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A core component of human language is its combinatorial sound system: meaningful signals are built from different combinations of meaningless sounds. Investigating whether nonhuman communication systems are also combinatorial is hampered by difficulties in identifying the extent to which vocalizations are constructed from shared, meaningless building blocks. Here we present an approach to circumvent this difficulty and show that a pair of functionally distinct chestnut-crowned babbler (Pomatostomus ruficeps) vocalizations can be decomposed into perceptibly distinct, meaningless entities that are shared across the 2 calls. Specifically, by focusing on the acoustic distinctiveness of sound elements using a habituation-discrimination paradigm on wild-caught babblers under standardized aviary conditions, we show that 2 multielement calls are composed of perceptibly distinct sounds that are reused in different arrangements across the 2 calls. Furthermore, and critically, we show that none of the 5 constituent elements elicits functionally relevant responses in receivers, indicating that the constituent sounds do not carry the meaning of the call and so are contextually meaningless. Our work, which allows combinatorial systems in animals to be more easily identified, suggests that animals can produce functionally distinct calls that are built in a way superficially reminiscent of the way that humans produce morphemes and words. The results reported lend credence to the recent idea that language's combinatorial system may have been preceded by a superficial stage where signalers neither needed to be cognitively aware of the combinatorial strategy in place, nor of its building blocks.
Assuntos
Passeriformes/fisiologia , Vocalização Animal/fisiologia , Acústica , Comunicação Animal , Animais , Idioma , SomRESUMO
Understanding how animals maximize reproductive success in variable environments is important in determining how populations will respond to increasingly extreme weather events predicted in the face of changing climates. Although temperature is generally considered a key factor in reproductive decisions, rainfall is also an important predictor of prey availability in arid environments. Here, we test the impact of weather (i.e., rainfall and temperature) on female reproductive investment in an arid-dwelling bird (i.e., clutch size and egg volume) and tradeoffs between the two. We predicted that female chestnut-crowned babblers (Pomatostomus ruficeps), endemic to the arid region of Australia, would increase clutch size at the expense of egg volume in response to variation in rainfall and temperature. We found that over 14 breeding seasons, clutch size decreased with increasing temperature, but increased following more rain. Egg volume, on the other hand, became larger as temperatures increased and, although not related to the amount of rain, was related to the number of days since the last rainfall. Finally, egg size decreased as clutch size increased, indicating a tradeoff between the two reproductive parameters. Our results suggest that chestnut-crowned babblers breed reactively in response to variable environments. We expect that clutch size variation in response to rain may reflect the impact of rain on arthropod abundance, whereas the effect of temperature may represent an established decline in clutch size observed in other seasonal breeders. As the tradeoff between clutch size and egg volume was modest, and clutch sizes were modified to a greater extent than egg volumes in response to rainfall, we suggest selection is more likely to increase offspring number than quality, at least in favorable years. Our results support the idea that reproductive investment is variable in fluctuating environments, which has implications for species living in habitats experiencing more extreme and less predictable weather as the global climate changes.
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[This corrects the article DOI: 10.1098/rsos.181269.][This corrects the article DOI: 10.1098/rsos.181269.].
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OBJECTIVE: To determine whether oxygen (O2) tension (20% vs. 5%) has an impact on oocyte maturation rates and morphology during in vitro maturation (IVM). DESIGN: A prospective, observational, monocentric, sibling-oocyte study. SETTING: University Hospital. PATIENTS: A total of 143 patients who underwent IVM for fertility preservation purposes from November 2016 to April 2021 were analyzed. Patients were included when ≥2 cumulus-oocyte complexes (COCs) were retrieved. The cohort of COCs obtained for each patient was randomly split into two groups: group 20% O2 and group 5% O2. INTERVENTION: Cumulus-oocyte complexes were incubated for 48 hours either under 5% O2 or 20% O2. After 24 and 48 hours of culture, every oocyte was assessed for maturity and morphology, to estimate oocyte quality. Morphology was evaluated considering six parameters (shape, size, ooplasm, perivitelline space, zona pellucida, and polar body characteristics), giving a total oocyte score ranging from -6 to +6. MAIN OUTCOME MEASURES: Maturation rates and total oocyte scores were compared using paired-sample analysis between group 20% O2 and group 5% O2. RESULTS: Patient median age was 31.4 [28.1-35.2] years-old. The mean serum antimüllerian hormone levels and antral follicle count were 3.2 ± 2.3 ng/mL and 27.2 ± 16.0 follicles, respectively. A mean of 10.7 COCs per cycle were retrieved, leading to 6.1 ± 2.4 metaphase II oocytes vitrified (total maturation rate = 57.3%; 991 metaphase II oocytes/1,728 COCs). A total of 864 COCs were included in each group. Oocyte maturation rates were not different between the two groups (group 20% O2: 56.82% vs. group 5% O2: 57.87%, respectively). Regarding oocyte morphology, the mean total oocyte score was significantly higher in group 5% O2 compared with group 20% O2 (3.44 ± 1.26 vs. 3.16 ± 1.32, P=.014). CONCLUSION: As culture under low O2 tension (5% O2) improves oocyte morphology IVM, our results suggest that culture under hypoxia should be standardized. Additional studies are warranted to assess the impact of O2 tension on oocyte maturation and the benefit of IVM under low O2 tension for embryo culture after utilization of frozen material.
Assuntos
Técnicas de Maturação in Vitro de Oócitos , Oócitos , Adulto , Humanos , Oxigênio , Corpos Polares , Estudos Prospectivos , Método Duplo-CegoRESUMO
The combination of meaning-bearing units (e.g., words) into higher-order structures (e.g., compound words and phrases) is integral to human language. Despite this central role of syntax in language, little is known about its evolutionary progression. Comparative data using animal communication systems offer potential insights, but only a handful of species have been identified to combine meaningful calls together into larger signals. We investigated a candidate for syntax-like structure in the highly social chestnut-crowned babbler (Pomatostomus ruficeps). Using a combination of behavioral observations, acoustic analyses, and playback experiments, we test whether the form and function of maternal contact calls is modified by combining the core "piping" elements of such calls with at least one other call element or call. Results from the acoustic analyses (236 analysed calls from 10 individuals) suggested that piping call elements can be flexibly initiated with either "peow" elements from middle-distance contact calls or adult "begging" calls to form "peow-pipe" and "beg-pipe" calls. Behavioral responses to playbacks (20 trials to 7 groups) of natural peow-pipe and beg-pipe calls were comparable to those of artificially generated versions of each call using peow elements and begging calls from other contexts. Furthermore, responses to playbacks (34 trials to 7 groups) of the three forms of maternal contact calls (piping alone, peow-pipe, beg-pipe) differed. Together these data suggest that meaning encoded in piping calls is modified by combining such calls with begging calls or peow elements used in other contexts and so provide rare empirical evidence for syntactic-like structuring in a nonhuman animal.
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Aposematic prey advertise their unprofitability with conspicuous warning signals that are often composed of multiple color patterns. Many species show intraspecific variation in these patterns even though selection is expected to favor invariable warning signals that enhance predator learning. However, if predators acquire avoidance to specific signal components, this might relax selection on other aposematic traits and explain variability. Here, we investigated this idea in the aposematic moth Amata nigriceps that has conspicuous black and orange coloration. The size of the orange spots in the wings is highly variable between individuals, whereas the number and width of orange abdominal stripes remains consistent. We produced artificial moths that varied in the proportion of orange in the wings or the presence of abdominal stripes. We presented these to a natural avian predator, the noisy miner (Manorina melanocephala), and recorded how different warning signal components influenced their attack decisions. When moth models had orange stripes on the abdomen, birds did not discriminate between different wing signals. However, when the stripes on the abdomen were removed, birds chose the model with smaller wing spots. In addition, we found that birds were more likely to attack moths with a smaller number of abdominal stripes. Together, our results suggest that bird predators primarily pay attention to the abdominal stripes of A. nigriceps, and this could relax selection on wing coloration. Our study highlights the importance of considering individual warning signal components if we are to understand how predation shapes selection on prey warning coloration.
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A critical component of language is the ability to recombine sounds into larger structures. Although animals also reuse sound elements across call combinations to generate meaning, examples are generally limited to pairs of distinct elements, even when repertoires contain sufficient sounds to generate hundreds of combinations. This combinatoriality might be constrained by the perceptual-cognitive demands of disambiguating between complex sound sequences that share elements. We test this hypothesis by probing the capacity of chestnut-crowned babblers to process combinations of two versus three distinct acoustic elements. We found babblers responded quicker and for longer toward playbacks of recombined versus familiar bi-element sequences, but no evidence of differential responses toward playbacks of recombined versus familiar tri-element sequences, suggesting a cognitively prohibitive jump in processing demands. We propose that overcoming constraints in the ability to process increasingly complex combinatorial signals was necessary for the productive combinatoriality that is characteristic of language to emerge.
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The evolutionary drivers underlying marked variation in the pigmentation of eggs within many avian species remains unclear. The leading hypotheses proposed to explain such variation advocate the roles of genetic differences, signalling and/or structural integrity. One means of testing among these hypotheses is to capitalize on museum collections of eggs obtained throughout a broad geographical range of a species to ensure sufficient variation in predictors pertaining to each hypothesis. Here, we measured coloration and patterning in eggs from 272 clutches of Australian magpies (Cracticus tibicen) collected across most of their geographical range of ca 7 million km2; encompassing eight subspecies, variation in environmental parameters, and the presence/absence of a brood parasite. We found considerable variation in background colour, as well as in the extent and distribution of patterning across eggs. There was little evidence that this variation was explained by subspecies or the contemporary presence of a brood parasite. However, measures of maximum temperature, leaf area index and soil calcium all contributed to variation in egg appearance, although their explanatory power was relatively low. Our results suggest that multiple factors combine to influence egg appearance in this species, and that even in species with highly variable eggs, coloration is not readily explained.
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The potential for animals to respond to changing climates has sparked interest in intraspecific variation in avian nest structure since this may influence nest microclimate and protect eggs and offspring from inclement weather. However, there have been relatively few large-scale attempts to examine variation in nests or the determinates of individual variation in nest structure within populations. Using a set of mostly pre-registered analyses, we studied potential predictors of variation in the size of a large sample (803) of blue tit (Cyanistes caeruleus) nests across three breeding seasons at Wytham Woods, UK. While our pre-registered analyses found that individual females built very similar nests across years, there was no evidence in follow-up (post hoc) analyses that their nest size correlated to that of their genetic mother or, in a cross-fostering experiment, to the nest where they were reared. In further pre-registered analyses, spatial environmental variability explained nest size variability at relatively broad spatial scales, and especially strongly at the scale of individual nest boxes. Our study indicates that nest structure is a characteristic of individuals, but is not strongly heritable, indicating that it will not respond rapidly to selection. Explaining the within-individual and within-location repeatability we observed requires further study.