Voice categorization in the four-month-old human brain.

Voices are the most relevant social sounds for humans and therefore have crucial adaptive value in development. Neuroimaging studies in adults have demonstrated the existence of regions in the superior temporal sulcus that respond preferentially to voices. Yet, whether voices represent a functionally specific category in the young infant's mind is largely unknown. We developed a highly sensitive paradigm relying on fast periodic auditory stimulation (FPAS) combined with scalp electroencephalography (EEG) to demonstrate that the infant brain implements a reliable preferential response to voices early in life. Twenty-three 4-month-old infants listened to sequences containing non-vocal sounds from different categories presented at 3.33 Hz, with highly heterogeneous vocal sounds appearing every third stimulus (1.11 Hz). We were able to isolate a voice-selective response over temporal regions, and individual voice-selective responses were found in most infants within only a few minutes of stimulation. This selective response was significantly reduced for the same frequency-scrambled sounds, indicating that voice selectivity is not simply driven by the envelope and the spectral content of the sounds. Such a robust selective response to voices as early as 4 months of age suggests that the infant brain is endowed with the ability to rapidly develop a functional selectivity to this socially relevant category of sounds.

Bioacoustic IoT Sensors as Next-Generation Tools for Monitoring: Counting Flying Insects through Buzz.

The global loss of biodiversity is an urgent concern requiring the implementation of effective monitoring. Flying insects, such as pollinators, are vital for ecosystems, and establishing their population dynamics has become essential in conservation biology. Traditional monitoring methods are labour-intensive and show time constraints. In this work, we explore the use of bioacoustic sensors for monitoring flying insects. Data collected at four Italian farms using traditional monitoring methods, such as hand netting and pan traps, and bioacoustic sensors were compared. The results showed a positive correlation between the average number of buzzes per hour and insect abundance measured by traditional methods, primarily by pan traps. Intraday and long-term analysis performed on buzzes revealed temperature-related patterns of insect activity. Passive acoustic monitoring proved to be effective in estimating flying insect abundance, while further development of the algorithm is required to correctly identify insect taxa. Overall, innovative technologies, such as bioacoustic sensors, do not replace the expertise and data quality provided by professionals, but they offer unprecedented opportunities to ease insect monitoring to support conservation biodiversity efforts.

Automatic Brain Categorization of Discrete Auditory Emotion Expressions.

Seamlessly extracting emotional information from voices is crucial for efficient interpersonal communication. However, it remains unclear how the brain categorizes vocal expressions of emotion beyond the processing of their acoustic features. In our study, we developed a new approach combining electroencephalographic recordings (EEG) in humans with a frequency-tagging paradigm to 'tag' automatic neural responses to specific categories of emotion expressions. Participants were presented with a periodic stream of heterogeneous non-verbal emotional vocalizations belonging to five emotion categories: anger, disgust, fear, happiness and sadness at 2.5 Hz (stimuli length of 350 ms with a 50 ms silent gap between stimuli). Importantly, unknown to the participant, a specific emotion category appeared at a target presentation rate of 0.83 Hz that would elicit an additional response in the EEG spectrum only if the brain discriminates the target emotion category from other emotion categories and generalizes across heterogeneous exemplars of the target emotion category. Stimuli were matched across emotion categories for harmonicity-to-noise ratio, spectral center of gravity and pitch. Additionally, participants were presented with a scrambled version of the stimuli with identical spectral content and periodicity but disrupted intelligibility. Both types of sequences had comparable envelopes and early auditory peripheral processing computed via the simulation of the cochlear response. We observed that in addition to the responses at the general presentation frequency (2.5 Hz) in both intact and scrambled sequences, a greater peak in the EEG spectrum at the target emotion presentation rate (0.83 Hz) and its harmonics emerged in the intact sequence in comparison to the scrambled sequence. The greater response at the target frequency in the intact sequence, together with our stimuli matching procedure, suggest that the categorical brain response elicited by a specific emotion is at least partially independent from the low-level acoustic features of the sounds. Moreover, responses at the fearful and happy vocalizations presentation rates elicited different topographies and different temporal dynamics, suggesting that different discrete emotions are represented differently in the brain. Our paradigm revealed the brain's ability to automatically categorize non-verbal vocal emotion expressions objectively (at a predefined frequency of interest), behavior-free, rapidly (in few minutes of recording time) and robustly (with a high signal-to-noise ratio), making it a useful tool to study vocal emotion processing and auditory categorization in general and in populations where behavioral assessments are more challenging.

Recent Advances in Plant-Insect Interactions.

Plant-insect interaction is a fast-developing research field that continues to increase the interest of numerous scientists, many of whom come from heterogeneous backgrounds [...].

The Role of Biogenic Amines in Social Insects: With a Special Focus on Ants.

Eusociality represents the higher degree of interaction in insects. This complex social structure is maintained through a multimodal communication system that allows colony members to be flexible in their responses, fulfilling the overall society's needs. The colony plasticity is supposedly achieved by combining multiple biochemical pathways through the neuromodulation of molecules such as biogenic amines, but the mechanisms through which these regulatory compounds act are far from being fully disentangled. Here, we review the potential function of major bioamines (dopamine, tyramine, serotine, and octopamine) on the behavioral modulation of principal groups of eusocial Hymenoptera, with a special focus on ants. Because functional roles are species- and context-dependent, identifying a direct causal relationship between a biogenic amine variation and behavioral changes is extremely challenging. We also used a quantitative and qualitative synthesis approach to summarize research trends and interests in the literature related to biogenic amines of social insects. Shedding light on the aminergic regulation of behavioral responses will pave the way for an entirely new approach to understanding the evolution of sociality in insects.

The Geomagnetic Field (GMF) Is Necessary for Black Garden Ant (Lasius niger L.) Foraging and Modulates Orientation Potentially through Aminergic Regulation and MagR Expression.

The geomagnetic field (GMF) can affect a wide range of animal behaviors in various habitats, primarily providing orientation cues for homing or migratory events. Foraging patterns, such as those implemented by Lasius niger, are excellent models to delve into the effects of GMF on orientation abilities. In this work, we assessed the role of GMF by comparing the L. niger foraging and orientation performance, brain biogenic amine (BA) contents, and the expression of genes related to the magnetosensory complex and reactive oxygen species (ROS) of workers exposed to near-null magnetic fields (NNMF, ~40 nT) and GMF (~42 µT). NNMF affected workers' orientation by increasing the time needed to find the food source and return to the nest. Moreover, under NNMF conditions, a general drop in BAs, but not melatonin, suggested that the lower foraging performance might be correlated to a decrease in locomotory and chemical perception abilities, potentially driven by dopaminergic and serotoninergic regulations, respectively. The variation in the regulation of genes related to the magnetosensory complex in NNMF shed light on the mechanism of ant GMF perception. Overall, our work provides evidence that the GMF, along with chemical and visual cues, is necessary for the L. niger orientation process.

The Pattern of Social Parasitism in Maculinea teleius Butterfly Is Driven by the Size and Spatial Distribution of the Host Ant Nests.

The parasitic relationship between Maculinea butterflies and Myrmica ants has been extensively studied but little information is available on the spatial occurrence of Maculinea larvae. We searched for the presence of Maculinea teleius in 211 ant nests at two sites in two crucial phases of its life cycle, i.e., in autumn, during the initial larval development, and in the following late spring, before pupation. We assessed variations in the proportion of infested nests and factors correlated with spatial distributions of parasites in Myrmica colonies. The parasitism rate in autumn was very high (∼50% of infestation rate) but decreased in the following spring. The most important factor explaining parasite occurrence in both seasons was the nest size. Further factors, such as the presence of other parasites, the Myrmica species or the site, concurred to explain the differential survival of Ma. teleius until the final development. Irrespective of the host nest distribution, the parasite distribution changed from even in autumn to clumped in late spring. Our work showed that the survival of Ma. teleius is correlated with colony features but also with the nest spatial distribution, which therefore should be taken into consideration in conservation strategies aiming at preserving these endangered species.

Combining environmental niche models, multi-grain analyses, and species traits identifies pervasive effects of land use on butterfly biodiversity across Italy.

Understanding how species respond to human activities is paramount to ecology and conservation science, one outstanding question being how large-scale patterns in land use affect biodiversity. To facilitate answering this question, we propose a novel analytical framework that combines environmental niche models, multi-grain analyses, and species traits. We illustrate the framework capitalizing on the most extensive dataset compiled to date for the butterflies of Italy (106,514 observations for 288 species), assessing how agriculture and urbanization have affected biodiversity of these taxa from landscape to regional scales (3-48 km grains) across the country while accounting for its steep climatic gradients. Multiple lines of evidence suggest pervasive and scale-dependent effects of land use on butterflies in Italy. While land use explained patterns in species richness primarily at grains ≤12 km, idiosyncratic responses in species highlighted "winners" and "losers" across human-dominated regions. Detrimental effects of agriculture and urbanization emerged from landscape (3-km grain) to regional (48-km grain) scales, disproportionally affecting small butterflies and butterflies with a short flight curve. Human activities have therefore reorganized the biogeography of Italian butterflies, filtering out species with poor dispersal capacity and narrow niche breadth not only from local assemblages, but also from regional species pools. These results suggest that global conservation efforts neglecting large-scale patterns in land use risk falling short of their goals, even for taxa typically assumed to persist in small natural areas (e.g., invertebrates). Our study also confirms that consideration of spatial scales will be crucial to implementing effective conservation actions in the Post-2020 Global Biodiversity Framework. In this context, applications of the proposed analytical framework have broad potential to identify which mechanisms underlie biodiversity change at different spatial scales.

Forests influence yeast populations vectored by insects into vineyards.

Introduction: In the vineyard, yeast communities impact the ripening and fermentation of grapes and are influenced by geographical location, climate, and soil characteristics. Despite the great advancement in our knowledge of the vineyard mycobiota, a key step of the process leading to the definition of the vineyard yeast community is still poorly understood: if geography, climate, and soil influence the mycobiota, potentially through selection, where do the yeast originate from, and how can they reach the vineyard? In this perspective, it is currently acknowledged that forests host several yeast species and that insects, particularly social wasps, can vector and maintain the yeasts known to populate the vineyard. Alas, the conveyance, fostered by insects, of yeasts from the forest to the vineyard has not been proven yet. In this study, we aimed to assess the existence of links between a potential natural source of yeasts (woods), the vectors (social wasps), and the composition of the vineyard mycobiota. Methods: For this purpose, the mycobiota of wasps caught in six Italian vineyards were analyzed over 2 years through culturomics approaches. Results: The results clearly indicate that the presence of wooded areas close to vineyards is associated with particular features of the mycobiota vectored by social wasps. Wasps caught in vineyards near wooded areas bear a higher number of yeast cells and higher biodiversity than insects caught in vineyards far from woods. Furthermore, insects caught in vineyards close to woods bear distinctive yeast populations, encompassing species such as Saccharomyces cerevisiae. Discussion: Overall, our work provides fundamental insights into the ecology of the vineyard mycobiota and highlights the need to maintain a vineyard-woodland mosaic landscape, thus preserving the suitable habitat for yeast species relevant to wine-making.

The Inquiline Ant Myrmica karavajevi Uses Both Chemical and Vibroacoustic Deception Mechanisms to Integrate into Its Host Colonies.

Social parasitism represents a particular type of agonistic interaction in which a parasite exploits an entire society instead of a single organism. One fascinating form of social parasitism in ants is the "inquilinism", in which a typically worker-less parasitic queen coexists with the resident queen in the host colony and produces sexual offspring. To bypass the recognition system of host colonies, inquilines have evolved a repertoire of deceiving strategies. We tested the level of integration of the inquiline Myrmica karavajevi within the host colonies of M. scabrinodis and we investigated the mechanisms of chemical and vibroacoustic deception used by the parasite. M. karavajevi is integrated into the ant colony to such an extent that, in rescue experiments, the parasite pupae were saved prior to the host's brood. M. karavajevi gynes perfectly imitated the cuticular hydrocarbon profiles of M. scabrinodis queens and the parasite vibroacoustic signals resembled those emitted by the host queens eliciting the same levels of attention in the host workers during playback experiments. Our results suggest that M. karavajevi has evolved ultimate deception strategies to reach the highest social status in the colony hierarchy, encouraging the use of a combined molecular and behavioural approach when studying host-parasite interactions.

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress.

A growing body of evidence indicates that extracellular fragmented self-DNA (eDNA), by acting as a signaling molecule, triggers inhibitory effects on conspecific plants and functions as a damage-associated molecular pattern (DAMP). To evaluate early and late events in DAMP-dependent responses to eDNA, we extracted, fragmented, and applied the tomato (Solanum lycopersicum) eDNA to tomato leaves. Non-sonicated, intact self-DNA (intact DNA) was used as control. Early event analyses included the evaluation of plasma transmembrane potentials (Vm), cytosolic calcium variations (Ca2+ cy t), the activity and subcellular localization of both voltage-gated and ligand-gated rectified K+ channels, and the reactive oxygen species (ROS) subcellular localization and quantification. Late events included RNA-Seq transcriptomic analysis and qPCR validation of gene expression of tomato leaves exposed to tomato eDNA. Application of eDNA induced a concentration-dependent Vm depolarization which was correlated to an increase in (Ca2+)cyt; this event was associated to the opening of K+ channels, with particular action on ligand-gated rectified K+ channels. Both eDNA-dependent (Ca2+)cyt and K+ increases were correlated to ROS production. In contrast, application of intact DNA produced no effects. The plant response to eDNA was the modulation of the expression of genes involved in plant-biotic interactions including pathogenesis-related proteins (PRPs), calcium-dependent protein kinases (CPK1), heat shock transcription factors (Hsf), heat shock proteins (Hsp), receptor-like kinases (RLKs), and ethylene-responsive factors (ERFs). Several genes involved in calcium signaling, ROS scavenging and ion homeostasis were also modulated by application of eDNA. Shared elements among the transcriptional response to eDNA and to biotic stress indicate that eDNA might be a common DAMP that triggers plant responses to pathogens and herbivores, particularly to those that intensive plant cell disruption or cell death. Our results suggest the intriguing hypothesis that some of the plant reactions to pathogens and herbivores might be due to DNA degradation, especially when associated to the plant cell disruption. Fragmented DNA would then become an important and powerful elicitor able to trigger early and late responses to biotic stress.

Southeast Asian clearwing moths buzz like their model bees.

BACKGROUND: The endless struggle to survive has driven harmless species to evolve elaborate strategies of deceiving predators. Batesian mimicry involves imitations of noxious species' warning signals by palatable mimics. Clearwing moths (Lepidoptera: Sesiidae), incapable of inflicting painful bites or stings, resemble bees or wasps in their morphology and sometimes imitate their behaviours. An entirely unexplored type of deception in sesiids is acoustic mimicry. We recorded the buzzing sounds of two species of Southeast Asian clearwing moths, Heterosphecia pahangensis and H. hyaloptera and compared them to their visual model bee, Tetragonilla collina, and two control species of bees occurring in the same habitat. Recordings were performed on untethered, flying insects in nature. RESULTS: Based on eight acoustic parameters and wingbeat frequencies calculated from slow-motion videos, we found that the buzzes produced by both clearwing moths highly resemble those of T. collina but differ from the two control species of bees. CONCLUSIONS: Acoustic similarities to bees, alongside morphological and behavioural imitations, indicate that clearwing moths display multimodal mimicry of their evolutionary models.

Fast Periodic Auditory Stimulation Reveals a Robust Categorical Response to Voices in the Human Brain.

Voices are arguably among the most relevant sounds in humans' everyday life, and several studies have suggested the existence of voice-selective regions in the human brain. Despite two decades of research, defining the human brain regions supporting voice recognition remains challenging. Moreover, whether neural selectivity to voices is merely driven by acoustic properties specific to human voices (e.g., spectrogram, harmonicity), or whether it also reflects a higher-level categorization response is still under debate. Here, we objectively measured rapid automatic categorization responses to human voices with fast periodic auditory stimulation (FPAS) combined with electroencephalography (EEG). Participants were tested with stimulation sequences containing heterogeneous non-vocal sounds from different categories presented at 4 Hz (i.e., four stimuli/s), with vocal sounds appearing every three stimuli (1.333 Hz). A few minutes of stimulation are sufficient to elicit robust 1.333 Hz voice-selective focal brain responses over superior temporal regions of individual participants. This response is virtually absent for sequences using frequency-scrambled sounds, but is clearly observed when voices are presented among sounds from musical instruments matched for pitch and harmonicity-to-noise ratio (HNR). Overall, our FPAS paradigm demonstrates that the human brain seamlessly categorizes human voices when compared with other sounds including musical instruments' sounds matched for low level acoustic features and that voice-selective responses are at least partially independent from low-level acoustic features, making it a powerful and versatile tool to understand human auditory categorization in general.

Changes in Alpine Butterfly Communities during the Last 40 Years.

Our work aims to assess how butterfly communities in the Italian Maritime Alps changed over the past 40 years, in parallel with altitudinal shifts occurring in plant communities. In 2019, we sampled butterflies at 7 grassland sites, between 1300-1900 m, previously investigated in 2009 and 1978, by semi-quantitative linear transects. Fine-scale temperature and precipitation data elaborated by optimal interpolation techniques were used to quantify climate changes. The changes in the vegetation cover and main habitat alterations were assessed by inspection of aerial photographs (1978-2018/1978-2006-2015). The vegetation structure showed a marked decrease of grassland habitats and an increase of woods (1978-2009). Plant physiognomy has remained stable in recent years (2009-2019) with some local exceptions due to geomorphic disturbance. We observed butterfly 'species substitution' indicating a general loss in the more specialised and a general gain in more tolerant elements. We did not observe any decrease in species richness, but rather a change in guild compositions, with (i) an overall increased abundance in some widespread and common lowland species and (ii) the disappearance (or strong decrease) of some alpine (high elevation) species, so that 'resilience' could be just delusive. Changes in butterfly community composition were consistent with predicted impacts of local warming.

Stabilisation of some names of European butterflies (Lepidoptera: Pieridae) in their prevailing usage.

To stabilise nomenclature in its prevailing usage, the authors designate three lectotypes, respectively for the nominal taxa Pontia daplidice race nitida Verity, 1908 (Museo di Storia naturale della Università di Firenze, sezione di Zoologia, 'La Specola' MZUF), for Euchloe crameri Butler, 1869 (Natural History Museum UK, NHMUK) and for Euchloe ausonia var. esperi Kirby, 1871 (National Museum of Ireland, NMI). They also designate two neotypes, respectively for [Papilio] ausonia Hübner, [1804] (MZUF) and for Pontia simplonia Freyer, 1829 (Jura Museum, Eichstätt, JME).

The Microbiome of the Maculinea-Myrmica Host-Parasite Interaction.

Maculinea (=Phengaris) are endangered butterflies that are characterized by a very complex biological cycle. Maculinea larvae behave as obligate parasites whose survival is strictly dependent on both particular food plants and species-specific Myrmica ants. In this interaction, Maculinea caterpillars induce Myrmica workers to retrieve and rear them in the nest by chemical and acoustic deception. Social insect symbiotic microorganisms play a key role in intraspecific and interspecific communication; therefore, it is possible that the Maculinea caterpillar microbiome might be involved in the chemical cross-talk by producing deceptive semiochemicals for host ants. To address this point, the microbiota of Maculinea alcon at different larval stages (phytophagous early larvae, intermediate larvae, carnivorous late larvae) was analyzed by using 16S rRNA-guided metabarcoding approach and compared to that of the host ant Myrmica scabrinodis. Structural and deduced functional profiles of the microbial communities were recorded, which were used to identify specific groups of microorganisms that may be involved in the chemical cross-talk. One of the most notable features was the presence in all larval stages and in the ants of two bacteria, Serratia marcescens and S. entomophila, which are involved in the chemical cross-talk between the microbes and their hosts.

Patterns of host use by brood parasitic Maculinea butterflies across Europe.

The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Host specificity pattern and chemical deception in a social parasite of ants.

In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide.

Correction: Origanum vulgare terpenoids modulate Myrmica scabrinodis brain biogenic amines and ant behaviour.

[This corrects the article DOI: 10.1371/journal.pone.0209047.].

Chemical, Physiological and Molecular Responses of Host Plants to Lepidopteran Egg-Laying.

Plant-lepidopteran interactions involve complex processes encompassing molecules and regulators to counteract defense responses they develop against each other. Lepidoptera identify plants for oviposition and exploit them as larval food sources to complete their development. In turn, plants adopt different strategies to overcome and limit herbivorous damages. The insect egg deposition on leaves can already induce a number of defense responses in several plant species. This minireview deals with the main features involved in the interaction between plants and lepidopteran egg-laying, focusing on responses from both insect and plant side. We discuss different aspects of direct and indirect plant responses triggered by lepidopteran oviposition. In particular, we focus our attention on the mechanisms underlying egg-induced plant defenses that can i) directly damage the eggs such as localized hypersensitive response (HR)-like necrosis, neoplasm formation, production of ovicidal compounds and ii) indirect defenses, such as production of oviposition-induced plant volatiles (OIPVs) used to attract natural enemies (parasitoids) able to kill the eggs or hatching larvae. We provide an overview of chemical, physiological, and molecular egg-mediated plant responses induced by both specialist and generalist lepidopteran species, also dealing with effectors, elicitors, and chemical signals involved in the process. Egg-associated microorganisms are also discussed, although little is known about this third partner participating in plant-lepidopteran interactions.