Brooding behavior in the shallow‐water brittle star Ophioderma wahlbergii

Brooding behavior and the brooded young of Ophioderma wahlbergii, a common, large, shallow‐water brittle star from South Africa, are described for the first time. Monthly samples of 20 specimens were collected from June 2013 to May 2014 (n=240 in total). The species was shown to be gonochoric. Females reached maturity at 17 mm disc diameter (dd), and their ovaries contained 5±3 yolky eggs of mean diameter 0.25±0.1 mm. No seasonal trends in reproduction were found, and >50% of females examined in each month were brooding. Brooding individuals contained an average of 7±6 and up to 33 developing young. Small stages were more frequent than larger young, suggesting that juveniles either emerge at different sizes, or more likely suffer mortality during development. Young within individual adults were of different clutches, but those within individual bursae were all of the same stage. No signs of larval stages were found, indicating that development is direct. Given the large size of emerging juveniles, the species is likely to be matrotrophic and hence truly viviparous. Brooding is a recent discovery in Ophioderma and, so far, the only known brooder has about 1000 small embryos. This study shows quite a different reproductive strategy within the genus, with few, large eggs developing into the largest brooded young known from any species of ophiuroid.     

An unusual hermaphrodite reproductive trait in the Antarctic brooding bivalve Lissarca miliaris (Philobryidae) from the Scotia Sea, Southern Ocean

The Antarctic marine environment is extreme in its low temperatures and short periods of primary productivity. Invertebrates must therefore adapt to maximise reproductive output where low temperature and limited food slow larval development. Brooding is a common reproductive trait in Antarctic marine bivalves; larval development occurs within the mantle cavity, and larvae are released as fully developed young. Lissarca miliaris is a small, short-lived, shallow-water brooding bivalve of circum-Antarctic distribution and found most abundant in the sub-Antarctic Magellan Region and islands of the Scotia Arc. Here, an unusual hermaphrodite reproductive trait is described for L. miliaris from King George Island (62°14′S, 58°38′W) and Signy Island (60°42′S, 45°36′W), Antarctica, using histological and dissection techniques. Specimens demonstrate simultaneous and sequential hermaphrodite traits; male and female gonads develop simultaneously, but the production of oocytes is reduced while testes are ripe. Functional females are more abundant in specimens above 3 mm shell length, although male reproductive tissue persists and functional males are found in all size classes. The number of previtellogenic oocytes produced by far exceeds the number of oocytes extruded and brooded, which may indicate an ancestral link to a planktotrophic past. Hermaphroditism in L. miliaris maximises reproductive efficiency in a short-lived species, in which the female’s capacity to brood its young is limited, and demonstrates a specialised adaptation to a cold stenothermal and food-limited environment prevailing in the Southern Ocean.     

Effect of reduced pH on shells of brooded veligers in the estuarine bivalve Ostrea chilensis Philippi 1845

The oyster Ostrea chilensis develops in estuaries and incubates its embryos inside the pallial cavity. Reduced external salinity triggers valve closure and isolation of the brood chamber, which in turn alters conditions in the pallial fluid, including pH reductions ranging from 7.65 (SD = 0.05) to 6.97 (SD = 0.02) in non-brooding females and 6.96 (SD = 0.10) in brooding females after 12 h of isolation. Exposing veliger larvae to acidic pH's (5 and 3) decreased the thickness of the embryonic shell valves. Calcium, sodium, chlorine, tin, sulphur, and magnesium were the most important (> 99%) elements constituting the veliger shells. Calcium content in the pallial cavity fluid increased with continued isolation in both brooding and non-brooding females, but calcium remained as the primary component (about 94%) of embryonic shells and maintained its normal proportion with respect to the rest of the elements at all tested pH's. The increased calcium in the pallial fluid was identified mainly as coming from the shells of brooding females. If any neutralizing elements were coming from embryonic shell valves, all elements in those shells must have been solubilising to the same degree. Veligers ceased all further shell growth while isolated within the female's brood chamber. However, veliger shell growth resumed once females were returned to high-salinity seawater. Our study shows that female isolation of the mantle cavity, often considered an adaptive response to the periodically reduced salinities of estuarine waters, can in fact generate adverse effects on brooded embryos.     

Structural study of the ovary,oogenesis and brooding in Tonicia lebruni (Polyplacophora Chitonidae) from Patagonia

Tonicia lebruni, a common, lower intertidal and subtidal chiton inhabiting Patagonian rocky shores, is a gonochoristic iteroparous species producing large eggs (≈ 400 μm in diameter), which are fertilized and brooded within the pallial groves until released as juveniles. A free larval stage is absent, despite this, T. lebruni is widely distributed along the south‐western Atlantic. At Puerto Deseado, T. lebruni has a marked seasonality in the reproductive cycle, reproducing only once a year. The reproductive period is quite short and defined in time: spawning and brooding take place during the late austral winter and beginning of spring. Recovery of the female gonad starts very soon after spawning. Oogenesis takes about 10–11 months for completion. Brood size is correlated with length of maternal individual. The number of embryos per brood varied between 785 and 5945. Extensive resorption of abortive eggs is viewed as related to limitation of space available for brooding. The egg hull is formed by a large number of minute pentagonal or hexagonal plates each one bearing a short spine bent onto the egg surface. The morphology and the surface of the hull could contribute to the cohesiveness of the brooded egg mass within the pallial grooves.     

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.     

Double brooding and offspring desertion in the barn owl Tyto alba

Many bird species produce two annual broods during a single breeding season. However, not all individuals reproduce twice in the same year suggesting that double brooding is condition‐dependent. In contrast to most raptors and owls, the barn owl Tyto alba produces two annual clutches in most worldwide distributed populations. Nevertheless, the determinants of double brooding are still poorly studied. We performed such a study in a Swiss barn owl population monitored between 1990 and 2014. The annual frequency of double brooding varied from 0 to 14% for males and 0 to 59% for females. The likelihood of double brooding was higher when individuals initiated their first clutch early rather than late in the season and when males had few rather than many offspring at the first nest. Despite the reproductive benefits of double brooding (single‐ and double‐brooded individuals produced 3.97 ± 0.11 and 7.07 ± 0.24 fledglings, respectively), double brooding appears to be traded off against offspring quality because at the first nest double‐brooded males produced poorer quality offspring than single‐brooded males. This might explain why females desert their first mate to produce a second brood with another male without jeopardizing reproductive success at the first nest. Furthermore, the reproductive cycle being very long in the barn owl (120 d from start of laying to offspring independence), selection may have favoured behaviours that accelerate the initiation of a second annual brood. Accordingly, half of the double‐brooded females abandoned their young offspring to look for a new partner in order to initiate the second breeding attempt, 9.48 d earlier than when producing the second brood with the same partner. We conclude that male and female barn owls adopt different reproductive strategies. Females have more opportunities to reproduce twice in a single season than males because mothers are not strictly required during the entire rearing period in contrast to fathers. A high proportion of male floaters may also encourage females to desert their first brood to re‐nest with a new male who is free of parental care duties.     

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.     

The effect of parental age,experience and historical reproductive success on wandering albatross (Diomedea exulans) chick growth and survival

Growth and survival of altricial young are influenced by their parents’ abilities to invest in a breeding attempt. As a result, chick growth and survival in one breeding season may be indicative of their parents’ long-term reproductive potential. To determine whether variation in long-term reproductive success is driven by differential breeding investment, parental care and chick growth in wandering albatrosses (Diomedea exulans) were correlated with parental historical reproductive success. Effects of age and breeding experience (determined from past breeding attempts) and pre-laying body condition (mass–size indices) on chick growth and survival also were tested. Longer brooding of chicks increased their survival, but length of chick brooding did not differ between historically unproductive and successful breeders. Past reproductive success also was not correlated with chick growth rates or fledging mass or size. Chick brooding period, chick growth rates, final mass and size were independent of parental body condition. Older and more experienced parents brooded chicks for longer and their chicks grew faster, supporting previous findings that breeding competence is a learnt skill. Chick care and growth characteristics differed more between than within pairs, suggesting that differences in these characteristics are driven by variation among pairs.     

Brooding in Psolus patagonicus (Echinodermata: Holothuroidea) from Argentina, SW Atlantic Ocean

The mode, season, and time of brooding, egg diameter, egg number per brood, and the characteristics of newly released juveniles of Psolus patagonicus were investigated off Mar del Plata, Buenos Aires, Argentina, between October 1999 and February 2001. Individuals were attached to the Patagonian scallop, Zygochlamys patagonica. Spawning occurs between February and March. The mean egg diameter, 887 ± 26 μm, is the highest reported for the family Psolidae. Eggs are brooded under the mother’s sole until they develop into crawling juveniles within 7 months. The largest embryos reached a length of 1,941 ± 228 μm in September. During the brooding period (February–September) the number of brooded embryos decreased while their size increased. Our study confirms brooding behaviour in female P. patagonicus.     

The reproductive biology of Theromyzon tessulatum (Glossiphoniidae: Hirudinoidea), with comments on Theromyzon rude

The reproductive biology and behaviour of Theromyzon tessalatum is described from the commencement of copulation to the release of the young and the death of the parent. Copulation occurs several times over a10–20 day period with either the same or different partners. Eggs were laid6–14 days after copulation in usually four cocoons each containing approximately 100 eggs. The cocoons were brooded by the parents and the young, on development of the embryonic attachment organ and later by the posterior sucker, attached to the ventral surface of the parent's abdomen. The young detached from the parent either on contact with a suitable host for a blood meal or after approximately five months just prior to the parent's death.     

Brooding sea anemones (Cnidaria: Anthozoa: Actiniaria): paragons of diversity in mode,morphology, and maternity

Brooding has been reported in at least 57 species of sea anemone. More than three quarters (44/57) of the species that are known to brood have been described since the last comprehensive treatment of brooding in this lineage. Different authors focusing on different taxonomic groups within sea anemones over the last 115 years have collectively produced an imprecise and inconsistent set of terminology with respect to brooding in general and to the variety of conditions of brooding in particular. In this review, I characterize brooding as a behavior in which offspring are retained by the adult to at least the juvenile stage, in contrast with the more common release of eggs, embryos, or larvae. Brooding occurs in two primary modes, internal and external, in which offspring may be produced via sexual or asexual means. I categorize structures associated with external brooding in three types: pits, chambers, and grooves. Early inferences that external brooding has a primarily bipolar distribution continue to be supported with current data, but it is doubtful that small size and simultaneous hermaphroditism are correlated with brooding in sea anemones. Finally, I identify open questions about brooding in sea anemones and suggest future lines of research that will broaden our understanding of this phenomenon.     

Oxygen consumption rates of adults and chicks during brooding in king quail (Coturnix chinensis)

Oxygen consumption rates were measured in chicks (0–7 days of age), and in non-brooding and brooding adults. Brooded chicks maintained a constant oxygen consumption rate at a chamber ambient temperature of 10–35°C (0–5 days of age: 2.95ml O₂·g^-1·h^-1 and 6–17 days of age: 5.80 ml O₂·g^-1·h^-1) while unbrooded chicks increased oxygen consumption rate at ambient temperature below 30°C to double the brooded oxygen consumption rate at 25 and 15°C for chicks < 5 days of age and>5 days of age, respectively. The massspecific oxygen consumption rate of breeding male and females (non-brooding) were significantly elevated within the thermoneutral zone thermal neutral zone (28–35°C) in comparison to non-breeding adults. Below the thermal neutral zone, oxygen consumption rate was not significantly different. The elevation in oxygen consumption rate of breeding quail was not correlated with the presence of broodpatches, which developed only in females, but is a seasonal adjustment in metabolism. Male and females that actively brooded one to five chicks had significantly higher oxygen consumption rate than non-brooding quail at ambient temperature below 30°C. Brooding oxygen consumption rate was constant during day and night, indicating a temporary suppression of the circadian rhythm of metabolism. Brooding oxygen consumption rate increased significantly with brood number, but neither adult body mass nor adult sex were significant factors in the relationship between brooding oxygen consumption rate and ambient temperature. The proportion of daylight hours that chicks were brooded by parents was negatively correlated with ambient temperature. After chicks were 5 days old brooding time was reduced but brooding oxygen consumption rate was unchanged. Heat from the brooding parent appeared to originate mainly from the apteria under the wings and legs rather than the broodpatch. The parental heat contribution to chick temperature regulation below the chicks' thermal neutral zone is achieved by increasing parental thermal conductance by a feedback control similar to that suggested for the control of egg temperature via the brood-patch. It is concluded that the brooding period is an energetic burden to parent quail, and the magnitude of the cost increases directly with brood number and inversely with ambient temperature during this period. The oxygen consumption rate of brooding parents was 5.80–6.90 ml O₂·g^-1·h^-1 (ambient temperature 10–15°C) at night and up to 5.10 ml O₂·g^-1·h^-1 (ambient temperature 18°C) during the day, which are 100 and 40% higher than non-brooding birds, respectively.Abbreviations bm body mass - SMR standard metabolic rate - T _a ambient temperature - T _b body temperature - I/O₂ oxygen consumption rate - C _wet wet thermal conductance - TNZ thermal neutral zone - ANOVA analysis of variance - ANCOVA analysis of covariance     

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.     

False killer whales (Pseudorca crassidens) from Japan and South Africa: Differences in growth and reproduction

Age and reproductive information for 65 false killer whales stranded in South Africa in 1981 are compared with similar material from 156 animals examined from drive fisheries in Japan in 1979 and 1980. Sizes at birth, sexual maturation, and physical maturity all indicated that both sexes were 10%–20% larger in Japan than South Africa. Females reached sexual maturation at similar ages (8–10.5 yr) in both populations, and although sample sizes were too small to establish male ages at puberty precisely the ranges in Japan (10.5–18.5 yr) and South Africa (5.25–17.5 yr) were not inconsistent. The initial ovulation rate for females from South Africa was 65% lower (and the apparent pregnancy rate 82% lower) than those from Japan and there were fewer animals ≤2 yr old within the school, but the magnitude of these differences suggests that the stranded school's reproductive performance was probably impaired. Collectively these comparisons and the literature indicate substantive size differences between false killer whales in different populations, although the patterns of growth appear similar. Firm conclusions about any geographical differences in reproduction require additional data.     

Immediate early gene expression associated with induction of brooding behavior in Japanese quail

Certain species can be induced to foster infant or neonatal animals through the process of sensitization. We induced brooding behavior in adult Japanese quail through repeated exposure to foster chicks across five 20-min trials. Brooding behavior was characterized by a bird allowing chicks to approach and remain underneath its wings while assuming a distinctive stationary crouching posture, preening, and feather fluffing. Birds who did not show brooding behavior actively avoided chicks. Among the birds that brooded chicks, females brooded chicks for longer durations compared to males. Brooding females continued a regular daily egg laying pattern; males showed no significant changes in testosterone levels after exposure to chicks. In a second experiment, we measured expression of two immediate early gene (IEG) protein products, ZENK and Fos, to identify the brain regions activated or inhibited by brooding behavior in females. ZENK and Fos expression in brooding or sensitized females (SF) were compared with expression in nonmaternal females with chicks (NMF) and with females without chicks and with blocks as control objects (BL). There was a reduced density of ZENK-like immunoreactive (ZENK-lir) cells in the medial preoptic nucleus (POM) in NMF birds. In SF birds, the density of Fos-like immunoreactive (Fos-lir) cells was elevated in the bed nucleus stria terminalis, medial portion (BSTm), and ectostriatum (E). These experiments begin to define the neural circuitry underlying brooding behavior in Japanese quail, and establish a model for future studies of the neural mechanisms of avian parental behavior.     

Egg mass destroying behaviour of the female giant water bugLethocerus deyrollei Vuillefroy (Heteroptera: Belostomatidae)

After being laid on emergent aquatic vegetation, the egg masses ofLethocerus deyrollei are brooded by the male. In laboratory studies, females were observed to destroy egg masses and ingest the fluid of eggs. Brooding males fought with these attackers at first, but then gave up the defense and mated with them. After destroying the egg masses, females laid new ones at the same sites on the same night or the following one, and males brooded the new offspring. The population density of this species is very low. Most males engage in brooding and cease to become acceptable mates after most of the females lay the first egg masses. It is costly for females to search out free males in the aquatic vegetation. By destroying egg masses, however, individual females can gain new mates with little exertion and can make them brood their own offspring. Furthermore, the survival of their own offspring increases with the elimination of their competitors.     

Response of chicks to two diets of differing energy levels under conditions of brooding with or without supplemental heat

A 2×2 factorial experiment was conducted to determine the performance and certain physiological parameters of 200 day-old chicks fed diets containing either 2600 or 3000 kcal metabolizable energy (ME) per kilogram for a period of 28 days under conditions of brooding with or without supplemental heat in a hot humid tropical area. The results indicated that within each dietary energy level, there was no significant difference in growth rates of chicks brooded with or without supplemental heat, however, the high energy diet significantly (P<0.01) promoted greater weight gains than the low energy diet. Brooding chicks with supplemental heat and with the high energy diet, decreased feed intake and improved feed conversion efficiency. Chicks brooded without supplemental heat consumed significantly (P<0.01) less water than those brooded with heat, irrespective of the dietary energy level. Mortality and blood glucose levels were not affected by the heat and dietary energy treatments. Thyroid weight expressed as percentage of body weight, haemoglobin and hematocrit values were significantly (P<0.01) higher for chicks brooded without supplemental heat. On the other hand, dietary energy levels did not exert any effect on these physiological parameters. No significant heat and dietary energy level interaction effects were noted on all the parameters considered under this trial.     

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.     

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.