Frequency of multiple brooding in Ring Ouzels,including first documented cases of triple brooding

Capsule The majority of female Ring Ouzels made two successful breeding attempts in a single season, but triple brooding was much less common.     

Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix

Self-compatible, hermaphroditic marine invertebrates have the potential to self-fertilize in the absence of mates or under sperm-limited conditions, and outcross when sperm is available from a variety of males. Hence, many hermaphroditic marine invertebrates may have evolved mixed-mating systems that involve facultative self-fertilization. Such mixed-mating strategies are well documented for plants but have rarely been investigated in animals. Here, I use allozyme markers to make estimates of selfing from population surveys of reef slope and reef flat sites, and contrast this with direct estimates of selfing from progeny-array analysis, for the brooding coral Seriatopora hystrix. Consistent heterozygote deficits previously reported for S. hystrix suggests that inbreeding (including the extreme of selfing) may be common in this species. I detected significant levels of inbreeding within populations (F(IS)=0.48) and small but significant differentiation among all sites (F(ST)=0.04). I detected no significant differentiation among habitats (F(HT)=0.009) though among site differentiation did occur within the reef slope habitat (F(SH)=0.06), but not within the reef flat habitat (F(SH)=0.015). My direct estimates of outcrossing for six colonies and their progeny from a single reef flat site revealed an intermediate value (t(m) (+/-s.d.)=0.53+/-0.20). Inbreeding coefficients calculated from progeny arrays (F(e)=0.31) were similar to indirect estimates based on adult genotype frequencies for that site (F(IS)=0.38). This study confirms that the mating system of this brooding coral is potentially variable, with both outcrossing and selfing.     

Renesting and brooding in the Caribbean flamingo

Caribbean flamingos were observed during the 1981 breeding season at the Audubon Zoological Garden in New Orleans, Louisiana. Two floods occurred during the breeding season, causing the flock to nest three times. At each new nesting there was a significant decline in the number of birds laying eggs. One pair brooded a chick during the final nesting. Immediately after hatching, the female usually brooded while the male defended the nest area; however, over the three-day period that the chick remained on the nest, the male began to spend more time brooding and less time defending the nest area. Thus there appeared to be some division of labor in this flamingo pair.     

The phylogenetic development of brooding behaviour in the hirudinea

Summary Within the Clitellata the habit of brooding the eggs and offspring is known only in the Glossiphoniidae, suggesting that the habit probably arose de novo in that family. Within extant glossiphoniids, the degree of protection given to the offspring can be arranged in a continuous series of increasing complexity, which may approximate the phylogenetic development of the behaviour culminating with a well developed brood pouch in Marsupiobdella. Further analysis of this brooding behaviour may shed light on the relationships of the higher categories of the Hirudinea. Brooding, which may have been derived from the habit of ventilating newly laid cocoons, known in some erpobdellids, probably evolved as a mechanism for increased survival of the offspring by protecting the offspring from heavy predation. Resume Chez la Clitellata l'habitude de couver les oeufs et les petits n'est connue que chez la Glossiphoniidae, ce qui suggère que l'habitude s'est probablement produite de novo dans cette famille. Chez les glossiphoniids la mesure de protection accordée aux petits peut s'arranger dans une série continue de complexité croissante, qui peut se rapprocher de la développement phylogénétique de l'habitude, se culminent en une poche ventrale chez le Marsupiobdella. Une analyse de cette habitude de couver les oeufs et les petits pourrait peut-être éclairer les parentés des genres des hirudinées. Cette habitude, qui peut avoir développé de l'habitude de ventiler les cocons récemment pondus, connue chez quelques erpobdellids, a probablement évolvé comme un méchanisme qui produirait une plus grande survie chez les petits en les protégant de la prédation sévère.     

Unusual chromosome complement in the brooding bivalve Lasaea consanguinea

Chromosomes of the brooding species Lasaea consanguinea were studied as part of a general invertigation of evolutionary genetics of antarctic bivalve species. Laseid species are of particular interest because they are widely distributed geographically, they inhabit the high intertidal zone, and they may reproduce apomictically.The diploid number of chromosomes for Lasaea consanguinea ranges from 100 to 120, 110 to 112 being most frequent. Karyological data (2n=108) show 6 groups of chromosomes. Group I includes 8 metacentric (m), 3 submetacentric (sm), 2 subtelocentric (st) and 4 telocentric (t) pairs. Group II has 11 t to st pairs; group III, 9 sm to m pairs; group IV, 8 m to sm pairs; group V, 6 st and group VI, 3 m pairs. Within each of the Groups II to VI chromosome pairs are of about the same size and morphology.The chromosomes of Lasaea consanguinea are unusual because of their abundance, their large size and their numerical variability. We suggest that Lasaea consanguinea has had a hermaphroditic ancestor where abnormal reproduction such as inbreeding, lack of males, and apomixy gave rise to genetic instability, the high number of chromosomes being related to the genetic instability with evolutionary polyploidy or/and supernumerary chromosomes.     

Bi-parental mouth brooding in Tilapia galilaea (Pisces, Cichlidae)

New evidence shows that Tilapia galilaea (Artédi) is almost certainly a bi-parental mouth brooder throughout its range, and that this habit is not confined only to races found in Israel. Previous classification of this species as a maternal brooder in Africa appears to be based on lack of observations; it is the only member of the genus definitely known to be a bi-parental brooder. The size of the eggs and the development of their adhesive stalk system is intermediate between those of substrate spawners and mouth brooders. Among the latter the adhesive stalk system of the only paternal brooding species is rudimentary but it is entirely absent in the maternal brooding species. The conclusion is drawn that maternal and paternal mouth brooders did not evolve directly from substrate spawners but independently from bi-parental brooders.     

Endocrine changes in the incubating and brooding turkey hen

Turkey hens were allowed to incubate eggs and to hatch and rear young. Plasma prolactin (Prl) levels increased prior to the start of continuous incubation and rose sharply as incubation progressed to reach a peak of 1178.2 +/- 221.8 ng/ml (mean +/- SEM) just before hatching. Prl levels then fell precipitously before the hens left the nest, and returned to preincubation levels (36.8 +/- 3.4 ng/ml) by the time the poults were 2 weeks old. These results show that the high plasma concentrations of Prl found during incubation are not initiated or maintained only by the stimulus of nesting. We suggest that the decline in Prl levels at the end of incubation could be related to the pipping and hatching of eggs, and the consequent shift to maternal behavior. Plasma growth hormone (GH) levels were significantly increased in hens which were brooding poults, but not in hens incubating eggs. An elevenfold, 1-day increase in plasma GH was observed immediately after the hens left the nests. Mean plasma GH levels rose from 12.0 +/- 4.7 ng/ml on the day that the hens left the nests to 133.0 +/- 32.0 ng/ml on the following day, and then declined to 23.1 +/- 9.6 ng/ml after an additional day. There were no significant changes in plasma thyroxine levels during laying, incubation and brooding. Plasma glucose concentration was significantly depressed during incubation.     

Evidence of brooding in Permian non-marine Ostracoda

The discovery of some exceptional non-marine fossil Ostracoda, showing larval stages within the carapaces of females, demonstrates that incubation was an ontogenetical adaptation which appeared at least as early as the Permian. Thus, it seems, the superfamilies Danvinulacea and Cytheracea diversified in Permian lakes where the Carbonitacea had flourished in the Carboniferous. The Cypridacea accomplished an evolutionary radiation in continental environments after a permanent invasion from the sea in the Middle Jurassic, thanks to the resistance of their eggs to dessication and heezing and the evolution of parthenogenetic reproduction.     

Mixed-mode bacterial transmission in the common brooding coral Pocillopora acuta

Reef-building corals form associations with a huge diversity of microorganisms, which are essential for the survival and well-being of their host. While the acquisition patterns of Symbiodiniaceae microalgal endosymbionts are strongly linked to the coral's reproductive strategy, few studies have investigated the transmission mode of bacteria, especially in brooding species. Here, we relied on 16S rRNA gene and Internal Transcribed Spacer 2 marker metabarcoding in conjunction with fluorescence in situ hybridisation microscopy to describe the onset of microbial associations in the common brooding coral Pocillopora acuta. We analysed the bacterial and Symbiodiniaceae community composition in five adult colonies, their larvae, and 4-day old recruits. Larvae and recruits inherited Symbiodiniaceae, as well as a small number of bacterial strains, from their parents. Rhodobacteraceae and Endozoicomonas were among the most abundant taxa that were likely maternally transmitted to the offspring. The presence of bacterial aggregates in newly released larvae was observed with confocal microscopy, confirming the occurrence of vertical transmission of bacteria in P. acuta. We concluded that host factors, as well as the environmental bacterial pool influenced the microbiome of P. acuta.     

Reproductive biology of the Caribbean brooding octocoral Antillogorgia hystrix

The reproductive biology of the Caribbean gorgonian Antillogorgia hystrix was studied in the shallow‐water reefs of Cross Harbour, Great Abaco (The Bahamas) from 2009 to 2010. Antillogorgia hystrix is an internal brooder that reproduces annually. The population at Cross Harbour was gonochoric and the sex ratio was skewed toward females (~3:1). Oogenesis precedes spermatogenesis by several months, and lasts at least 9 months, with oocytes >100 μm in diameter first becoming visible in dissections of samples from February; mature oocytes are present in late October–November. The size of mature oocytes (400–900 μm in diameter) was greater than that of the spermaries, which were rarely larger than 400 μm. Brooded planulae were observed in polyps from early November to mid‐December, and planula release was observed in aquaria in December 2009, which suggests that planulation occurs continuously over this period. Planulae of A. hystrix contained dinoflagellate symbionts, presumably acquired during embryogenesis and/or by mature planulae while they were in the gastrovascular cavity of the polyp. Brooding is an uncommon reproductive strategy among Caribbean gorgonians and this is the first report of internal brooding in the genus Antillogorgia. The genus contains a number of sympatric species with different modes of reproduction, and knowledge of their reproductive biology is critical to understand their ecology and evolution.     

Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina

Celleporella hyalina (L.) is unusual among cheilostomes in producing sexually dimorphic gonozooids which are frontally budded from a layer of sterile autozooids, and also in the possession of a placental system for extracoelomic nutrition of the developing embryo. This paper investigates these two aspects of the reproductive strategy, combining observations of living colonies with ultrastructural study of preserved material. The formation of the male and female gonozooids is described. Female zooids underwent a maximum of four successive reproductive cycles before senescence. About 29% of embryos failed to develop to completion and were prematurely expelled from the ovicell. Spermatogenesis follows the typical cheilostome pattern. Fertilization is internal, and probably occurs during vitellogenesis of the oocyte. Oogenesis involves the activity of a nurse cell. The telolecithal egg increases in volume approximately 15–fold after transfer to the ovicell, and is nourished by a relatively simple placental system formed by the distal epithelium of the maternal zooid.     

Maternal-larval population genetic traits in Stylophora pistillata, a hermaphroditic brooding coral species

Aspects of maternal-planula larval genetics in the monoecious scleractinian coral Stylophora pistillata (Red Sea, Eilat) were studied by amplified fragment length polymorphism (AFLP) methodology in two successive reproductive seasons. In total, 293 planulae and 10 adult colonies were analyzed. In June 2006, 147 planulae were collected from 10 shallow water colonies. In March, April and June 2007, 146 additional planulae were sampled from five of the ten 2006 sampled colonies. All AFLP products showed unalike band profiles indicating a fully sexual production pattern. We used 181 and 210 putative AFLP loci, of which the overall level of polymorphism in 2006 was 92 and 99 % in 2007 (respectively). Differences were also observed between 2006 and 2007 reproductive seasons in terms of total average gene diversity (0.191 vs. 0.247, respectively), suggesting fast turnover of sperm donor genotypes. In addition, increased numbers of potential sperm donor colonies in the vicinity of gravid females showed no impact on genetic differentiation levels in released larvae. UPGMA tree revealed clustering of maternal genotypes and their offspring, suggesting, as expected, high relatedness between planulae and their mothers. In addition, the average heterozygosity of each group of siblings was persistently lower than heterozygosity calculated for the respective maternal colony, suggesting the possibility of partial inbreeding. This trend of reduced genetic heterogeneity in Stylophora pistillata is an alarming sign for populations residing in the northern Red Sea coral reefs.     

Internal brooding favours pre-metamorphic chimerism in a non-colonial cnidarian, the sea anemone Urticina felina

The concept of intraorganismal genetic heterogeneity resulting from allogeneic fusion (i.e. chimerism) has almost exclusively been explored in modular organisms that have the capacity to reproduce asexually, such as colonial ascidians and corals. Apart from medical conditions in mammals, the natural development of chimeras across ontogenetic stages has not been investigated in any unitary organism incapable of asexual propagation. Furthermore, chimerism was mainly studied among gregarious settlers to show that clustering of genetically similar individuals upon settlement promotes the occurrence of multi-chimeras exhibiting greater fitness. The possible occurrence of chimeric embryos and larvae prior to settlement has not received any attention. Here we document for the first time the presence of natural chimeras in brooded embryos and larvae of a unitary cnidarian, the sea anemone Urticina felina. Rates of visible bi- and multi-chimerism of up to 3.13 per cent were measured in the broods of 16 females. Apart from these sectorial chimeras, monitored fusion events also yielded homogeneous chimeric entities (mega-larvae) suggesting that the actual rates of natural chimerism in U. felina are greater than predicted by visual assessment. In support of this assumption, the broods of certain individuals comprised a dominant proportion (to 90%) of inexplicably large embryos and larvae (relative to oocyte size). Findings of fusion and chimerism in a unitary organism add a novel dimension to the framework within which the mechanisms and evolutionary significance of genetic heterogeneity in animal taxa can be explored.     

Egg brooding by deep-sea octopuses in the North Pacific Ocean

Videotapes made from the submersible Alvin on Baby Bare, a 2600-m-deep North Pacific basalt outcrop, and at two other deep-sea localities document that octopuses of the genera Graneledone and Benthoctopus attach their eggs to hard substrate and apparently brood them through development. The behavior of brooding females was generally similar to that of shallow-water octopuses, but the genera showed apparent differences. In addition to the high density of brooding females observed at Baby Bare, which may relate to the increased availability of exposed hard substrates for egg attachment and of prey, females are suggested to increasingly associate with hard substrates as they mature. The biology of Baby Bare may seem unduly unique because the outcrop is isolated on a sedimented plain and is among the few exposures of hard substrate other than hydrothermal vents that have been explored by submersible. On the sediment-covered ocean floor, the availability of hard substrate may strongly affect the distribution of brooding octopuses. The size and shape of boreholes in 19 of over 400 thyasirid clam shells collected from Baby Bare support the hypothesis that octopuses had preyed upon the clams.     

Mass brooding of the blue octocoral,Heliopora coerulea on a sedimented equatorial reef

The octocoral Heliopora coerulea is a gonochoric surface brooder. Although the species is common on shallow Indo-Pacific coral reefs, information on its reproductive biology is limited and spawning timings have only been reported from four locations. We report the first observations of surface brooding in H. coerulea on a sedimented equatorial reef. In April 2014, 46 and 26 brooding colonies were recorded, respectively, from reefs fringing the islands of Kusu and Lazarus in Singapore. The brooded coral larvae were tightly bound to inflated coral polyps, forming a dense white mat which blanketed the brown coral tissue. The inflated polyps also protruded from layers of sediment, which accumulated in colony crevices, such that the brooded larvae were elevated above the settled sediment. Our observations supplement existing knowledge on the reproductive timing of H. coerulea and highlight the adaptations that improve survival of this species on sediment-impacted reefs.     

Ontogeny and origin of the brooding system in Antarctic urechinid sea urchins (Echinodermata,Holasteroida)

Summary Echinoids usually broadcast gametes, and do not generally engage in a high degree of parental care. However, when they do, juveniles are typically maintained among the spines, or in shallow, external depressions in the test itself. The brooding Antarctic holasteroids Urechinus mortenseni and Plexechinus nordenskjoldi are bizarre exceptions: females develop an elaborate brooding system in which a small number of direct developing young are protected. Ontogeny of post-natal brooding urechinids is marked by profound divergence in the growth trajectories of male and female apical systems. In females, this leads to dramatic departures from the patterns found in all other echinoids. Otherwise, coronal skeleton allometry of males and females is almost identical. Juveniles in brood pouches grow larger than the diameter of the apical aperture through which they must pass to reach the external environment. The apical plates, from which the brooding system is suspended, hinge downward to enlarge the aperture, allowing the young to emerge from the female. A possible origin for the brooding system suggests derivation by centripetal plate addition from the ocular plates in the coronal skeleton. We develop a contrasting model for the origin of the brooding system that relies on a proposed homology between genital and periproctal elements of the apical system of echinoids and the more highly developed dorsal skeleton of other echinoderm classes.     

Evidence of fostering in an internally brooding sea anemone

Evidence of alloparental care during the incubation stage has largely been demonstrated for species that incubate their offspring externally in a nest. Alloparental care in these species generally consists of the rearing of mixed broods which contain a low proportion of “foreign” young alongside the host's own offspring. However, many animals, including sea anemones, incubate offspring either on or within their bodies. The beadlet anemone Actinia equina incubate their young internally, and as many sea anemones are capable of reproducing both sexually and asexually, the origin of these internally brooded young has been the subject of much debate. While genetically identical young are brooded internally under the juvenile stage, it is thought that those produced sexually are released as larvae into the water and must return to the gastric cavity of an adult in order for metamorphosis to occur. As the likelihood of a planula larva finding its way back to its parent is slim, this suggests that alloparental care may play a role in the survival of juveniles in this species, a hypothesis first suggested a century ago but rarely tested. Here, using highly polymorphic microsatellite markers, we find evidence of alloparental care in A. equina. Our results indicate that while a high proportion of juveniles were genetically identical to their brooding adult, the remaining juveniles showed stark genetic differences to their brooding adult. These juveniles shared far fewer alleles with their “parent” than expected under sexual reproduction, indicating that they were not the adult's offspring. Furthermore, we found variation in the genetic composition of broods, which consisted either of (a) entirely genetically identical individuals, (b) a mix of unique individuals and clonemates or (c) entirely unique individuals, that is no shared genotype. Our results thus indicate that adult A. equina tolerate the presence of non-offspring within their gastric cavity and furthermore that they may incubate entirely “foreign” broods.