Seasonal plasticity of brain aromatase mRNA expression in glia: divergence across sex and vocal phenotypes

Although teleost fishes have the highest levels of brain aromatase (estrogen synthase) compared to other vertebrates, little is known of its regulation and function in specific brain areas. Previously, we characterized the distribution of aromatase in the brain of midshipman fish, a model system for identifying the neural and endocrine basis of vocal-acoustic communication and alternative male reproductive tactics. Here, we quantified seasonal changes in brain aromatase mRNA expression in the inter- and intrasexually dimorphic sonic motor nucleus (SMN) and in the preoptic area (POA) in males and females in relation to seasonal changes in circulating steroid hormone levels and reproductive behaviors. Aromatase mRNA expression was compared within each sex throughout non-reproductive, pre-nesting, and nesting periods as well as between sexes within each season. Intrasexual (male) differences were also compared within the nesting period. Females had higher mRNA levels in the pre-nesting period when their steroid levels peaked, while acoustically courting (type I) males had highest expression during the nesting period when their steroid levels peaked. Females had significantly higher levels of expression than type I males in all brain areas, but only during the pre-nesting period. During the nesting period, non-courting type II males had significantly higher levels of aromatase mRNA in the SMN but equivalent levels in the POA compared to type I males and females. These results demonstrate seasonal and sex differences in brain aromatase mRNA expression in a teleost fish and suggest a role for aromatase in the expression of vocal-acoustic and alternative male reproductive phenotypes.     

A Test of the Effect of Male Song on Female Nesting Behaviour in the Serin (Serinus serinus): a Field Playback Experiment

It is well established, through laboratory experiments, that male song in birds can stimulate female reproductive activity, affecting their behaviour and physiology, such as follicular growth, nest building and egg‐laying. However no clear demonstration has yet been provided that this effect works under natural conditions. Previous work in natural populations of serins showed that female nest‐building behaviour correlated with male singing time. Furthermore male serin song peaked exactly in the day that rapid follicular growth was estimated to start in females, suggesting that in this species song may also serve to stimulate the female's reproductive development. Direct causal evidence, however, was lacking. We conducted field playback experiments to investigate how song can influence female nesting activity during nest building. Our results show that females who listened daily to playbacks of serin songs, during the nest‐building stage, spent more time nest building than females that were not exposed to additional songs. Moreover, the singing behaviour of the mated males was not affected by the playbacks, suggesting that the song playback treatment had a direct positive effect on female nesting behaviour.     

Mating system and spawning cycle in the blenny,Istiblennius enosimae,at Kagoshima,Japan

Synopsis Field observations on reproductive ecology and territoriality of the blennyIstiblennius enosimae, were made in a tidepool at Hanaze Beach, Kagoshima Prefecture, Japan during the summer of 1988. This blenny was herbivorous, and nesting males (> 73 mm SL) maintained territories around nest sites, which were located in rocky crevices of the tidepool. Males courted females wandering near their nests, and spawnings coincided with neap tides. Males guarded the eggs until the embryos hatched at following spring tides. It was suggested that this semilunar spawning cycle guarantees a maximum dispersal of newly hatched embryos away from natal tidepool. Male reproductive success was related to large body size and/or large nest size. There is a size-assortative relationship between male and female among pairs. Egg predation rates by fishes, crabs and sea urchins were not correlated with the body size of male blennies.     

Temporal Variation in Decisions about Parental Care in Bluegill, Lepomis macrochirus

Parental investment theory states that an individual will trade‐off present and future reproductive potential to maximize lifetime reproductive success. Only when parental care is costly in terms of reduced future reproductive potential should individuals be sensitive to changes in the value of current offspring and adjust their care. Here, we examine temporal variation in parental care decision‐making in bluegill (Lepomis macrochirus), in which care is provided by males called ‘parentals’. Previous research has shown that parentals that nest early in the breeding season are in higher energetic condition than those that nest later, and early nesting males appear not to pay an opportunity cost to their care in terms of reduced future reproductive potential. Early nesting males also may have higher paternity in their broods than later nesting males. To examine the parental care decisions made by early and mid‐season nesting parentals, we experimentally reduced males’ perceived paternity by swapping eggs between nests. We found that experimental males that nested early in the breeding season adjusted their brood defence behaviour similarly to control males, which had sham egg swaps performed. Conversely, experimental males that nested mid‐season significantly decreased their brood defence behaviour after the manipulation as compared with control males. Thus, unlike mid‐season nesting males, early nesting males appear relatively insensitive to changes in brood value (paternity), possibly because early nesting males pay little cost in terms of reduced future reproductive potential to providing full care or because these males have a predisposition to high paternity.     

Nesting, courtship and kidney hypertrophy in Schistocephalus-infected male three-spined stickleback from an upland lake

The effect of Schistocephalus solidus infection on reproductive development and behaviour of male three-spined stickleback Gasterosteus aculeatus from an upland lake (Llyn Frongoch, Wales, U.K.) was investigated. Uninfected and infected males were collected on two separate occasions during the 2005 breeding season and encouraged to build nests under favourable laboratory conditions. Male nuptial colouration, courtship levels and nesting activity were recorded daily over two separate 21 day studies. Completed nests were removed, encouraging males to build multiple nests. On termination of each study, males were dissected and the kidney and any S. solidus plerocercoids were removed and weighed. In contrast to uninfected males, which readily built multiple nests, no infected males completed a nest during either study. Infected males also exhibited significantly reduced courtship levels, nesting activity, nuptial colouration, kidney development and body condition, compared with uninfected fish. Among infected three-spined stickleback, courtship and nesting behaviours tended to be more severely impacted in fish harbouring heavier plerocercoid burdens. In contrast to other populations, male three-spined stickleback from Llyn Frongoch appear to be unable to overcome the negative impacts of infections on reproductive development and behaviour when provided with short-term favourable conditions. Discrepancies between populations might have been related to the trophic status at the site of capture, emphasizing the importance of studying the biological effects of infections under different environmental conditions.     

Intra‐ and Intersexual swim bladder dimorphisms in the plainfin midshipman fish (Porichthys notatus): Implications of swim bladder proximity to the inner ear for sound pressure detection

The plainfin midshipman fish, Porichthys notatus , is a nocturnal marine teleost that uses social acoustic signals for communication during the breeding season. Nesting type I males produce multiharmonic advertisement calls by contracting their swim bladder sonic muscles to attract females for courtship and spawning while subsequently attracting cuckholding type II males. Here, we report intra‐ and intersexual dimorphisms of the swim bladder in a vocal teleost fish and detail the swim bladder dimorphisms in the three sexual phenotypes (females, type I and II males) of plainfin midshipman fish. Micro‐computerized tomography revealed that females and type II males have prominent, horn‐like rostral swim bladder extensions that project toward the inner ear end organs (saccule, lagena, and utricle). The rostral swim bladder extensions were longer, and the distance between these swim bladder extensions and each inner‐ear end organ type was significantly shorter in both females and type II males compared to that in type I males. Our results revealed that the normalized swim bladder length of females and type II males was longer than that in type I males while there was no difference in normalized swim bladder width among the three sexual phenotypes. We predict that these intrasexual and intersexual differences in swim bladder morphology among midshipman sexual phenotypes will afford greater sound pressure sensitivity and higher frequency detection in females and type II males and facilitate the detection and localization of conspecifics in shallow water environments, like those in which midshipman breed and nest.     

Differential effects of 11-ketotestosterone on dimorphic traits in a teleost with alternative male reproductive morphs

Species with dimorphic males typically have one morph (type I) associated with territoriality and courtship, and another morph (type II) associated with cuckoldry. In teleost fishes, type I males generally have higher levels of the androgen 11-ketotestosterone (KT) than type II males. Is KT causal to phenotypic differences between morphs? We investigated this question in the midshipman fish (Porichthys notatus) in which type I males have detectable levels of KT during the breeding season, whereas levels in type II males are usually undetectable. Type I midshipman will either cuckold or hold territories and court females, whereas type II males are only known to cuckold. Acoustic courtship by type I's is supported by the sonic motor nucleus, which innervates a sound-producing sonic muscle. Type I males have larger sonic motor nuclei and larger sonic muscles than type II males, consistent with the more dynamic vocal repertoire of type I's. Here, we tested whether intraperitoneal KT implants in adult type II males would induce type I male-like traits in brain, sonic muscle, and behavior. Type II's treated with KT did not differ from blank-implanted type II's in sonic motor nucleus volume. Sonic muscle mass increased in KT-implanted type II's, but did not reach the relative mass naturally observed in type I's. While neither territoriality nor courtship were induced, cuckoldry behavior intensified in KT-implanted type II's. Thus, for some but not all characters, KT exaggerated the expression of already existing type II male traits rather than inducing the type I male-like traits of territoriality, courtship, and an expansive vocal motor system.     

Nonsequential developmental trajectories lead to dimorphic vocal circuitry for males with alternative reproductive tactics

Midshipman fish, Porichthys notatus, have two male reproductive morphs: type I males generate long duration advertisement calls (“hums”) to attract females to a nest; type II males sneak-spawn and, like females, do not produce mate calls but generate short duration agonistic calls. A vocal pacemaker circuit includes: motoneurons in the caudal brain stem and rostral spinal cord that innervate vocal/sonic muscles; pacemaker neurons that are located ventrolateral to motoneurons and establish their fundamental discharge frequency; and a ventral medullary nucleus that couples the motoneuron-pacemaker circuit bilaterally. Transneuronal biocytin transport identified morph-specific developmental trajectories for the vocal circuit. Among nonreproductive, juvenile type I males, motoneuron soma size and motor nucleus volume increase most during a stage prior to sexual maturation. An additional increase in motoneuron size and nucleus volume is coupled to the greatest increase in pacemaker soma size at a stage coincident with the onset of sexual maturity; ventral medullary neurons show similar growth increments during both stages. Type II males (and females) mature with no or little change in cell size or motor nucleus volume. The results indicate that alternative mating tactics are paralleled by alternative developmental trajectories for the neurons that determine tactic-specific behaviors, in this case vocalizations. Together with aging data based on otolith growth, the results support the hypothesis that alternative male morphs in midshipman fish adopt nonsequential, mutually exclusive life history tactics. © 1996 John Wiley & Sons, Inc.     

Dyadic relationships in nesting males of the three-spined stickleback, Gasterosteus aculeatus

Multidimensional scaling analysis of nest site location, nesting interval, and aggressive and mating interactions revealed that male three-spined sticklebacks, Gasterosteus aculeatus, formed nesting clusters comprising five patterns of dyadic relationships. These patterns were defined by intervening variables such as size difference between the two males, nest site locations, synchronization of nesting cycles (egg presence in the nest), distance between two nests, and nest raiding behaviours. Several patterns of dyadic relationships were integrated among nesting males and their constellations indicated an expression of the social structure. Through an understanding the social structure, I described effects of social context or situations on individual reproductive success.     

Endocrinology of oviposition in the tuatara (Sphenodon punctatus): I. Plasma steroids and prostaglandins during natural nesting

Plasma concentrations of estradiol, progesterone, prostaglandin (PG) E2 and PGF were measured during three stages of the natural nesting cycle of the tuatara (Sphenodon punctatus), a rare New Zealand reptile. Specifically, we tested whether nesting activity in this species is correlated with significant modifications in plasma concentrations of these hormones. Tuatara dig a nest over a period of several nights, oviposit a complete clutch on a single night, and then guard that nest for several nights. We observed no significant changes in mean plasma concentrations of estradiol or progesterone among the different stages of nesting. In contrast, PGE2 was elevated during nest digging and oviposition but declined significantly during nest guarding. Plasma PGF was elevated during nest digging, rose significantly during oviposition, and declined to basal levels during nest guarding. These data indicate that oviposition in reptiles is associated with elevated plasma concentrations of PGs, suggesting that these hormones function in causing oviducal contractions and/or luteolysis. Moreover, these data suggest that the role of PGs in oviducal function may have been conserved throughout evolution of the amniote vertebrates.     

Impacts of nest predators and weather on reproductive success and population limitation in a long‐distance migratory songbird

Although avian nesting success is much studied, little is known about the relative importance of the factors that contribute to annual reproductive success and population limitation, especially for long‐distance migratory songbird species. We combined a field experiment limiting access to nests by mammalian predators with modeling of long‐term field data of American redstarts (Parulidae: Setophaga ruticilla) to assess the effects of multiple environmental variables on breeding success and population limitation. Experimental treatment (baffles placed around tree boles beneath active nests; n = 71) increased nesting success of this single‐brooded species significantly (77 vs 50% in controls; n = 343), demonstrating that scansorial mammals, primarily red squirrels Tamiasciurus hudsonicus and eastern chipmunks Tamias striatus, reduced reproductive success. Based on unbaffled nests (n = 466), daily nest survival varied annually, and was positively influenced by May temperature and negatively by sciurid nest predator abundance. Daily nest survival was also influenced positively by June rainfall, and declined with nest age but not with calendar date. Since nest failure was overwhelmingly caused by nest predation, these significant climate and nest‐age effects in our models are indirect, likely influencing nest predator and/or nesting bird behaviors that in turn influenced nest predation. Redstart population density had no effect on nesting success, after accounting for other factors. Annual reproductive success accounted for 34% of the variability in annual population change in redstarts in our study area. Our findings document 1) breeding season population limitation in this species, 2) a link between tree masting and bird population dynamics via mammal population fluctuations, 3) the independent contributions of summer versus winter population processes in a migratory species, and 4) the potential complexity of climate‐biotic interactions.     

Alternative Male Spawning Tactics and Acoustic Signals in the Plainfin Midshipman Fish Porichthys notatus Girard (Teleostei,Batrachoididae)

The plainfin midshipman Porichthys notatus has two male reproductive morphs, ‘Type I’ and ‘Type II’, which are distinguishable by their physical traits alone. Type I males are eight times larger in body mass than Type II males and have a six-fold larger relative sonic (vocal) muscle mass than Type II males. In contrast, the testicles of Type II males are seven times larger than those of Type I males. This study demonstrates morph-specific patterns of reproduction, including acoustic signals, for Type I and II males. Field censuses of nests showed that only Type 1 males maintained nests. Type II males and females transiently appeared in these nests in association with each other. Infra-red video and hydrophone recordings in aquaria showed that Type I males maintained nests and readily vocalized. Long-duration ‘hums’ and sequences of short-duration ‘grunts’ were produced during advertisement and agonistic contexts, respectively. Humming Type I males attracted females to their nests, pair-spawned, and then guarded egg clutches alone. By contrast, Type II males neither acoustically courted females nor maintained available nest sites, but rather ‘sneak-’ or ‘satellite-spawned’ at the nests of Type I males. Type II males infrequently produced low amplitude, short duration grunts that were similar in spectral, temporal and amplitude characteristics to the grunts of females. Type II males appear to be obligate sexual parasites of the nest-building, mate-calling, and egg-guarding Type I males. The dimorphic body and vocal muscle traits of the two male morphs in the plainfin midshipman are thus paralleled by a divergence in their reproductive tactics and the properties of their acoustic signals.     

Nest Defence Behaviour of the Eurasian Kestrel (Falco tinnunculus) Against Human Predators

Man has become the main predator of many animal species. Because the characteristics of humans are quite distinct with respect to other terrestrial predators, the cost and benefits of defence behaviour may also differ. In this paper, we study the factors affecting nest defence behaviour of the Eurasian Kestrel ( Falco tinnunculus canariensis ) against a potential human predator throughout the reproductive cycle, as well as the balance of cost and benefits of this behaviour. The study population inhabits the island of Tenerife, and the nests are located on cliffs. The intensity of the defensive behaviour was unrelated to the frequency of human visits, prey abundance (Orthoptera, Coleoptera, lizards, birds and rodents), laying date, or number of offspring in the nest. Both males and females increased their defensive behaviour as the nesting period advanced, particularly when the chicks were older than 15 days. Moreover, the intensity of the defensive behaviour, especially of males, decreased when nests were more inaccessible. Although nest defence behaviour against humans appeared to be similar to those against other predators, the benefits are not clear because the probability of nest robbing was greater for these more aggressive pairs.     

Seasonal changes in condition, reproduction and fecundity in the wild European rabbit (Oryctolagus cuniculus)

A total of 1248 rabbits ( Oryctolagus amiculus ) were shot on farmland in Cambridgeshire, UK over a period of three years. This provided pooled estimates of changes in reproductive and body condition and of fecundity during the annual cycle. Both males and females showed a significant annual cycle in reproductive condition as indicated by changes in the size of the gonads and accessory glands of reproduction. No females were pregnant during October, November and December, but males with active spermatogenesis were found during every month of the year. The distribution of pregnancies through the year showed that the reproductive season varied greatly between individuals. Peak fecundity occurred during April, May and June. On average, each female conceived 23.9 and suckled 17.2 young per breeding season. Proportionately more young died during the early stages of the reproductive season. The body weight of adult males, but not of females, varied seasonally. Body condition (kidney fat index) in adults was maximal at the start of the breeding season and minimal at the end.     

Condition-dependent nesting in bluegill sunfish Lepomis macrochirus

1. There are two prominent, nonmutually exclusive hypotheses to explain the timing of reproduction in animals: energetic constraint and adaptive behaviour. 2. We tested these hypotheses by quantifying the costs and benefits of nesting at different times in the season for male bluegill sunfish Lepomis macrochirus, a species with paternal care, in Lake Opinicon (Ontario, Canada). 3. The value of nesting at different times during the breeding season (RSb) was determined from spawning individuals as RSb = Pb x Cb x Sb x Ob, where Pb is the probability of spawning during each bout b, Cb is the expected brood size, Sb is the expected brood survivorship to 'swim-up', and Ob is the survivorship of free-swimming fry to age 1 year. 4. The results show that the value of nesting peaks during the middle of the season. However, nesting patterns varied with male condition and not all males nested at the peak. 5. Larger males, which were able to nest multiple times, first nested early in the season when overwinter survivorship of offspring and renesting opportunities later in the season were maximized. These males had the highest seasonal reproductive success. 6. Smaller males, which nested a single time, delayed nesting until the middle of the season when spawning opportunities and brood sizes were greatest. 7. These data suggest that both energetics and adaptive behaviour play roles in determining the timing of reproduction.     

Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection

European starlings ( Sturnus vulgaris ) introduced to North America compete with native cavity-nesting birds for nest sites. I examined whether natural selection could favour a strategy of delayed nesting in a population of northern flickers ( Colaptes auratus ), a native woodpecker, to reduce overlap in breeding phenology with starling competitors. I developed a mathematical model based on reproductive parameters for a population of flickers from central British Columbia, Canada. On average, 7% of flicker nests each year were usurped by starlings; daily probabilities of takeover declined through the season but were relatively low (1–2%). Flickers laid between 3 and 13 eggs and there was a negative correlation between clutch size and date. The probability of renesting after nest failure also declined during the season, but renesting intervals (2–19 days) were not associated with female age, or stage of nest loss. The model suggested that costs of delaying reproduction would outweigh benefits of an early start except when the probability of nest usurpation is very high (>75%) early in the season and declines rapidly through the summer. Thus, early laying dates should be favoured especially in northern latitudes where breeding seasons are short.     

Factors Affecting Daily Nest Survival of Burrowing Owls Within Black-Tailed Prairie Dog Colonies

ABSTRACT Identifying environmental parameters that influence probability of nest predation is important for developing and implementing effective management strategies for species of conservation concern. We estimated daily nest survival for a migratory population of burrowing owls (Athene cunicularia) breeding in black-tailed prairie dog (Cynomys ludovicianus) colonies in Wyoming, USA. We compared estimates based on 3 common approaches: apparent nesting success, Mayfield estimates, and a model-based logistic-exposure approach. We also examined whether 8 intrinsic and extrinsic factors affected daily nest survival in burrowing owls. Positive biases in apparent nest survival were low (3–6%), probably because prior knowledge of nest locations and colonial behavior among nesting pairs facilitated discovery of most nests early in the nesting cycle. Daily nest survival increased as the breeding season progressed, was negatively correlated with ambient temperature, was positively correlated with nest-burrow tunnel length, and decreased as the nesting cycle progressed. Environmental features were similar between failed and successful nests based on 95% confidence intervals, but the seasonal midpoint was earlier for failed nests (31 May) compared to successful nests (15 Jun). The large annual variation in nest survival (a 15.3% increase between 2003 and 2004) accentuates the importance of multiyear studies when estimating reproductive parameters and when examining the factors that affect those parameters. Failure to locate and monitor nests throughout the breeding season may yield biased estimates of nesting success in burrowing owls (and possibly other species), and some of the variation in nesting success among years and across study sites may be explained by annual and spatial variation in ambient temperature. Any management actions that result in fewer prairie dogs, shorter burrow lengths, or earlier nesting may adversely affect reproductive success of burrowing owls.     

Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons

In one species of vocalizing (sonic) fish, the midshipman (Porichthys notatus), there are two classes of sexually mature males--Types I and II--distinguished by a number of traits including body size, gonad size, and reproductive tactic. The larger Type-I males (unlike Type-II males and females) build nests, guard eggs, and generate several types of vocalizations. Sound production by Type-I males is paralleled by a proportionate increase of 600% in their sonic muscle mass. The motor volley from ventral occipital roots innervating the sonic muscles establishes their contraction rate and, in turn, the fundamental frequency of emitted sounds. Electrical stimulation of the midbrain in every male and female elicited a rhythmic sonic discharge as recorded in the occipital roots; however, the fundamental frequency was slightly, but significantly, higher (20%) in Type-I males. Intracellular recording from identified motoneurons and presumed presynaptic "pacemaker" neurons showed their synaptic and action potentials had the same frequency as that of the nerve volley in every male and female. Reconstructions of physiologically identified motoneurons and pacemaker neurons following intracellular horseradish-peroxidase (HRP) filling showed their somata and dendrites to be 100-300% larger in Type-I males. These data unambiguously show that the size of a target muscle is correlated with the size of both the respective motoneurons and their presynaptic afferent neurons. As discussed, this implies that the dramatic increase in neuron size in the sonic motor system of Type-I males is causally dependent upon expansion of the sonic muscle. It is further likely that the more modest sex difference in the rhythmic central discharge is established by the intrinsic membrane properties of sonic neurons. These results also corroborate, at a number of behavioral, morphological, and neurophysiological levels, that the sonic motor system of "sneak spawning" Type-II males is similar to that of females. Thus, unlike the vocalizing Type-I males, sexual differentiation of the reproductive system in Type-II males is not linked to concomitant changes in the neurophysiological and morphological features of the sonic motor circuit.     

Semi-lunar spawning cycle and mating tactics in the marine goby <Emphasis Type="Italic">Asterropteryx semipunctata</Emphasis>

The reproductive behaviors of the marine goby Asterropteryx semipunctata were studied at Sakurajima, Kagoshima, Japan. Spawning occurred from late June to early October with a peak at 3–4 days after the full and new moon. This semi-lunar cycle might be advantageous to reducing nest-egg mortality but may not to larvae dispersion. Large males maintained spawning nests, and females spawned a whole clutch at a nest but with multiple males during a season. Females were less likely to be choosy due probably to a predation risk and/or nesting male shortage. Smaller males adopted sneaking tactics, and some of them became nesting males.     

Changes in reproductive physiology and behaviour over the nesting cycle in male three‐spined sticklebacks

Plasma 11‐Ketotestosterone (11 KT) and testosterone (T) levels and spiggin‐mRNA levels, as well as the kidney‐somatic index ( I _K) were measured in sexual males and in paternal males at the middle (5 days paternal) and at the end (8 days paternal with hatched eggs) of the nesting cycle in three‐spined sticklebacks Gasterosteus aculeatus from two populations. Glueing (using threads of 11 KT induced kidney‐protein spiggin) and fanning behaviour was measured daily. Fanning increased in paternal fish and remained low in sexual males. Plasma 11 KT and T levels, on the other hand, declined significantly in parental compared to sexual males as did spiggin expression, I _K and glueing behaviour. Thus, the drastic decrease in circulating 11 KT levels during the later parental phase may have resulted in an energy‐saving decrease in spiggin‐production and glueing, when this was no longer needed for nest maintenance. In addition, the mRNA levels of the β‐subunits of both gonadotropins, luteinising hormone (LH) and follicle stimulating hormone (FSH) were measured. The expression of both gonadotropins declined in the parental phase (not significant for β‐FSH in one of the populations) which was consistent with a decline in androgen levels possibly controlled via decreased gonadotropin secretion.