshell and embryo bones preserved their original oxygen isotope compositions, this method could be extended to investigate some reproductive traits of other extinct groups of oviparous amniotes.     

Phylogenetic analysis of the Sphaeriidae (Mollusca: Bivalvia) based on partial mitochondrial 16s rDNA gene sequences

Abstract. We have constructed molecular phylogenetic trees for members of the Sphaeriidae in order to test proposed generic level relationships, and to reconstruct the evolutionary pattern of parental care, in this exclusively freshwater family of heterodont bivalves. An ∼480 nucleotide fragment of the mitochondrial large ribosomal subunit (16s rDNA) was sequenced for 4 corbiculid outgroups in addition to 19 sphaeriid ingroup taxa. Ingroup species were obtained from North and South America, Europe, and Australasia and included representatives of the main sphaeriid genera. Our analyses support four primary conclusions: 1) the Sphaeriinae are robustly monophyletic with respect to Eupera platensis ; 2) the genus Pisidium is paraphyletic and P. sterkianum is sister to the 17 other sphaeriine taxa in our dataset; 3) synchronous brooding is the ancestral reproductive pattern in the Sphaeriinae; 4) the sequential brooders form a clade in which Musculium taxa are monophyletic and nested among lineages of Sphueriunz. Our gene trees reveal an evolutionary progression in parental care complexity from the relatively simple pattern in the Euperinae, to the origin of brood sacs and of extraoogonial embryonic nutrition in the common ancestor of the Sphaeriinae, and ultimately to the development of sequential brooding in Sphaerium/Musculium taxa.     

Filial cannibalism improves survival and development of beaugregory damselfish embryos

Cannibalism of small numbers of offspring by a parent has been proposed as an adaptive parental strategy, by providing energy to support parental care. However, there are few empirical studies to support this hypothesis. We conducted field and laboratory experiments to investigate partial filial cannibalism in Stegastes leucostictus, a coral reef fish with paternal care. Partial cannibalism was shown to be common, and males were found to remove developing embryos from throughout a clutch in a random pattern, rather than in the more aggregated pattern seen during embryo predation. Males that received a diet supplement grew faster than control males, but did not engage in less cannibalism. Also, males did not concentrate cannibalism on early embryonic stages with the highest energetic value. Experimental reduction of embryo densities was found to significantly increase embryo development rate and survival from egg deposition to hatching, and experimental reduction of oxygen levels significantly increased rates of partial filial cannibalism by males. Artificial spawning sites with low oxygen levels were avoided by spawning females, and cannibalism rates by males were higher. We propose that partial filial cannibalism serves as an adaptive parental strategy to low oxygen levels in S. leucostictus by increasing the hatching success of embryos.     

The cost of incline locomotion in ghost crabs (<Emphasis Type="Italic">Ocypode quadrata</Emphasis>) of different sizes

It is well established that the metabolic cost of horizontal locomotion decreases as a regular function of animal body mass, regardless of body form and phylogeny. How body size affects the cost of incline exercise remains much less clear. Studies on vertebrates have led to the hypotheses that the cost of vertical work is independent of body mass and that the added cost of locomoting on inclines is lower for small animals. Studies on vertebrates and a few invertebrates provide evidence both for and against these hypotheses. To gain further insight into the cost of incline exercise, we measured oxygen consumption of small (2.33 ± 0.07 g) and large (46.66 ± 5.33 g) ghost crabs (Ocypode quadrata) locomoting horizontally and up a 20° incline. The slope of the oxygen consumption versus speed relationship (= minimum cost of transport) was not significantly different for small crabs exercising horizontally and on an incline. However, the intercept for incline exercise was significantly higher, indicating that small crabs used more energy during incline exercise than during horizontal exercise. Incline had no effect on the slope or intercept of the oxygen consumption versus speed relationship for large crabs. Our results suggest that the cost of incline locomotion may be large for small animals and that the cost is not independent of body size. Our results add to the growing body of research indicating that body mass is but one factor that determines the cost of incline locomotion and efficiency of vertical work.     

Temporal and spatial complexity of maternal thermoregulation in tropical pythons

Parental care is a widespread adaptation that evolved independently in a broad range of taxa. Although the dynamics by which two parents meet the developmental needs of offspring are well studied in birds, we lack understanding about the temporal and spatial complexity of parental care in taxa exhibiting female-only care, the predominant mode of parental care. Thus, we examined the behavioral and physiological mechanisms by which female water pythons Liasis fuscus meet a widespread developmental need (thermoregulation) in a natural setting. Although female L. fuscus were not facultatively thermogenic, they did use behaviors on multiple spatial scales (e.g., shifts in egg-brooding postures and surface activity patterns) to balance the thermal needs of their offspring throughout reproduction (gravidity and egg brooding). Maternal behaviors in L. fuscus varied by stage within reproduction and were mediated by interindividual variation in body size and fecundity. Female pythons with relatively larger clutch sizes were cooler during egg brooding, suggesting a trade-off between reproductive quantity (size of clutch) and quality (developmental temperature). In nature, caregiving parents of all taxa must navigate both extrinsic factors (temporal and spatial complexity) and intrinsic factors (body size and fecundity) to meet the needs of their offspring. Our study used a comprehensive approach that can be used as a general template for future research examining the dynamics by which parents meet other developmental needs (e.g., predation risk or energy balance).     

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail

Predator-induced hatching plasticity has been demonstrated in many species of amphibians. However, animals from other clades (e.g., marine species of molluscs and annelids) also place their embryos in capsules or gelatinous masses and might also exhibit hatching plasticity to predators. To date there is no evidence of predator-induced hatching plasticity from any marine species or a major clade of bilateria animals, the Lophotrochozoa. We studied predator-induced hatching plasticity of Nucella lamellosa, a carnivorous marine snail that deposits embryos in capsules. We used two experiments to investigate the effects of two types of predator, crabs and isopods, on developing embryos. In the first experiment, we quantified proportion of hatched embryos from capsules through time exposed to water-borne chemicals of crabs and isopods. Crabs delayed time-to-hatching, and the effects of predators were additive. In the second experiment, we quantified proportion of hatched embryos from capsules through time, developmental stage, and size of embryos in capsules exposed to water-borne chemicals of crabs and conspecifics. With this experiment, we wanted to answer: (1) whether a delay in hatching corresponded to embryos developing slower, and (2) whether the general products of metabolic waste from organisms can delay hatching. We unexpectedly observed that adult conspecific snails accelerated hatching but not developmental rate—the few past studies on the effects of conspecifics have all demonstrated that conspecifics delay time-to-hatching and rate of development. The results were also inconsistent with metabolic waste in general causing a delay in hatching, although the effect of conspecifics does weaken this inference. This study demonstrates that predators delay time-to-hatching in a marine mollusc, and suggests that predator-induced hatching plasticity is widespread among animals and likely evolved multiple times within the bilateria. In addition, conspecifics accelerated time-to-hatching in a marine mollusc, which suggests that conspecifics, like predators, might commonly influence when embryos hatch.     

Obligate costs of parental care to offspring: egg brooding-induced hypoxia creates smaller, slower and weaker python offspring

Python egg brooding typifies parental care because it consists of multiple behaviours that provide for multiple developmental needs. For example, tightly coiling around the eggs benefits embryonic water balance, but periodic female postural adjustments improve embryonic gas exchange. Regardless of these postural adjustments, egg brooding creates a hypoxic intra-clutch environment that constrains embryonic metabolism. We further examined this novel and useful parental care model to determine: (1) any fitness-related costs of egg brooding to offspring; (2) whether any long-term costs are alleviated by postural adjustments. We artificially incubated Children's python ( Antaresia childreni ) clutches and modulated oxygen partial pressure ( P O₂) to create three treatments: normoxic (NRM, 20.3 kPa O₂), brooding [BRD, P O₂ profile typical of clutch P O₂ ( P O_2clutch) in maternally brooded clutches, 15.8–19.3 kPa O₂] and low (LOW, predicted P O₂ profile of maternally brooded P O_2clutch if females did not make postural adjustments, 14.4–18.6 kPa O₂). Using various metrics from ∼12 days pre-hatching to 14 days post-hatching, we demonstrated that NRM offspring were larger, faster and stronger than BRD offspring. As only hatchling heart mass differed between BRD and LOW treatments (LOW > BRD), postural adjustments may not alleviate hypoxia-related costs to embryos. Our results demonstrate that parental care may represent a compromise between competing developmental needs and thus entails obligate costs to the offspring.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 414–421.