Socially induced brain differentiation in a cooperatively breeding songbird

Birds living in social groups establish dominance hierarchies, and taking up the dominant position influences behaviour and physiological parameters. In cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), the transition from subordinate helper to dominant breeder male induces the production of a new type of song. This song contains a large number of new syllables and differs in temporal pattern from duet songs produced by all other group members. Here we show that this change in social status of adult males affects the morphology of a behavioural control circuit, the song control system of songbirds that is composed of large neuron populations. The volume of the song control areas HVC and RA and their gene-expression levels depend on males' social status. Dominant males have several times larger testes than subordinates, which is not reflected in circulating androgen and oestrogen levels. Our findings suggest a remarkable differentiation of adult vertebrate brains in relation to changing social cues.     

Variation in the oxytocin content of caprine corpora lutea across the breeding season

Ovarian tissues were obtained from cyclic goats during the early, mid and late breeding season. Immunoreactive oxytocin was measured by RIA in tissue extracts after chromatography on octadecylsilica cartridges. Luteal oxytocin concentrations were significantly greater during the early breeding season than during the mid or late breeding season. Oxytocin is luteolytic in goats. High concentrations of luteal oxytocin may be related to the high incidence of short estrus at the onset of the breeding season.     

Melatonin delays clutch initiation in a wild songbird

The hormone melatonin is known to play an important role in regulating many seasonal changes in physiology, morphology and behaviour. In birds, unlike in mammals, melatonin has thus far been thought to play little role in timing seasonal reproductive processes. This view is mainly derived from laboratory experiments on male birds. This study tests whether melatonin is capable of influencing the timing of clutch initiation in wild female songbirds. Free-living female great tits (Parus major) treated with melatonin-filled implants prior to the breeding season initiated their first clutch of the season significantly later than females carrying an empty implant. Melatonin treatment did not affect clutch size. Further, melatonin treatment did not delay the onset of daily activity in the wild nor adversely affect body mass in captivity compared with controls. These data suggest a previously unknown role for this hormone in regulating the timing of clutch initiation in the wild.     

Dynamic occupancy models reveal within‐breeding season movement up a habitat quality gradient by a migratory songbird

The timing of settlement decisions likely influences the quality of breeding site choices.This is particularly the case in migratory birds, because the conditions that enhance breeding success are often not apparent upon arrival after migration. A strategy that addresses this problem is to adjust settlement decisions when reliable information becomes available. We used a new indirect method – dynamic site occupancy modeling – to estimate apparent movement of black‐throated blue warblers Dendroica caerulescens among sites within a breeding season. Because individuals should disperse to sites that maximize their fitness, we hypothesized that warblers would move up a habitat quality gradient when opportunities arose. For our study species, that would involve moving into sites with greater shrub density and at higher elevation within northern hardwoods forest, as these two features are positively correlated with reproduction and apparent survival in this species. Although the probability of site occupancy in our study landscape remained consistent throughout the breeding season (range: 0.66–0.69), occupancy models revealed substantial support for apparent movement of individuals within the breeding season. The mean probability of emigration from a point count site was 0.21 (±0.03 SE), and the mean probability of immigration to a site not previously occupied was 0.51 (±0.05 SE). The spatial distribution of this movement was a function of habitat quality. A portion of the black‐throated blue warbler population appears to arrive on the breeding grounds and settle initially in sub‐optimal habitat, moving subsequently into high quality densely shrubbed habitat at higher elevations. This modeling approach provides a new means to test hypotheses about habitat selection and movement by using presence–non‐detection data.     

Developmental changes in malonate-related enzymes of rat brain.

Mitochondria and high-speed supernatant were prepared from rat brain homogenates at 0–50 days of age. The development of malonyl-CoA synthetase, malonyl-CoA decarboxylase, coenzyme A-transferases and acetyl-CoA hydrolase was examined and compared to de novo fatty acid biosynthesis. The specific activity of malonyl-CoA synthetase rose steeply between 6 and 10 days, and this sudden increase coincided with peak specific activity of fatty acid synthetase. Similarly, malonate activation by coenzyme A-transfer from succinyl-CoA increased rapidly at the same time. Transfer of the coenzyme A moiety from acetoacetyl-CoA was only minimal during this period. Brain mitochondria had active malonyl-CoA decarboxylase which showed an almost linear increase of specific activity between 0 and 50 days. Acetyl-CoA resulting from malonyl-CoA decarboxylation underwent enzymatic hydrolysis to acetate and free coenzyme A. Only traces of acetoacetate were recovered. In mitochondria, acetyl-CoA hydrolase increased progressively whereas the cytosolic enzyme had high specific activity at birth which declined slowly during maturation.     

Family- and sex-specific vocal traditions in a cooperatively breeding songbird

Although songbirds provide well-known examples of cultural transmission of vocalizations, little is known about this process in species that live in stable social groups. Here I describe complex vocal traditions in a cooperatively breeding songbird, the stripe-backed wren (Campylorhynchus nuchalis). Repertoires of stereotyped calls were recorded from individually marked males and females in cooperative family groups. Males in the same patriline, whether in the same group or in different groups, had call repertoires that were nearly identical. Females in the same matriline also had identical call repertoires; however, female calls never matched the calls of males in the same group or in any nearby groups. Unrelated birds almost never shared calls. Call repertoires are apparently learned preferentially from same-sex relatives within family groups, so that call traditions separately follow patrilines and matrilines. This unique pattern of transmission results in vocal cues that reflect both sex and kinship.     

Territorial aggression does not feed back on testosterone in a multiple-brooded songbird species with breeding and non-breeding season territoriality,the European stonechat

Testosterone mediates reproductive behaviours in male vertebrates. For example, breeding season territoriality depends on testosterone in many species of birds and in some, territorial interactions feed back on testosterone concentrations. However, the degree to which territorial behaviour and testosterone are associated differs even between species with seemingly similar life histories, especially between species that also defend territories outside the breeding season. Here, we investigate the link between territorial behaviour and testosterone in European stonechats. Previous studies found that territorial aggression in stonechats depends on testosterone in a breeding, but not in a non-breeding context. We investigated whether stonechats show a rise in testosterone during simulated territorial intrusions (STI) during the breeding season. Post-capture testosterone concentrations of males caught after an STI were not higher than those of males caught in a control situation regardless of breeding stage. However, most of the males would have been able to mount a testosterone response because the same individuals that did not increase testosterone during the STI showed a substantial increase in testosterone after injections of gonadotropin-releasing hormone (GnRH). GnRH-induced and post-capture testosterone concentrations were positively correlated and both decreased with successive breeding stages. Further, territory owners with a short latency to attack the decoy expressed higher post-capture testosterone concentrations than males with a longer latency to attack the decoy. Thus, there is no evidence for behavioural feedback on testosterone concentrations during male-male interactions in stonechats. In combination with previous studies our data suggest that testosterone functions as an on/off switch of high intensity territorial aggression during the breeding season in stonechats. The among-species variation in the androgen control of territorial behaviour may be only partly a result of environmental differences. Instead, potential differences in how territoriality evolved in different species may have influenced whether and how a reproductive hormone such as testosterone was co-opted into the mechanistic control of territorial behaviour.     

Immunocontraception in wild horses (Equus caballus) extends reproductive cycling beyond the normal breeding season

Background

Although the physiological effects of immunocontraceptive treatment with porcine zona pellucida (PZP) have been well studied, little is known about PZP''s effects on the scheduling of reproductive cycling. Recent behavioral research has suggested that recipients of PZP extend the receptive breeding period into what is normally the non-breeding season.

Methodology/Principal Findings

To determine if this is the case, we compiled foaling data from wild horses (Equus caballus) living on Shackleford Banks, North Carolina for 4 years pre- and 8 years post-contraception management with PZP (pre-contraception, n = 65 births from 45 mares; post-contraception, n = 97 births from 46 mares). Gestation lasts approximately 11–12 months in wild horses, placing conception at approximately 11.5 months prior to birth. Since the contraception program began in January 2000, foaling has occurred over a significantly broader range than it had before the contraception program. Foaling in PZP recipients (n = 45 births from 27 mares) has consistently occurred over a broader range than has foaling in non-recipients (n = 52 births from 19 mares). In addition, current recipients of PZP foaled later in the year than did prior recipient and non-recipient mares. Females receiving more consecutive PZP applications gave birth later in the season than did females receiving fewer applications. Finally, the efficacy of PZP declined with increasing consecutive applications before reaching 100% after five consecutive applications.

Conclusions/Significance

For a gregarious species such as the horse, the extension of reproductive cycling into the fall months has important social consequences, including decreased group stability and the extension of male reproductive behavior. In addition, reproductive cycling into the fall months could have long-term effects on foal survivorship. Managers should consider these factors before enacting immunocontraceptive programs in new populations. We suggest minor alterations to management strategies to help alleviate such unintended effects in new populations.     

Reproductive development according to elevation in a seasonally breeding male songbird

Seasonal temperate zone breeders respond to increasing day length to anticipate the approach of spring breeding conditions. Other (supplementary) environmental cues, such as temperature and precipitation, were historically thought to play unimportant roles in reproductive timing. We demonstrate variation in reproductive timing across small geographic distances by examining the vernal testicular recrudescence of adult song sparrows (Melospiza melodia morphna) breeding in coastal (0–10 m elevation) and montane (280–1220 m elevation) habitats. Each year, these birds experienced the same photoperiod, but were exposed to different supplementary cues that varied with altitude. Coastal birds experienced warmer and more stable temperatures during late winter and early spring than did montane birds. We measured bud opening, emergence of new green shoots, and arthropod biomass to monitor the pace of springs approach. New spring shoots emerged 2 months earlier on the coast than in the mountains and buds on flowering trees and shrubs also tended to open earlier at the coast. Arthropod biomass was similar in both the mountains and the coast during early spring, and began to increase in early summer. Reproductive morphology (i.e. testis volume and cloacal protuberance length) developed up to 2 months earlier on the coast than in the mountains. Testicular recrudescence occurred earlier on the coast in most years and proceeded at a faster rate in 1 year. Circulating levels of luteinizing hormone, follicle stimulating hormone and prolactin increased through the season, but did not correlate with differences between sites. Both populations responded similarly when exposed to identical photoperiodic cues in the laboratory. Therefore, we suggest that an integrated response to cues characteristic of location and elevation account for differences in patterns measured in the field.     

Auditory-vocal cholinergic pathway in the songbird brain

Male zebra finches learn to imitate a tutor's song through auditory and motor learning. The two main song control nuclei in the zebra finch forebrain, the higher vocal center (HVC) and the robust nucleus of the archistriatum (RA), receive cholinergic innervation from the ventral paleostriatum (VP) of the basal forebrain which may play a key role in song learning. By injecting neuroanatomical tracers, we found a topographically segregated pathway from nucleus ovoidalis (Ov) to VP that in turn projects in a topographic fashion to HVC and RA. Ov is a major relay in the main ascending auditory pathway. The results suggest that the cholinergic neurons in the VP responsible for song learning are regulated by auditory information from the Ov.     

Predation by sparrowhawks decreases with increased breeding density in a songbird,the great tit

Predators may regulate prey populations if predation rate increases with prey density. Alternatively, if space-limited (e.g. territorial) predators become satiated when prey exceed a certain density, increased prey abundance may lead to reduced predation rate. These alternatives have been difficult to test experimentally for mobile prey in the wild. We present such a test, manipulating the density of great tits (Parus major) by adding nest boxes in territories of sparrowhawks (Accipiter nisus). Predation rate was measured for young tits after they left the nests. Although the great tit is an important prey, there was no evidence for regulation during the breeding season: the rate of hawk predation declined with increasing density of tits. This result was not confounded by changes in breeding density of alternative prey species (other songbirds). Hawk predation can therefore favour dense breeding in a territorial (solitary) bird, and conspecific attraction and aggregation reported in several territorial species may partly result from predation pressure. This result also has potential implications for conservation work.     

Ovarian follicular population changes with the advance of the breeding season in intact and unilaterally ovariectomized ewes

In ewes at the 1st, 2nd or 4th oestrous cycle after unilateral ovariectomy, the ovulation rate remained constant at 1.5 in the control (sham-operated) ewes, but increased from 1.3 to 2.0 in unilaterally ovariectomized ewes. In control ewes, the proportion of preantral follicles declined significantly (P less than 0.05) with each oestrous cycle while the antral follicles increased as the breeding season progressed (P less than 0.05). In contrast, after unilateral ovariectomy, the proportion of preantral and antral follicles remained constant throughout the cycles studied. The rate of atresia of antral follicles, especially those from small size classes, decreased significantly after one cycle of unilateral ovariectomy (P less than 0.05). Larger antral follicles had a different rate of atresia as the breeding season advanced. It is concluded that unilateral ovariectomy acutely decreased the rate of atresia and maintained the within-ovary equilibrium between preantral and antral follicles which otherwise would have decreased due to the depletion of preantral follicles with the advance of the breeding season.     

3beta-HSD activates DHEA in the songbird brain

Dehydroepiandrosterone (DHEA) is an abundant circulating prohormone in humans, with a variety of reported actions on central and peripheral tissues. Despite its abundance, the functions of DHEA are relatively unknown because common animal models (laboratory rats and mice) have very low DHEA levels in the blood. Over the past decade, we have obtained considerable evidence from avian studies demonstrating that (1) DHEA is an important circulating prohormone in songbirds and (2) the enzyme 3beta-hydroxysteroid dehydrogenase/isomerase (3beta-HSD), responsible for converting DHEA into a more active androgen, is expressed at high levels in the songbird brain. Here, we first review biochemical and molecular studies demonstrating the widespread activity and expression of 3beta-HSD in the adult and developing songbird brain. Studies examining neural 3beta-HSD activity show effects of sex, stress, and season that are region-specific. Second, we review studies showing seasonal and stress-related changes in circulating DHEA in captive and wild songbird species. Third, we describe evidence that DHEA treatment can stimulate song behavior and the growth of neural circuits controlling song behavior. Importantly, brain 3beta-HSD and aromatase can work in concert to locally metabolize DHEA into active androgens and estrogens, which are critical for controlling behavior and robust adult neuroplasticity in songbirds. DHEA is likely secreted by the avian gonads and/or adrenals, as is the case in humans, but DHEA may also be synthesized de novo in the songbird brain from cholesterol or other precursors. Irrespective of its source, DHEA seems to be an important prohormone in songbirds, and 3beta-HSD is a key enzyme in the songbird brain.     

Dominant male song performance reflects current immune state in a cooperatively breeding songbird

Conspicuous displays are thought to have evolved as signals of individual “quality”, though precisely what they encode remains a focus of debate. While high quality signals may be produced by high quality individuals due to “good genes” or favourable early‐life conditions, whether current immune state also impacts signalling performance remains poorly understood, particularly in social species. Here, we experimentally demonstrate that male song performance is impaired by immune system activation in the cooperatively breeding white‐browed sparrow weaver (Plocepasser mahali). We experimentally activated the immune system of free‐living dominant males via subcutaneous injection of phytohemagglutinin (PHA) and contrasted its effects with those of a control (phosphate buffered saline) injection. PHA‐challenged males showed significant reductions in both the duration and the rate of their song performance, relative to controls, and this could not be readily attributed to effects of the challenge on body mass, as no such effects were detected. Furthermore, male song performance prior to immune‐challenge predicted the scale of the inflammatory response to the challenge. Our findings suggest that song performance characteristics are impacted by current immune state. This link between current state and signal performance might therefore contribute to enforcing the honesty of signal performance characteristics. Impacts of current state on signaling may be of particular importance in social species, where subordinates may benefit from an ability to identify and subsequently challenge same‐sex dominants in a weakened state.     

Cereal breeding takes a walk on the wild side

Elite cultivated crop gene pools of the Triticeae tribe (wheat, barley and rye) exhibit limited genetic diversity, raising concerns about our ability to increase or simply sustain crop yield and quality in the face of dynamic environmental and biotic threats. Although exploiting their wild relatives as a source of novel alleles is challenging, it has provided notable successes in cereal improvement for >100 years. Increasingly facile gene discovery, improved enabling technologies for genetics and breeding and a better understanding of the factors limiting practical exploitation of exotic germplasm promise to transform existing, and accelerate the development of new, strategies for efficient and directed germplasm utilization.     

Short term, repeated exposure to rams during the transition into the breeding season improves the synchrony of mating in the breeding season

The ram effect is widely used in Mediterranean breeds of sheep but its use in temperate genotypes is restricted by breed seasonality. However, ewes from these highly seasonal genotypes are sensitive to stimulation by rams close to the onset of the natural breeding season. In this study we developed a pre-mating protocol of repeated, short-term exposure to rams (fence-line contact or vasectomised rams) beginning during late anoestrus and continuing into the breeding season. We hypothesised that this pre-mating protocol would synchronise the distribution of mating of North of England Mule ewes during the breeding season above that observed in ewes isolated from rams prior to mating. Ram-exposed ewes were given contact with rams (Experiment 1: fence-line; FR, n = 94 and Experiment 2: vasectomised rams; VR; n = 103) for 24 h on Days 0 (10 September), 17 and 34 of the experiment. Control ewes (Experiment 1; FC, n = 98 and Experiment 2; VC; n = 106) remained isolated from rams prior to mating. In Experiment 2, a subset of VR (n = 35) and VC ewes (n = 35) were blood sampled twice weekly to monitor their pre-mating progesterone profiles. At mating, harnessed entire rams were introduced, 17 or 16 days after the last ram exposure (Experiments 1 and 2) and raddle marks were recorded daily. The median time from ram introduction to mating was reduced in ewes given both fence-line and vasectomised ram contact (P < 0.001), leading to a more compact distribution of mating and lambing (At least P < 0.01). In the blood sampled VR ewes, there was a progressive decline in the number of days from ram exposure to the onset of dioestrus (at least P < 0.05). This observation indicates that the cycles in VR ewes became increasingly synchronised over the pre-mating period, a pattern not evident in VC ewes. In conclusion, repeated, short-term exposure of ewes to rams during the transition into the breeding season is an effective method of synchronising the distribution of mating during the breeding season.     

Morphological and functional changes of stallion spermatozoa after cryopreservation during breeding and non-breeding season

The study compared quality and freezability of stallion semen during breeding and non-breeding seasons. Ejaculates were collected twice per week from four stallions during May (n = 24) and December (n = 24). The semen was mixed with skim milk extender, centrifuged and resuspended in fresh extender. Aliquots of this sperm suspension were separated from extender and diluted in TALP medium for sperm evaluation or with cryoextender (type "Gent" or a combination of Triladyl and skim milk). Samples of 0.5ml were cryopreserved in straws using a programmed freezer. Parameters of sperm quality were evaluated before and after freezing/thawing. These included percentages of motile spermatozoa and of morphological intact sperm. Typical injuries were demonstrated by scanning electron microscopy (S.E.M.). The acrosomal status was visualised using FITC-conjugated peanut agglutinin, and the acrosome reaction was induced by calcium ionophore A 23187. The chromatin stability was estimated by acridine orange test.In winter, the average percentages of motile and morphologically normal sperm (67 and 74.3%, respectively) were higher than during the breeding season in May (59 and 65.9%; P < 0.05). After freezing/thawing the proportions of vital and intact sperm decreased significantly. The number of motile sperm declined to 15 and 18% in May and December (range 5-40%), and of morphologically intact sperm to 51% in both seasons. Results of S.E.M. showed typical membrane ruptures in the acrosomal region and some sperm with abnormal necks. The proportion of frozen sperm with spontaneous acrosome reaction was higher during winter (86.5 versus 77.0%), suggesting a higher degree of membrane reactivity. Percentages of spermatozoa with denaturated chromatin were minimal and showed minimal differences between fresh and frozen state, stallions or seasons. An additional decondensation treatment with papain and DTE revealed a slightly enhanced number of spermatozoa with denaturable DNA after cryopreservation, especially in December (5.4 +/- 1.3%). The influence of cryoextenders was not significant for most sperm parameters, but there was a high variability between the stallions. Altogether, the influence of factors on the quality of spermatozoa has the following rank order: cryopreservation > stallion > season. Different cellular structures seem to have different susceptibilities to physicochemical stress. The cryopreservation of sperm during December results in survival rates similar to those measured during the breeding season, even more important for successful preservation is the selection of suitable semen donors.     

Gregarious foraging in barn swallows after the breeding season

Aerial vertebrate foragers, e.g. insectivorous bats, martins and swallows, often show gregarious behavior such as colonial breeding, communal roosting and aggregating behavior during foraging. Studies of gregariousness in aerial foragers have mostly focused on colonial breeding or communal roosting, and only a few intensive studies have dealt with gregariousness during foraging. Here, we report on large and stable aggregations of barn swallows, Hirundo rustica, observed during daytime after the breeding season in Japan. Relatively large aggregations of 20 or more birds were located around poultry, pig and cattle farms and mounds of manure. The aggregations were stable in size both within-days and between-days. Their activities consisted only of repeated cycles of foraging and resting around the farms where their prey, the large black soldier fly Hermetia illuceus (>10 mm) and other medium (5–10 mm) flies, was dense. Distributions of swallows around the farms overlapped with the distributions of prey, and the size of the aggregations significantly correlated with the abundance of prey.     

An increase in parental investment during the breeding season

The intensity of nest-defence aggression by female redwinged black birds (Agelaius phoeniceus) with eggs decreased late in the breeding season, while aggression at this time increased amongst females defending broods. High predation pressure late in the breeding season decreased the probability of survival of the late nesting attempts, so that females with young had a much greater chance of success than females with eggs at this time. The observed changes in aggressive responses are predicted by the theory of parental investment.