Sensory pollutants alter bird phenology and fitness across a continent.

Expansion of anthropogenic noise and night lighting across our planet1,2 is of increasing conservation concern3-6. Despite growing knowledge of physiological and behavioural responses to these stimuli from single-species and local-scale studies, whether these pollutants affect fitness is less clear, as is how and why species vary in their sensitivity to these anthropic stressors. Here we leverage a large citizen science dataset paired with high-resolution noise and light data from across the contiguous United States to assess how these stimuli affect reproductive success in 142 bird species. We find responses to both sensory pollutants linked to the functional traits and habitat affiliations of species. For example, overall nest success was negatively correlated with noise among birds in closed environments. Species-specific changes in reproductive timing and hatching success in response to noise exposure were explained by vocalization frequency, nesting location and diet. Additionally, increased light-gathering ability of species' eyes was associated with stronger advancements in reproductive timing in response to light exposure, potentially creating phenological mismatches7. Unexpectedly, better light-gathering ability was linked to reduced clutch failure and increased overall nest success in response to light exposure, raising important questions about how responses to sensory pollutants counteract or exacerbate responses to other aspects of global change, such as climate warming. These findings demonstrate that anthropogenic noise and light can substantially affect breeding bird phenology and fitness, and underscore the need to consider sensory pollutants alongside traditional dimensions of the environment that typically inform biodiversity conservation.

Ecological light pollution affects anuran calling season, daily calling period, and sensitivity to light in natural Brazilian wetlands.

Ecological light pollution alters an environment's light cycle, potentially affecting photoperiod-controlled behavior. Anurans, for example, generally breed nocturnally, and the influence of light pollution on their natural history may therefore be especially strong. In this study, we tested this hypothesis by measuring male calling behavior of anuran communities in natural wetlands in southern Brazil exposed or not exposed to street lights. We recorded seasonal and diel calling activity and calling response to a light pulse. The peak calling season differed between continuously lit and unlit locations with most species in illuminated wetlands shortening their calling season and calling earlier in the year. In unlit breeding sites, Boana pulchella, Pseudis minuta, and Pseudopaludicola falcipes confined their calling activity to well-defined hours of the night, but in continuously lit areas, these species called more continuously through the night. A 2-minute light pulse inhibited calling, but only in unlit wetlands. After a light pulse, frogs quickly resumed calling-suggesting acclimatization to brief artificial light exposure. Our field experiment presents a convincing example of ecological light pollution showing that artificial light alters the seasonal and diel calling time of some South American wetland anurans. It also documents their acclimatization to brief lighting when being continuously exposed to light.

Social behavioral testing and brain magnetic resonance imaging in chicks exposed to mobile phone radiation during development.

BACKGROUND: The potential adverse effect of mobile phone radiation is currently an area of great concern in the field of public health. In the present study, we aimed to investigate the effect of mobile phone radiation (900 MHz radiofrequency) during hatching on postnatal social behaviors in chicks, as well as the effect on brain size and structural maturity estimated using 3.0 T magnetic resonance imaging. At day 4 of incubation, 76 normally developing chick embryos were divided into the control group (n = 39) and the radiation group (n = 37). Eggs in the radiation group were exposed to mobile phone radiation for 10 h each day from day 4 to 19 of incubation. Behavioral tests were performed 4 days after hatching. T2-weighted MR imaging and diffusion tensor imaging (DTI) were subsequently performed. The size of different brain subdivisions (telencephalon, optic lobe, brain stem, and cerebellum) and corresponding DTI parameters were measured. The Chi-square test and the student's t test were used for statistical analysis. P < 0.05 was considered statistically significant. RESULTS: Compared with controls, chicks in the radiation group showed significantly slower aggregation responses (14.87 ± 10.06 vs. 7.48 ± 4.31 s, respectively; P < 0.05), lower belongingness (23.71 ± 8.72 vs. 11.45 ± 6.53 s, respectively; P < 0.05), and weaker vocalization (53.23 ± 8.60 vs. 60.01 ± 10.45 dB/30 s, respectively; P < 0.05). No significant differences were found between the radiation and control group for brain size and structural maturity, except for cerebellum size, which was significantly smaller in the radiation group (28.40 ± 1.95 vs. 29.95 ± 1.41 cm(2), P < 0.05). The hatching and heteroplasia rates were also calculated and no significant difference was found between the two groups. CONCLUSIONS: Mobile phone radiation exposure during chick embryogenesis impaired social behaviors after hatching and possibly induced cerebellar retardation. This indicates potential adverse effects of mobile phone radiation on brain development.

Mice Lacking Serotonin 2C Receptors Have increased Affective Responses to Aversive Stimuli.

Although central serotonergic systems are known to influence responses to noxious stimuli, mechanisms underlying serotonergic modulation of pain responses are unclear. We proposed that serotonin 2C receptors (5-HT2CRs), which are expressed within brain regions implicated in sensory and affective responses to pain, contribute to the serotonergic modulation of pain responses. In mice constitutively lacking 5-HT2CRs (2CKO mice) we found normal baseline sensory responses to noxious thermal, mechanical and chemical stimuli. In contrast, 2CKO mice exhibited a selective enhancement of affect-related ultrasonic afterdischarge vocalizations in response to footshock. Enhanced affect-related responses to noxious stimuli were also exhibited by 2CKO mice in a fear-sensitized startle assay. The extent to which a brief series of unconditioned footshocks produced enhancement of acoustic startle responses was markedly increased in 2CKO mice. As mesolimbic dopamine pathways influence affective responses to noxious stimuli, and these pathways are disinhibited in 2CKO mice, we examined the sensitivity of footshock-induced enhancement of startle to dopamine receptor blockade. Systemic administration of the dopamine D2/D3 receptor antagonist raclopride selectively reduced footshock-induced enhancement of startle without influencing baseline acoustic startle responses. We propose that 5-HT2CRs regulate affective behavioral responses to unconditioned aversive stimuli through mechanisms involving the disinhibition of ascending dopaminergic pathways.

Light pollution alters the phenology of dawn and dusk singing in common European songbirds.

Artificial night lighting is expanding globally, but its ecological consequences remain little understood. Animals often use changes in day length as a cue to time seasonal behaviour. Artificial night lighting may influence the perception of day length, and may thus affect both circadian and circannual rhythms. Over a 3.5 month period, from winter to breeding, we recorded daily singing activity of six common songbird species in 12 woodland sites, half of which were affected by street lighting. We previously reported on analyses suggesting that artificial night lighting affects the daily timing of singing in five species. The main aim of this study was to investigate whether the presence of artificial night lighting is also associated with the seasonal occurrence of dawn and dusk singing. We found that in four species dawn and dusk singing developed earlier in the year at sites exposed to light pollution. We also examined the effects of weather conditions and found that rain and low temperatures negatively affected the occurrence of dawn and dusk singing. Our results support the hypothesis that artificial night lighting alters natural seasonal rhythms, independently of other effects of urbanization. The fitness consequences of the observed changes in seasonal timing of behaviour remain unknown.

A risk function for behavioral disruption of Blainville's beaked whales (Mesoplodon densirostris) from mid-frequency active sonar.

There is increasing concern about the potential effects of noise pollution on marine life in the world's oceans. For marine mammals, anthropogenic sounds may cause behavioral disruption, and this can be quantified using a risk function that relates sound exposure to a measured behavioral response. Beaked whales are a taxon of deep diving whales that may be particularly susceptible to naval sonar as the species has been associated with sonar-related mass stranding events. Here we derive the first empirical risk function for Blainville's beaked whales (Mesoplodon densirostris) by combining in situ data from passive acoustic monitoring of animal vocalizations and navy sonar operations with precise ship tracks and sound field modeling. The hydrophone array at the Atlantic Undersea Test and Evaluation Center, Bahamas, was used to locate vocalizing groups of Blainville's beaked whales and identify sonar transmissions before, during, and after Mid-Frequency Active (MFA) sonar operations. Sonar transmission times and source levels were combined with ship tracks using a sound propagation model to estimate the received level (RL) at each hydrophone. A generalized additive model was fitted to data to model the presence or absence of the start of foraging dives in 30-minute periods as a function of the corresponding sonar RL at the hydrophone closest to the center of each group. This model was then used to construct a risk function that can be used to estimate the probability of a behavioral change (cessation of foraging) the individual members of a Blainville's beaked whale population might experience as a function of sonar RL. The function predicts a 0.5 probability of disturbance at a RL of 150 dBrms re µPa (CI: 144 to 155) This is 15dB lower than the level used historically by the US Navy in their risk assessments but 10 dB higher than the current 140 dB step-function.

Circadian regulation of bird song, call, and locomotor behavior by pineal melatonin in the zebra finch.

As both a photoreceptor and pacemaker in the avian circadian clock system, the pineal gland is crucial for maintaining and synchronizing overt circadian rhythms in processes such as locomotor activity and body temperature through its circadian secretion of the pineal hormone melatonin. In addition to receptor presence in circadian and visual system structures, high-affinity melatonin binding and receptor mRNA are present in the song control system of male oscine passeriform birds. The present study explores the role of pineal melatonin in circadian organization of singing and calling behavior in comparison to locomotor activity under different lighting conditions. Similar to locomotor activity, both singing and calling behavior were regulated on a circadian basis by the central clock system through pineal melatonin, since these behaviors free-ran with a circadian period and since pinealectomy abolished them in constant environmental conditions. Further, rhythmic melatonin administration restored their rhythmicity. However, the rates by which these behaviors became arrhythmic and the rates of their entrainment to rhythmic melatonin administration differed among locomotor activity, singing and calling under constant dim light and constant bright light. Overall, the study demonstrates a role for pineal melatonin in regulating circadian oscillations of avian vocalizations in addition to locomotor activity. It is suggested that these behaviors might be controlled by separable circadian clockworks and that pineal melatonin entrains them all through a circadian clock.

Two genetic loci control syllable sequences of ultrasonic courtship vocalizations in inbred mice.

BACKGROUND: The ultrasonic vocalizations (USV) of courting male mice are known to possess a phonetic structure with a complex combination of several syllables. The genetic mechanisms underlying the syllable sequence organization were investigated. RESULTS: This study compared syllable sequence organization in two inbred strains of mice, 129S4/SvJae (129) and C57BL6J (B6), and demonstrated that they possessed two mutually exclusive phenotypes. The 129S4/SvJae (129) strain frequently exhibited a "chevron-wave" USV pattern, which was characterized by the repetition of chevron-type syllables. The C57BL/6J strain produced a "staccato" USV pattern, which was characterized by the repetition of short-type syllables. An F1 strain obtained by crossing the 129S4/SvJae and C57BL/6J strains produced only the staccato phenotype. The chevron-wave and staccato phenotypes reappeared in the F2 generations, following the Mendelian law of independent assortment. CONCLUSIONS: These results suggest that two genetic loci control the organization of syllable sequences. These loci were occupied by the staccato and chevron-wave alleles in the B6 and 129 mouse strains, respectively. Recombination of these alleles might lead to the diversity of USV patterns produced by mice.

Effect of chronic intermittent exposure to AM radiofrequency field on responses to various types of noxious stimuli in growing rats.

There are several reports of altered pain sensation after exposure (from a few minutes to hours in single or repeated doses for 2-3 weeks) to electromagnetic fields (EMF) in adults. The commonly utilized noxious stimulus is radiant heat. The nociceptive responses are known to be influenced by characteristics of stimulus, organism, and environment. We studied the pattern of nociceptive responses to various noxious stimuli in growing rats exposed to radiofrequency field (73.5 MHz amplitude modulated, 16 Hz power density 1.33 mw/cm(2), SAR = 0.4 w/kg) for 45 d (2 h/d). Threshold current for stimulation of nociceptive afferents to mediate motor response of tail (TF), vocalization during stimulus (VD), and vocalization after discharge (VA); the withdrawal latency of tail (TFL) and hind paw (HPL) to thermal noxious stimulus and tonic pain responses were recorded in every rat. The TFL was not affected, HPL was decreased (p < 0.01), and the thresholds of TF and VD were not affected, while, that of VA was significantly decreased. The tonic pain rating was decreased (p < 0.01). A decrease in the threshold of VA (p < 0.01) is indicative of an increase in the emotional component of the response to the phasic pain, whereas a decrease in the pain rating indicates analgesia in response to the tonic pain. The results of our study suggest that chronic (45 d), intermittent (2 h/d) amplitude modulated RF field exposure to the peripubertal rat increases the emotional component of phasic pain over a basal eaualgesic state, while late response to tonic pain is decreased. The data suggest that amplitude modulated RF field differentially affects the mechanisms involved in the processing of various noxious stimuli.

Seasonal and diurnal patterns of black-capped chickadee (Poecile atricapillus) vocal production.

Changes in vocal behaviour observed in temperate songbirds have been linked to changes in photoperiod. Research has focused on the fluctuation of hormones that lead to photosensitivity, photostimulation and photorefractoriness, as well as the 'dawn chorus' observed in numerous species. However, photoperiod in the natural environment is a complex event that occurs as seasons change. To determine the natural relationships between photoperiod and vocal behaviour we sampled vocal production of black-capped chickadees for three major vocal classes over one year at dawn, meridian and sunset. Fee-bee song production increased twice, once in the winter and once in the spring, and occurred almost exclusively at dawn. Chick-a-dee call production was highest in autumn and winter generally at the meridian. Gargle production did not differ significantly by season; however, the most gargle production occurred during the winter at the meridian.

Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies.

Fifty-kHz ultrasonic vocalizations have been proposed to reflect a positive appetitive affective state in rats, being consistently linked to the positive appetitive behavior. In the first study, we examined the brain substrates of 50-kHz ultrasonic vocalizations (USVs) by using localized electrical stimulation of the brain (ESB) at various sites that are known to mediate reward. We found that the brain areas that produced ESB-induced 50-kHz calls are the areas that have previously been shown to support the most vigorous self-stimulation behavior (prefrontal cortex, nucleus accumbens, ventral pallidum, lateral preoptic area, lateral hypothalamus, ventral tegmental area, and raphe). Importantly, all animals that showed repeatable ESB-induced 50-kHz USVs demonstrated self-stimulation behavior. In the second study, conditioned place preference was assessed following microinjection of the mu-opiate agonist Tyr-D-Ala-Gly-N-methyl-Phe-Gly-ol (DAMGO) directly into the ventral tegmental area (VTA) at a dose previously found to be rewarding. Animals that showed more 50-kHz USVs in response to drug injections compared to vehicle injections showed significant place preferences, whereas animals that did not show elevated vocalization to DAMGO did not show place preference. In experiment 3, we examined the effect of VTA electrolytic lesions, 6-OHDA lesions, and the effect of the D1/D2 dopamine antagonist flupenthixol (0 and 0.8 mg/kg, i.p.) on 50-kHz ultrasonic vocalizations. We found that these manipulations all selectively reduced 50-kHz ultrasonic vocalizations, and that these effects could be disassociated from any side effects. These data are consistent with the proposition that 50-kHz calls are tightly linked to reward in rats and that the neural circuit of 50-kHz calls closely overlaps that of ESB self-stimulation reward, drug reward, and the mesolimbic dopamine system.

On the role of the reticular formation in vocal pattern generation.

This review is an attempt to localize the brain region responsible for pattern generation of species-specific vocalizations. A catalogue is set up, listing the criteria considered to be essential for a vocal pattern generator. According to this catalogue, a vocal pattern generator should show vocalization-correlated activity, starting before vocal onset and reflecting specific acoustic features of the vocalization. Artificial activation by electrical or glutamatergic stimulation should produce artificially sounding vocalization. Lesioning is expected to have an inhibitory or deteriorating effect on vocalization. Anatomically, a vocal pattern generator can be assumed to have direct or, at least, oligosynaptic connections with all the motoneuron pools involved in phonation. A survey of the literature reveals that the only area meeting all these criteria is a region, reaching from the parvocellular pontine reticular formation just above the superior olive through the lateral reticular formation around the facial nucleus and nucleus ambiguus down to the caudalmost medulla, including the dorsal and ventral reticular nuclei and nucleus retroambiguus. It is proposed that vocal pattern generation takes place within this whole region.

Prenatal malnutrition alters diazepam-mediated suppression of ultrasonic vocalizations in an age dependent manner.

The sensitivity of prenatally malnourished rats to the ultrasonic vocalization (USV) suppressant effect of diazepam (a non-specific benzodiazepine (BZ) receptor agonist) was investigated. Male offspring of dams provided with a protein deficient diet (6% casein) for 5 weeks prior to mating and throughout pregnancy were compared to the offspring of mothers provided with a diet of adequate protein content (25% casein). At postnatal day 7 or 11, pups were injected with vehicle or one of five doses of DZ (0.03, 0.1, 0.3, 1 or 3mg/kg) 30 min after removal from their dam. Thirty minutes later they were subjected to 2 min of cooling on a 20 degrees C surface and their USVs were quantified. DZ dose-dependently suppressed USV at both ages. At P7, the USV suppressant effect of DZ was the same for both groups. However, by P11 the prenatally malnourished rats showed significantly greater suppression of USV by 0.03 and 0.1mg/kg DZ than well-nourished controls. These differences were not related to degree of temperature loss or body weight. Thus, differential sensitivity to BZ receptor agonists develops in the second postnatal week in prenatally malnourished rats. This reflects either an altered program of development of the GABAergic system, or adaptive, compensatory changes in the GABAergic system in response to more extensive functional disturbances in the developing brain.

Projections of the ventrolateral pontine vocalization area in the squirrel monkey.

In four squirrel monkeys (Saimiri sciureus), the tracer biotin dextranamine (BDA) was injected into the ventrolateral pons at a site at which injection of the glutamate antagonist kynurenic acid blocked vocalization electrically elicited from the periaqueductal gray (PAG). Anterograde projections could be traced into all cranial motor and sensory nuclei involved in phonation, that is, the nucleus ambiguus, facial, hypoglossal and trigeminal motor nuclei, the motorneuron column in the ventral gray substance innervating the extrinsic laryngeal muscles, the nucleus retroambiguus, solitary tract and spinal trigeminal nuclei. Projections were also found into a number of auditory nuclei, namely the nucleus cochlearis-complex, superior olive, ventral and dorsal nuclei of the lateral lemniscus and inferior colliculus. Furthermore, there were projections into the reticular formation of the lateral and dorsocaudal medulla and lateral pons, into nucleus gracilis, inferior and medial vestibular nuclei, lateral reticular nucleus, ventral raphe, pontine gray, superior colliculus, PAG and mediodorsal thalamic nucleus. Injection of the tracer wheat germ agglutinin-conjugated horseradish peroxidase into the ventrolateral pontine vocalization-blocking area in one animal yielded retrograde labeling throughout the PAG. Injection of BDA into a vocalization-eliciting site of the PAG in another animal yielded projections into the ventrolateral pontine vocalization-blocking area. It is concluded that the ventral paralemniscal area in the ventrolateral pons represents a relay station of the descending periaqueductal vocalization-controlling pathway.

Sonic and electric fish: at the crossroads of neuroethology and behavioral neuroendocrinology.

Field and laboratory studies of weakly electric and sound-producing teleost fishes demonstrate how steroidal and non-steroidal hormones mediate the translation of neural events into behavior. The development of this research program has depended upon an interdisciplinary neuroethological approach that has characterized the neurophysiological properties of the motor and sensory pathways that lead to the production and detection of easily quantified highly stereotyped behaviors, namely, electric organ discharges (EODs) and vocalizations. Neuroethological studies of these teleosts have now integrated a behavioral neuroendocrinology approach that has provided several examples of how hormone-sensitive neurobiological traits contribute to adaptive behavioral plasticity in natural habitats. As such, these studies provide guideposts for comparable studies in other groups of teleosts and vertebrates in general.

Electroacupuncture attenuates morphine withdrawal signs and c-Fos expression in the central nucleus of the amygdala in freely moving rats.

Experimental efforts for understanding the mechanisms of electroacupuncture (EA) for opiate addiction are partially hampered by restraint stress. In unrestrained animals, it is difficult to perform EA stimulation at acupuncture points frequently selected on the four limbs. The present study was performed to evaluate the effect of EA at the acupuncture point Shen-Shu (BL.23) on morphine withdrawal signs and c-Fos expression of the amygdala in freely moving rats or restrained rats. We applied immunohistochemistry to detect c-Fos-positive nuclei. Corticosterone levels and behavioral responses were measured during EA stimulation. The needles were bilaterally inserted and fixed at BL.23, and 100-Hz electric stimulation was conducted 30 min before naloxone-precipitated withdrawal. In both freely moving rats and restrained rats, EA significantly reduced the signs of morphine withdrawal. Notably, EA stimulation in freely moving rats attenuated c-Fos expression in the central nucleus of the amygdala while EA in restrained animals increased this response. In addition, the restrained rats emitted greater levels of vocalization and facial expression than freely moving rats during EA stimulation. Corticosterone levels were also significantly higher in restrained animals after EA stimulation. The new EA paradigm demonstrated in the present study might help the analysis of certain physiological responses induced by EA that would otherwise have been hindered by restraint stress.

Selectivity of canary HVC neurons for the bird's own song: modulation by photoperiodic conditions.

To what extent seasonal factors modify the neuronal functional properties within the nuclei of the avian song system remains an open question. In adult songbirds, neurons of the song premotor nucleus HVC (used as a proper name) exhibit selective responses for the bird's own song (BOS). Here we examine whether, outside the breeding season, when songs are less stereotyped, HVC neurons of male canaries still respond selectively to the BOS produced during this period. In an initial experiment, single-unit recordings (n = 114) revealed that the neuronal selectivity for the current BOS was attenuated in males exposed to a short-day photoperiod (typical of the nonbreeding season) compared with that found in males exposed to a long-day photoperiod. In long-day conditions, 35% of the cells responded to the BOS, whereas only 12% did in short-day conditions; there were four times more selective cells (d' > 1) in long-day than in short-day conditions. To determine whether these effects were the consequence of differences in acoustic features between breeding and nonbreeding songs, neurons (n = 72) recorded in short-day conditions were tested with both a short-day BOS and a long-day BOS. A low percentage of neurons exhibited responses to short-day or to long-day BOS (11% for each song). Responses of putative interneurons (spike duration < 0.4 ms) and of putative relay cells were similarly attenuated by the short-day conditions. These results strongly suggest that, in canary, rather than being a fixed property, the selectivity for the BOS moves along a continuum and peaks when the day length mimics the breeding conditions.

Partial muting leads to age-dependent modification of motor patterns underlying crystallized zebra finch song.

The crystallized structure of adult zebra finch (Taeniopygia guttata) song is modifiable if sensory feedback is altered during sound production. Such song plasticity has been studied by examining acoustic modifications to the motif; however, the underlying changes to the vocal motor patterns of these acoustic modifications have not been addressed. Adult birds in two age categories (young=90-120 days or middle aged 150-250 days) that sang crystallized song were used in the experiment. Vocal motor patterns were monitored by recording respiratory air sac pressure before, during, and after song plasticity was induced by partial or complete reduction of phonation (i.e., "partial muting"). Birds were recorded until changes in air sac pressure patterns underlying the song structure were observed (up to 160 days). Young adult birds were more likely to insert shorter duration (<125 ms) expiratory pulses (EPs) into the motif than middle-aged adults. These shorter duration EPs were produced with a unique pressure pattern relative to the intact song, and therefore appeared to be generated by novel motor gestures. Stuttering (atypical repetition of an EP) was observed when these novel EPs were inserted into the motif, regardless of age. The EP of the distance call, which is also a learned vocalization in zebra finches, showed a similar reduction in duration if EPs were also shortened in the song. The emergence of shorter duration EPs was not related to sound production, or nonspecific effects of the surgical procedure, which suggests an age-dependent neural process for song plasticity.

Ultrasonic singing by the blue-throated hummingbird: a comparison between production and perception.

Blue-throated hummingbirds produce elaborate songs extending into the ultrasonic frequency range, up to 30 kHz. Ultrasonic song elements include harmonics and extensions of audible notes, non-harmonic components of audible syllables, and sounds produced at frequencies above 20 kHz without corresponding hearing range sound. To determine whether ultrasonic song elements function in intraspecific communication, we tested the hearing range of male and female blue-throated hummingbirds. We measured auditory thresholds for tone pips ranging from 1 kHz to 50 kHz using auditory brainstem responses. Neither male nor female blue-throated hummingbirds appear to be able to hear above 7 kHz. No auditory brainstem responses could be detected between 8 and 50 kHz at 90 dB. This high-frequency cutoff is well within the range reported for other species of birds. These results suggest that high-frequency song elements are not used in intraspecific communication. We propose that the restricted hummingbird hearing range may exemplify a phylogenetic constraint.

Modelos animales de ansiedad incondicionada (I) / Animal models of unconditioned anxiety (I)

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