Factors determining the frequency and productivity of double brooding of Barn Owls Tyto alba

Capsule: Early nesting Barn Owls Tyto alba and those that switched nest sites fledged most chicks overall because they could fit two, more productive, nesting attempts into a breeding season.

Aims: To determine the frequency and productivity of double broods in Barn Owls, and for double brooders, to determine what affects the probability of nest switching and how that affects productivity.

Methods: We monitored the first egg date of each nesting attempt, whether it was in a ‘vole year’, whether a breeding attempt was first or a second annual attempt, the number of chicks fledged from each attempt, and whether a pair switched nest sites, if breeding twice, from 602 Barn Owl breeding attempts in an area of lowland England from 1996 to 2007. General linear models were used to determine predictors of the probability that a pair had a second brood and the number of chicks fledged in each nesting attempt, and then for those owls that double brooded, which variables best predicted the probability of switching, and the number of chicks fledged from the second nest. Finally, we tested whether switching resulted in a shorter laying interval and higher annual productivity.

Results: Early nesting birds were more likely to double brood, although this was relaxed in vole years when later nesting birds also double brooded. Productivity (through increased numbers of chicks fledged or reduced chick loss) was higher the earlier a nest occurred, and there were more chicks fledged in good vole years and in second nesting attempts. Productivity, brood depletion, first clutch date and vole years did not determine whether a double brooding pair switched nesting sites. Productivity in the second nest did not change with a switch but productivity increased for early first nests and second nests with a shorter interval between the first and second nest. Switching however decreased nesting interval and nesting interval was also shorter if there were fewer fledglings from the first nest. Overall productivity was higher for pairs that switched.

Conclusions: Double brooding in Barn Owls increased seasonal productivity substantially and its occurrence depended on vole abundance or early nesting. Nest switching between broods may be a strategy for earlier laying of the second brood. Provision of alternative nest sites, close together in a Barn Owl’s home range, may allow earlier re-nesting and so increase productivity.     

Photoperiodic regulation of feeding and reproduction in a brooding sea star from central California

Summary

Individuals of the sea star genus Leptasterias from the Monterey Peninsula, California, were maintained for 34 months under two contrasting regimes of seasonally changing photoperiod. In one regime the lights turned on and off in phase with local sunrise and sunset; in the other the daily photoperiod was kept 6 months out of phase with ambient photoperiods. Annual cycles of feeding, gametogenesis, and embryo brooding of the out-of-phase animals were all shifted out of phase with respect to those of the in-phase animals. These small, relatively hardy sea stars appear well suited for more detailed analyses of photoperiodism in asteroids.     

The evolution of mating systems in a group of brooding sea anemones (Epiactis)

Summary

The sea anemone genus Epiactis provides an unusually good opportunity to study the evolution of brooding and mating systems. The four Epiactis species on the Pacific coast of North America all brood their offspring up to the juvenile stage, but each has a different combination of internal vs. external brooding and gonochory vs. simultaneous or gynodioecious hermaphroditism. Two of the four species (E. prolifera and E. lisbethae) were indistinguishable with allozymes (20 loci), but could be differentiated using multilocus DNA fingerprinting. Phylogenetic analyses of the allozyme data by distance and parsimony methods using three outgroups suggest that the four nominal Epiactis species are polyphyletic, with the two internal brooders evolving independently of the two external brooders. This topology does not allow inferences about the evolutionary order of hermaphroditism, dioecy and gynodioecy. Separate sexes and obligate outcrossing are of ten believed to be ancestral, with hermaphroditism and the potential for self-fertilization being favored in taxa where restricted dispersal promotes inbreeding. Previous studies of population genetic structure in these Epiactis species is consistent with this hypothesis, as even the cross-fertile species were highly inbred.     

Gametogenesis,brooding and planulation in laboratory populations of a temperate scleractinian coral Balanophyllia elegans maintained under contrasting photoperiod regimes

Summary

Males of Balanophyllia elegans Verrill, 1864 in Monterey Bay, California, spawn in the fall. Fertilization occurs within the females and the internally brooded embryos develop into large benthic planulae that are released mainly in the late winter. Field-collected corals were held in the laboratory under contrasting photoperiod regimes (ambient or in-phase, and 6 months out-of-phase) for 6.5 years. After two years in the laboratory corals planulated at the same time, independent of photoperiod. Corals show a cyclic pattern of later winter and early spring planulation that coincides with declining sea temperatures in Monterey Bay. Gametes appeared in the first laboratory generation at IS months and brooded embryos were found in females at 31 months under both light regimes. Planulae production by laboratory-reared corals peaked at the same time as that of the parents. These findings suggest that the temporal pattern of planulation is regulated by both endogenous and exogenous components that can be modified in some way by disturbance caused to the corals when collected or by the time of collection.     

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.     

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.     

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.     

Highly stable symbioses among western Atlantic brooding corals

The reproductive mode of corals largely determines how zooxanthellae (Symbiodinium spp.) are acquired. Typically, broadcast spawning corals obtain symbionts from the surrounding environment, whereas most brooders transfer symbionts from maternal parent to offspring. Brooding corals are therefore predicted to harbor stable communities of Symbiodinium. This study documents the associations between Symbiodinium spp. and brooding corals in response to seasonal environmental fluctuations. Between March 2002 and December 2005, endosymbiont identity was determined seasonally from replicate colonies (n = 6) of three brooding species, Agaricia agaricites, Porites astreoides and Siderastrea radians, from shallow environments (1–4 m) of the Florida Keys and Bahamas. Symbionts were identified via denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region. No change was detected in the Symbiodinium communities harbored within these brooding colonies. Additionally, no change in symbiosis was observed through a moderate bleaching event, thereby demonstrating that some bleached corals recover without changing symbionts.     

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.     

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.     

Internal embryonic brooding and development in the southern Australian micro-snail Tricolia rosea (Angas, 1867) (Vetigastropoda: Phasianellidae: Tricoliinae)*

ABSTRACT

Internal embryonic brooding has been suggested as an adaptation to enhance reproductive success in minute gastropods. It is rare in vetigastropods, previously known in only two species of Spectamen Iredale, 1924 (Solariellidae) from South Africa. Herein it is confirmed in the temperate Australian micro-snail Tricolia rosea (Angas, 1867), with up to 46 embryos observed within a gravid female. Embryos are brooded to an advanced stage, possessing a translucent, calcified shell and a calcified operculum. The initial protoconch is colourless, spirally sculptured and delineated by a consistent axial demarcation at the 0.75 whorl mark, when it measures 320?µm across. Beyond this, the second part of the protoconch is tinted pink, the strong spiral sculpture continues but the ribs and interstices are broader, with smoother surface microsculpture. At the 1.1 to 1.125 whorl mark the protoconch measures 400?µm across when transition to smooth teleoconch sculpture occurs. No brooded embryos possessed teleoconch sculpture. The potential relationship of protoconch morphology to embryonic development, hatching, feeding and release are considered. The mechanism of fertilisation is unknown, but embryos in a brood are at the same developmental stage. Unanswered questions in embryonic development and problems with protoconch terminologies in vetigastropods are also discussed.     

Factors influencing double brooding in Eurasian Hoopoes Upupa epops

Double brooding may be a good strategy for short‐lived species to maximize annual and lifetime reproductive success (ARS and LRS, respectively). Nevertheless, there is typically individual variation in the probability of producing a second clutch. Here we evaluate factors that influence the decision to double brood in the Eurasian Hoopoe Upupa epops. Analyses of an 11‐year dataset showed that 36% of the females and 21% of the males produced a second clutch after successfully raising a first clutch. Double‐brooded females had higher ARS (9.1 ± 1.9 fledglings; mean ± se) and LRS (0.93 ± 0.08 recruits) than single‐brooded females (ARS: 4.5 ± 2.1 fledglings; LRS: 0.36 ± 0.03 recruits). This suggests that double brooding is adaptive in Hoopoes, and raises the question of why most individuals only produce one clutch per season. The probability of double brooding varied only slightly between years, suggesting that it is influenced by individual characteristics rather than by external, population‐level environmental factors. In both sexes, the probability of double brooding increased with earlier timing of the first clutch, and the timing of reproduction was the most important factor influencing reproductive success. The latter is likely to be mediated by changes in resources during the season. The probability of double brooding also increased slightly with female age, due to differences in intrinsic quality among females rather than to a gain in experience. In contrast to many other studies, the probability of double brooding increased with an increasing number of fledglings from the first clutch, suggesting that it is a strategy of individuals of high quality. Taken together, we show that the individual quality of the breeder and the timing of their first clutches are key factors influencing the decision to double brood, and thereby that they are important determinants of reproductive performance in Eurasian Hoopoes.     

King penguin brooding and defending a sub-Antarctic skua chick

Interspecific parental care is rare, conveys no ultimate evolutionary advantage, and is usually attributed to reproductive errors in species with analogous habitat, behaviour and diet. We report on interspecific parental care (brooding and “defence” of unrelated chick) provided by a king penguin to a sub-Antarctic skua chick on Marion Island, despite substantial risk of injury to the penguin due to the presence of the true parents.     

Larval behaviour and settlement cues of a brooding coral reef sponge

Patterns of larval release, dispersal and settlement in sponges are poorly understood despite their significance in explaining adult ecology. Time of release, swimming speeds, phototaxis and vertical migration were quantified for larvae of the dictyoceratid sponge Coscinoderma matthewsi. The influence of cues associated with biofilms and coral rubble on larval settlement and metamorphosis was also measured. C. matthewsi is a brooding sponge and releases tufted parenchymellae larvae during the day. Upon release, larvae (>90%) have no phototactic response, maintaining their position at the water surface for 80 min ± 0 (mean ± SE) regardless of a light cue (natural daylight) before exhibiting negative phototaxis. At 28 h post-release, the majority of larvae (94.7% ± 6.1) exposed to light from the surface migrated to the bottom and assumed a demersal phase. Without light, larvae occupied the surface for up to 28 h post-release (89.3% ± 1.8) before migrating to the bottom. Larvae did not settle gregariously and began to settle and metamorphose after 28 h post-release without a cue. Settlement and metamorphosis were faster in the presence of a biofilm (settlement = 15.0% ± 8.7 and metamorphosis = 12.5% ± 9.5 at 28 h post-release), while the addition of coral rubble accelerated metamorphosis further (settlement = 10.0% ± 4.1 and metamorphosis = 27.5% ± 10.3 at 28 h post-release) compared to controls (sterile surfaces) (settlement = 0% and metamorphosis = 0% at 28 h post-release). However, both biofilms and coral rubble decrease total metamorphosis (control = 92.5% ± 4.8, biofilms = 67.5% ± 7.5 and coral rubble = 55.0% ± 13.2) due to mortality after 76 h post-release.     

Experimental taphonomy of embryo preservation in a Cenozoic brooding bivalve

To distinguish between alternative explanations for the presence of synchronous broods in the Miocene-Pliocene bivalve, Transenriella species. we performed in situ burial experiments of the Recent species T. corfusa . All Recent Transennella species are asynchronous brooders; a single brood contains all or most developmental stages. Specimens from Miocene—Pliocene deposits of California suggest that some members of this taxon were synchronous brooders, i.e., all the embryos of a brood develop simultaneously with only one developmental stage represented at any time. The presence of synchronous Transennella broods in the Miocene—Pliocene could indicate that an evolutionary change in mode of reproduction has occurred in this genus. Alternatively, asynchronous brooding in this taxon may he conservative and preferential preservation of later stages of development, or seasonal variation in reproduction, could result in a taphonomic overprint. Our burial experiments indicate that the earliest stages of development are almost entirely lost; however. there is enough preservation of the later stages of development to distinguish the two modes of reproduction. Additionally. we discovered a single fossil specimen with an asynchronous brood. Based primarily on this specimen, and observations from the burial experiments, we conclude that the fossil synchronous broods are an artifact of preservation and asynchronous brooding in Transenella is conservative.     

Foraging strategies of incubating and brooding king penguins Aptenodytes patagonicus

For oceanic birds like king penguins, a major constraint is the separation of foraging areas from the breeding colony, largely because swimming increases foraging costs. However, the relationship between foraging strategy and breeding stage has been poorly investigated. Using time-depth recorders, we studied the diving behaviour of two groups of king penguins that were either incubating or brooding chicks at Crozet Islands (Southern Indian Ocean) at the same period of the year. Although birds with chicks had the highest predicted energy demand, they made foraging trips half as long as incubating birds (6 vs. 14 days) and modified their time and depth utilisation. Birds with chicks dived deeper during daylight (mean maximum depth of 280 m vs. 205 m for those incubating). At night, birds with chicks spent twice as much time diving as those incubating, but birds at both stages never dived beyond 30 m. Movements to greater depths by brooding birds are consistent with the vertical distribution of myctophid fish which are the main prey. As chick provisioning limits trip duration, it is suggested that it is more efficient for parents to change their diving patterns rather than to restrict their foraging range. Received: 23 June 1997 / Accepted: 3 November 1997     

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.     

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.     

Behavioural temperature preference in a brooding male pipefish Syngnathus typhle

In the broad‐nosed pipefish Syngnathus typhle, brooding males positioned themselves significantly more often towards the warmer part (18° C) of an aquarium, whereas females were indifferent in this respect. This behavioural temperature preference may increase male brooding rate and indirectly influence patterns of mating competition.