Divergent ecological responses to typhoon disturbance revealed via landscape-scale acoustic monitoring.

Climate change is increasing the frequency, intensity, and duration of extreme weather events across the globe. Understanding the capacity for ecological communities to withstand and recover from such events is critical. Typhoons are extreme weather events that are expected to broadly homogenize ecological dynamics through structural damage to vegetation and longer-term effects of salinization. Given their unpredictable nature, monitoring ecological responses to typhoons is challenging, particularly for mobile animals such as birds. Here, we report spatially variable ecological responses to typhoons across terrestrial landscapes. Using a high temporal resolution passive acoustic monitoring network across 24 sites on the subtropical island of Okinawa, Japan, we found that typhoons elicit divergent ecological responses among Okinawa's diverse terrestrial habitats, as indicated by increased spatial variability of biological sound production (biophony) and individual species detections. This suggests that soniferous communities are capable of a diversity of different responses to typhoons. That is, spatial insurance effects among local ecological communities provide resilience to typhoons at the landscape scale. Even though site-level typhoon impacts on soundscapes and bird detections were not particularly strong, monitoring at scale with high temporal resolution across a broad spatial extent nevertheless enabled detection of spatial heterogeneity in typhoon responses. Further, species-level responses mirrored those of acoustic indices, underscoring the utility of such indices for revealing insight into fundamental questions concerning disturbance and stability. Our findings demonstrate the significant potential of landscape-scale acoustic sensor networks to capture the understudied ecological impacts of unpredictable extreme weather events.

Targeted treatment of injured nestmates with antimicrobial compounds in an ant society.

Infected wounds pose a major mortality risk in animals. Injuries are common in the ant Megaponera analis, which raids pugnacious prey. Here we show that M. analis can determine when wounds are infected and treat them accordingly. By applying a variety of antimicrobial compounds and proteins secreted from the metapleural gland to infected wounds, workers reduce the mortality of infected individuals by 90%. Chemical analyses showed that wound infection is associated with specific changes in the cuticular hydrocarbon profile, thereby likely allowing nestmates to diagnose the infection state of injured individuals and apply the appropriate antimicrobial treatment. This study demonstrates that M. analis ant societies use antimicrobial compounds produced in the metapleural glands to treat infected wounds and reduce nestmate mortality.

Breakdown in seasonal dynamics of subtropical ant communities with land-cover change.

Concerns about widespread human-induced declines in insect populations are mounting, yet little is known about how land-use change modifies both the trends and variability of insect communities, particularly in understudied regions. Here, we examine how the seasonal activity patterns of ants-key drivers of terrestrial ecosystem functioning-vary with anthropogenic land-cover change on a subtropical island landscape, and whether differences in temperature or species composition can explain observed patterns. Using trap captures sampled biweekly over 2 years from a biodiversity monitoring network covering Okinawa Island, Japan, we processed 1.2 million individuals and reconstructed activity patterns within and across habitat types. Forest communities exhibited greater temporal variability of activity than those in more developed areas. Using time-series decomposition to deconstruct this pattern, we found that sites with greater human development exhibited ant communities with diminished seasonality, reduced synchrony and higher stochasticity compared with sites with greater forest cover. Our results cannot be explained by variation in regional or site temperature patterns, or by differences in species richness or composition among sites. Our study raises the possibility that disruptions to natural seasonal patterns of functionally key insect communities may comprise an important and underappreciated consequence of global environmental change that must be better understood across Earth's biomes.

The feeding apparatus of ants: an overview of structure and function.

Ants are a dominant family of eusocial terrestrial insects with a diversity of ecologies, lifestyles and morphologies. Ant diet preferences range from strict carnivory through omnivory to almost complete herbivory in species feeding on seeds or exudates of plant-sucking insects. While several studies have investigated ant feeding performance on different substrates, comparatively little is known about the functional morphology of the structures involved in food uptake or their diversification across the ants. To take stock of our current knowledge, we give an overview of how adult ants ingest food, followed by a morphological description of the mouthparts, preoral space and cephalic sucking pump. The mandibles are the most prominent mouthparts and have received considerable attention in the literature, so we focus on the maxillae and labium here. We present current hypotheses for the movement patterns of these parts and discuss morphological differences among ants that may be related to their ecological diversity. Finally, we give short comparisons of the ant condition with some other insects and vertebrates, as well as an outlook summarizing gaps in our knowledge. This sets the stage for future studies elucidating the connections between ant feeding mechanisms and mouthpart evolution. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Generalized mutualisms promote range expansion in both plant and ant partners.

Mutualism improves organismal fitness, but strong dependence on another species can also limit a species' ability to thrive in a new range if its partner is absent. We assembled a large, global dataset on mutualistic traits and species ranges to investigate how multiple plant-animal and plant-microbe mutualisms affect the spread of legumes and ants to novel ranges. We found that generalized mutualisms increase the likelihood that a species establishes and thrives beyond its native range, whereas specialized mutualisms either do not affect or reduce non-native spread. This pattern held in both legumes and ants, indicating that specificity between mutualistic partners is a key determinant of ecological success in a new habitat. Our global analysis shows that mutualism plays an important, if often overlooked, role in plant and insect invasions.

Behavioural individuality determines infection risk in clonal ant colonies.

In social groups, infection risk is not distributed evenly across individuals. Individual behaviour is a key source of variation in infection risk, yet its effects are difficult to separate from other factors (e.g., age). Here, we combine epidemiological experiments with chemical, transcriptomic, and automated behavioural analyses in clonal ant colonies, where behavioural individuality emerges among identical workers. We find that: (1) Caenorhabditis-related nematodes parasitise ant heads and affect their survival and physiology, (2) differences in infection emerge from behavioural variation alone, and reflect spatially-organised division of labour, (3) infections affect colony social organisation by causing infected workers to stay in the nest. By disproportionately infecting some workers and shifting their spatial distribution, infections reduce division of labour and increase spatial overlap between hosts, which should facilitate parasite transmission. Thus, division of labour, a defining feature of societies, not only shapes infection risk and distribution but is also modulated by parasites.

Global determinants of insect mitochondrial genetic diversity.

Understanding global patterns of genetic diversity is essential for describing, monitoring, and preserving life on Earth. To date, efforts to map macrogenetic patterns have been restricted to vertebrates, which comprise only a small fraction of Earth's biodiversity. Here, we construct a global map of predicted insect mitochondrial genetic diversity from cytochrome c oxidase subunit 1 sequences, derived from open data. We calculate the mitochondrial genetic diversity mean and genetic diversity evenness of insect assemblages across the globe, identify their environmental correlates, and make predictions of mitochondrial genetic diversity levels in unsampled areas based on environmental data. Using a large single-locus genetic dataset of over 2 million globally distributed and georeferenced mtDNA sequences, we find that mitochondrial genetic diversity evenness follows a quadratic latitudinal gradient peaking in the subtropics. Both mitochondrial genetic diversity mean and evenness positively correlate with seasonally hot temperatures, as well as climate stability since the last glacial maximum. Our models explain 27.9% and 24.0% of the observed variation in mitochondrial genetic diversity mean and evenness in insects, respectively, making an important step towards understanding global biodiversity patterns in the most diverse animal taxon.

Evidence of a thoracic crop in workers, soldiers, and queens of Carebara perpusilla ants (Formicidae: Myrmicinae).

The ability to share and store food is paramount in group-living animals, allowing a finely tuned distribution of resources over time and individuals and an enhanced survival over periods of food scarcity. Ants have several ways to store food: one of them is their gastral crop, also known as a "social stomach." Nutrients in the crop can be regurgitated to nestmates through oral trophallaxis (mouth-to-mouth) or proceed to the midgut by opening the proventriculus, a valve connecting the crop to the midgut. However, some ants are also known to have a so-called "thoracic crop," an extension of the esophagus that allows for additional storage space. In this study, we provide the first evidence of a thoracic crop in the genus Carebara, in reproductive (queen) and sterile (soldier and worker) castes. We discuss how the ant body plan allowed for the evolution of a novel food storage structure in the mesothorax.

Morphology of the metapleural gland and its associated novel atrial cone gland in Strumigenys ants.

The metapleural gland is a unique feature of the ant phenotype, but diversity in its anatomy and function across the ants is not well documented or understood. We studied the morphology of the metapleural gland in 20 mainly Oriental Strumigenys species using histology, scanning and transmission electron microscopy, and micro-CT. The gland is formed by a cluster of class-3 cells, their secretion is transported through a bundle of ducts into the sclerotized atrium and is guided along a series of parallel cuticular ridges towards the atrial opening. Among the examined species, queens have more gland cells than conspecific workers, while the examined males do not have the gland. The social parasite S. mutica has the most developed metapleural gland. In addition, we describe a novel class-1 atrial cone gland which is associated with the metapleural gland. The epithelium of this cone gland forms an invagination into the ventral atrium of the metapleural gland. The cuticular cone may be lacking in some Afrotropical and Neotropical species, although these may still contain the epithelial gland. The functional and evolutionary drivers of morphological variation in the exocrine system across species form interesting questions for future work.

The impact of land use on non-native species incidence and number in local assemblages worldwide.

While the regional distribution of non-native species is increasingly well documented for some taxa, global analyses of non-native species in local assemblages are still missing. Here, we use a worldwide collection of assemblages from five taxa - ants, birds, mammals, spiders and vascular plants - to assess whether the incidence, frequency and proportions of naturalised non-native species depend on type and intensity of land use. In plants, assemblages of primary vegetation are least invaded. In the other taxa, primary vegetation is among the least invaded land-use types, but one or several other types have equally low levels of occurrence, frequency and proportions of non-native species. High land use intensity is associated with higher non-native incidence and frequency in primary vegetation, while intensity effects are inconsistent for other land-use types. These findings highlight the potential dual role of unused primary vegetation in preserving native biodiversity and in conferring resistance against biological invasions.

The global spread and invasion capacities of alien ants.

Many alien species are neither cultivated nor traded but spread unintentionally, and their global movements, capacities to invade ecosystems, and susceptibility to detection by biosecurity measures are poorly known.1,2,3,4 We addressed these key knowledge gaps for ants, a ubiquitous group of stowaway and contaminant organisms that include some of the world's most damaging invasive species.5,6,7,8,9,10 We assembled a dataset of over 146,000 occurrence records to comprehensively map the human-mediated spread of 520 alien ant species across 525 regions globally. From descriptions of the environments in which species were collected within individual regions-such as in imported cargoes, buildings, and outdoor settings-we determined whether different barriers to invasion had been overcome11 and classified alien ant species under three levels of invasion capacity corresponding to increasing biosecurity threat. We found that alien species of different invasion capacities had different sources and sinks globally. For instance, although the diversity of indoor-confined species peaked in the Palearctic realm, that of species able to establish outdoors peaked in the Nearctic and Oceanian realms, and these mainly originated from the Neotropical and Oriental realms. We also found that border interceptions worldwide missed two-thirds of alien species with naturalization capacity, many associated with litter and soil. Our study documents the vast spread of alien ants globally while highlighting avenues for more targeted biosecurity responses, such as prioritizing the screening of imports from regions that are diversity hotspots for species of high invasion capacity and improving the detection of cryptic alien invertebrates dwelling in substrates.

Richness and resilience in the Pacific: DNA metabarcoding enables parallelized evaluation of biogeographic patterns.

Islands make up a large proportion of Earth's biodiversity, yet are also some of the most sensitive systems to environmental perturbation. Biogeographic theory predicts that geologic age, area, and isolation typically drive islands' diversity patterns, and thus potentially impact non-native spread and community homogenization across island systems. One limitation in testing such predictions has been the difficulty of performing comprehensive inventories of island biotas and distinguishing native from introduced taxa. Here, we use DNA metabarcoding and statistical modelling as a high throughput method to survey community-wide arthropod richness, the proportion of native and non-native species, and the incursion of non-natives into primary habitats on three archipelagos in the Pacific - the Ryukyus, the Marianas and Hawaii - which vary in age, isolation and area. Diversity patterns largely match expectations based on island biogeography theory, with the oldest and most geographically connected archipelago, the Ryukyus, showing the highest taxonomic richness and lowest proportion of introduced species. Moreover, we find evidence that forest habitats are more resilient to incursions of non-natives in the Ryukyus than in the less taxonomically rich archipelagos. Surprisingly, we do not find evidence for biotic homogenization across these three archipelagos: the assemblage of non-native species on each island is highly distinct. Our study demonstrates the potential of DNA metabarcoding to facilitate rapid estimation of biogeographic patterns, the spread of non-native species, and the resilience of ecosystems.

Collective and harmonized high throughput barcoding of insular arthropod biodiversity: Toward a Genomic Observatories Network for islands.

Current understanding of ecological and evolutionary processes underlying island biodiversity is heavily shaped by empirical data from plants and birds, although arthropods comprise the overwhelming majority of known animal species, and as such can provide key insights into processes governing biodiversity. Novel high throughput sequencing (HTS) approaches are now emerging as powerful tools to overcome limitations in the availability of arthropod biodiversity data, and hence provide insights into these processes. Here, we explored how these tools might be most effectively exploited for comprehensive and comparable inventory and monitoring of insular arthropod biodiversity. We first reviewed the strengths, limitations and potential synergies among existing approaches of high throughput barcode sequencing. We considered how this could be complemented with deep learning approaches applied to image analysis to study arthropod biodiversity. We then explored how these approaches could be implemented within the framework of an island Genomic Observatories Network (iGON) for the advancement of fundamental and applied understanding of island biodiversity. To this end, we identified seven island biology themes at the interface of ecology, evolution and conservation biology, within which collective and harmonized efforts in HTS arthropod inventory could yield significant advances in island biodiversity research.

GABI-I: The global ant biodiversity informatics-island database.

Island systems are known to harbor disproportionate amounts of geographically restricted biodiversity and to experience high rates of species loss, and they ultimately represent critical systems with significant conservation values. However, knowledge of the biodiversity value of insular systems remains highly fragmented and incomplete for many groups of organisms, especially insects. This gap limits our understanding of their global significance for biodiversity and inhibits prioritization for future exploration and conservation efforts. Here, we developed a new database to present current knowledge on ants on 2678 islands globally, based on nominal species, and provide information on their native or exotic status. In total, this database contains 7010 ant species (44.6% of the known global ant fauna) that have been recorded on islands globally from 449,232 records. In addition, this database identifies 108 large islands (area > 200 km2 ) that have received no ant sampling efforts globally. This new data set provides the most comprehensive understanding of ant diversity and composition on islands globally, opening up new opportunities to address questions on a multitude of research questions and fields related to biogeography, ecology, and evolution. This data set also provides a roadmap for future exploration and conservation actions in connection with ants on islands as well as overall ant diversity, with updates available as new records and taxonomic updates are published. There are no copyright restrictions on this database and users should cite this data paper in publications when using the data.

Periodic Environmental Disturbance Drives Repeated Ecomorphological Diversification in an Adaptive Radiation of Antarctic Fishes.

AbstractThe ecological theory of adaptive radiation has profoundly shaped our conceptualization of the rules that govern diversification. However, while many radiations follow classic early-burst patterns of diversification as they fill ecological space, the longer-term fates of these radiations depend on many factors, such as climatic stability. In systems with periodic disturbances, species-rich clades can contain nested adaptive radiations of subclades with their own distinct diversification histories, and how adaptive radiation theory applies in these cases is less clear. Here, we investigated patterns of ecological and phenotypic diversification within two iterative adaptive radiations of cryonotothenioid fishes in Antarctica's Southern Ocean: crocodile icefishes and notoperches. For both clades, we observe evidence of repeated diversification into disparate regions of trait space between closely related taxa and into overlapping regions of trait space between distantly related taxa. We additionally find little evidence that patterns of ecological divergence are correlated with evolution of morphological disparity, suggesting that these axes of divergence may not be tightly linked. Finally, we reveal evidence of repeated convergence in sympatry that suggests niche complementarity. These findings reflect the dynamic history of Antarctic marine habitats and may guide hypotheses of diversification dynamics in environments characterized by periodic disturbance.

Updating the taxonomy of the ant genus Myrmecina (Hymenoptera, Formicidae) in China with descriptions of three new species.

In this study, we present a taxonomic update for the ant genus Myrmecina in China that includes 14 species in total. A recent survey of the leaf litter ant fauna in Chinas Hengduan Mountains collected three unknown Myrmecina species, which we describe here as Myrmecina eowilsoni sp. nov., M. gaoligongensis sp. nov., and Myrmecina pierceae sp. nov. These new species are clearly distinguishable from all the other species in the genus. We provide an update to the identification key of Chinese Myrmecina, as well as a diagnostic discussion and high-quality specimen images. In addition, Myrmecina raviwonghei Jaitrong, Samung, Waengsothorn Okido 2019 is reported for the first time from China.

The global distribution of known and undiscovered ant biodiversity.

Invertebrates constitute the majority of animal species and are critical for ecosystem functioning and services. Nonetheless, global invertebrate biodiversity patterns and their congruences with vertebrates remain largely unknown. We resolve the first high-resolution (~20-km) global diversity map for a major invertebrate clade, ants, using biodiversity informatics, range modeling, and machine learning to synthesize existing knowledge and predict the distribution of undiscovered diversity. We find that ants and different vertebrate groups have distinct features in their patterns of richness and rarity, underscoring the need to consider a diversity of taxa in conservation. However, despite their phylogenetic and physiological divergence, ant distributions are not highly anomalous relative to variation among vertebrate clades. Furthermore, our models predict that rarity centers largely overlap (78%), suggesting that general forces shape endemism patterns across taxa. This raises confidence that conservation of areas important for small-ranged vertebrates will benefit invertebrates while providing a "treasure map" to guide future discovery.

Toward global integration of biodiversity big data: a harmonized metabarcode data generation module for terrestrial arthropods.

Metazoan metabarcoding is emerging as an essential strategy for inventorying biodiversity, with diverse projects currently generating massive quantities of community-level data. The potential for integrating across such data sets offers new opportunities to better understand biodiversity and how it might respond to global change. However, large-scale syntheses may be compromised if metabarcoding workflows differ from each other. There are ongoing efforts to improve standardization for the reporting of inventory data. However, harmonization at the stage of generating metabarcode data has yet to be addressed. A modular framework for harmonized data generation offers a pathway to navigate the complex structure of terrestrial metazoan biodiversity. Here, through our collective expertise as practitioners, method developers, and researchers leading metabarcoding initiatives to inventory terrestrial biodiversity, we seek to initiate a harmonized framework for metabarcode data generation, with a terrestrial arthropod module. We develop an initial set of submodules covering the 5 main steps of metabarcode data generation: (i) sample acquisition; (ii) sample processing; (iii) DNA extraction; (iv) polymerase chain reaction amplification, library preparation, and sequencing; and (v) DNA sequence and metadata deposition, providing a backbone for a terrestrial arthropod module. To achieve this, we (i) identified key points for harmonization, (ii) reviewed the current state of the art, and (iii) distilled existing knowledge within submodules, thus promoting best practice by providing guidelines and recommendations to reduce the universe of methodological options. We advocate the adoption and further development of the terrestrial arthropod module. We further encourage the development of modules for other biodiversity fractions as an essential step toward large-scale biodiversity synthesis through harmonization.

Minute workers and large soldiers in the subterranean ant Carebara perpusilla: Musculoskeletal consequences of Haller's rule in the thorax.

Many organismal traits vary with body size, often reflecting trade-offs in the face of size-dependent constraints. For example, Haller's rule, the allometric pattern whereby smaller organisms have proportionally larger brains, can have carry-on effects on head design as the brain competes for space with other structures. Ant species with polymorphic worker castes are interesting cases for helping us understand these allometric effects. Here, we examine the effects of miniaturization on the ant power core, the mesosoma (thorax), with particular attention to how the scaling of nervous system structures affects the skeletomuscular elements involved with load bearing and locomotion. Using X-ray computed microtomography (microCT), we studied the thorax of Carebara perpusilla, an African ant species that has minute workers (1.5 mm-long) and larger soldiers (3.0 mm-long), allowing strong intraspecific comparisons. We find that the thoracic nervous system is relatively larger in minute workers, similar to Haller's rule, with consequences on the skeletomuscular organisation. Minute workers have relatively smaller petiole muscles and indirect head muscles, but relatively larger external trochanter muscles and direct head muscles. We link these allometric trade-offs to miniaturization and division of labor, and discuss how thorax design underlies the success of minute ants.

Patterns of morphological simplification and innovation in the megadiverse Holometabola (Insecta).

We analyzed patterns of complexity and simplicity in holometabolan insects using parsimony and maximum-likelihood. By contrast with other groups of arthropods (and most other groups of animals), insects have undergone a stepwise process of structural simplification in their evolution. The megadiverse Holometabola are characterized mainly by structurally simplified larvae, which differ strongly from the adults in their morphology and usually also in their life habits. Although smaller groups such as Neuropterida have largely maintained their structural complexity in adults and immature life stages, a series of reductions occurred with the appearance and diversification of Coleopterida, Mecopterida and especially Antliophora. Parasitic Strepsiptera or fleas display conspicuous patterns of reduction in different life stages and body regions, and high degrees of simplification also occur in groups with short-lived adults. Larvae living in moist substrates display far-reaching structural simplifications and also morphological uniformity, especially in the species-rich Diptera, but also in other groups. Liquid feeding leads to correlated simplifications and innovation of adult head structures, especially of the mouthparts. Functional or anatomical dipterism leads to an optimization of the flight apparatus in most holometabolous groups, which is correlated with reductions in one of the pterothoracic segments, and coupled (e.g. by hamuli), partly reduced or transformed wings (e.g. halteres). In flightless groups, the pterothoracic skeleto-muscular apparatus is strongly simplified. In the abdomen of adult females a stepwise reduction of the lepismatoid ovipositor occurs. By contrast, the male genital apparatus often undergoes an extreme diversification. Our evaluations revealed a highly correlated complexity between larval and adult stages.