The role of climatic variables on nest evolution in tanagers.

Avian nests are fundamental structures in avian reproduction and face strong selective forces. Climatic conditions are likely to have shaped the evolution of specific nest traits, but evidence is scarce at a macroevolutionary level. The Thraupidae family (commonly known as tanagers) is an ideal clade to understand the link between nest architecture and climate because it presents wide variation in nest traits. To understand whether climatic variables have played a role in the diversification of nest traits among species in this family, we measured nests from 49 species using museum collections. We observed that dome-nesting species are present in dryer and hotter environments, in line with previous findings suggesting that domed nests are a specialisation for arid conditions. We also found evidence that nests with thicker walls are present in locations with lower precipitation and that solar radiation can influence the shape of domed nests; birds tend to build shorter and narrower domes in areas with high levels of solar radiation. Open nest architecture is also potentially influenced by wind speed, with longer and deeper nests in areas characterised by strong winds. Our results support the hypothesis that different climatic variables can drive the evolution of specific aspects of nest architecture and contribute to the diversity of nest shapes we currently observe. However, climatic variables account only for a small fraction of the observed structural variation, leaving a significant portion still unexplained.

The inheritance of alternative nest architectural traditions in stingless bees.

The transmission of complex behavior and culture in humans has long been attributed to advanced forms of social learning,1,2 which play a crucial role in our technological advancement.3 While similar phenomena of behavioral traditions and cultural inheritance have been observed in animals,1,2,4,5,6 including in primates,7 whales,8 birds,9 and even insects,10 the underlying mechanisms enabling the persistence of such animal traditions, particularly in insects, are less well understood. This study introduces pioneering evidence of enduring architectural traditions in the stingless bee Scaptotrigona depilis, which are maintained without any evidence for social learning. We demonstrate that S. depilis exhibits two distinct nest architectures, comprising either helicoidal or flat, stacked horizontal combs, which are transmitted across generations through stigmergy11,12,13,14,15,16,17-an environmental feedback mechanism whereby the presence of the existing comb structures guides subsequent construction behaviors-thereby leading to a form of environmental inheritance.18,19,20 Cross-fostering experiments further show that genetic factors or prior experience does not drive the observed variation in nest architecture. Moreover, the experimental introduction of corkscrew dislocations within the combs prompted helicoidal building, confirming the use of stigmergic building rules. At a theoretical level, we establish that the long-term equilibrium of building in the helicoidal pattern fits with the expectations of a two-state Markov chain model. Overall, our findings provide compelling evidence for the persistence of behavioral traditions in an insect, based on a simple mechanism of environmental inheritance and stigmergic interactions, without requiring any sophisticated learning mechanism, thereby expanding our understanding of how traditions can be maintained in non-human species.

Experimental evidence that increased surface temperature affects bioturbation by ants.

Ants are important bioturbators that actively produce biopores and move soil particles. They could be particularly affected by global warming as they are ectotherms. Nevertheless, they can indirectly regulate their temperature, through changes in their circadian cycles and the architecture of their nests (e.g. digging deep nests or using insulating materials). Nest architecture has been considered an expanded functional trait of ant colonies and thus sensitive to environmental changes such as increasing temperatures. This work aimed to study the nest architecture of ants as a functional trait and its effects on soil bioturbation. We hypothesized that, when exposed to increased surface temperatures, ants would increase their excavation activities, build deeper nests and alter the layout of chambers to maintain their preferred temperature and humidity, thus enhancing soil porosity. We allowed 17 young Lasius niger ant colonies to excavate nests in soil columns exposed to three surface temperatures (mild, n = 5; medium, n = 6; and high, n = 6) for 100 days. We measured the amount of soil excavated weekly and took X-ray scans of the soil column on Days 7, 14, 28, and 88 to characterize the three-dimensional structure of the nests (depth, shape, volume of chambers and tunnels). We then collected the colonies and measured their growth during the experiment, and the size and weight of workers. Ants reacted to surface temperature. Colonies exposed to medium and high temperatures excavated larger and deeper nests than those exposed to mild temperature. Nests excavated under high and medium temperatures had the same maximal depth, but chambers were located deeper in the former, which were further characterized by the refiling of some of the upper chambers. Colonies grew well in all treatments, although less under mild temperature. They produced normal-sized workers despite differences in surface temperature. Overall, these results suggest that ants exposed to higher temperatures live in deeper chambers. This study shows that surface temperature affects ant nest architecture, confirming its status as extended phenotype and highlighting its flexibility over time, which has in turn consequences on soil porosity.

The evolution of nest site use and nest architecture in modern birds and their ancestors.

The evolution of nest site use and nest architecture in the non-avian ancestors of birds remains poorly understood because nest structures do not preserve well as fossils. Nevertheless, the evidence suggests that the earliest dinosaurs probably buried eggs below ground and covered them with soil so that heat from the substrate fuelled embryo development, while some later dinosaurs laid partially exposed clutches where adults incubated them and protected them from predators and parasites. The nests of euornithine birds-the precursors to modern birds-were probably partially open and the neornithine birds-or modern birds-were probably the first to build fully exposed nests. The shift towards smaller, open cup nests has been accompanied by shifts in reproductive traits, with female birds having one functioning ovary in contrast to the two ovaries of crocodilians and many non-avian dinosaurs. The evolutionary trend among extant birds and their ancestors has been toward the evolution of greater cognitive abilities to construct in a wider diversity of sites and providing more care for significantly fewer, increasingly altricial, offspring. The highly derived passerines reflect this pattern with many species building small, architecturally complex nests in open sites and investing significant care into altricial young. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Foraging behaviour affects nest architecture in a cross-species comparison of ant nests.

Animals construct and inhabit nests that can exhibit dramatic intra- and interspecific variation due to differences in behaviour, the biotic and abiotic environment, and evolutionary history. In ants, variation in nest architecture reflects both differences in ecology and in the collective behaviour of the colonies that live in the nests. Each component of the nest (such as depth, and the number, size and connectivity of chambers) reflects selective pressures for different functions, or structural constraints that are imposed by the environment or evolutionary history. To determine potential drivers of nest structure variation in subterranean nests, we performed a meta-analysis of measures of published ant nests to compare different structural elements within and across species. We complemented this survey with 42 nest casts of two closely related species. We quantified nest features that can potentially impact ant foraging behaviour and examined whether phylogeny or foraging strategy are better explanatory variables for the variation we observed. We found that foraging strategy better explained nest features than evolutionary history. Our work reveals the importance of ecology in shaping nest structure and provides an important foundation for future investigations into the selective pressures that have shaped ant nest architecture. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Evolution of nest architecture in tyrant flycatchers and allies.

Innovations in nest design are thought to be one potential factor in the evolutionary success of passerine birds (order: Passeriformes), which colonized new ecological niches as they diversified in the Oligocene and Miocene. In particular, tyrant flycatchers and their allies (parvorder: Tyrannida) are an extremely diverse group of New World suboscine passerines occupying a wide range of habitats and exhibiting substantial extant variation in nest design. To explore the evolution of nest architecture in this clade, we first described nest traits across the Tyrannida phylogeny and estimated ancestral nest conditions. We then quantified macroevolutionary transition rates between nest types, examined a potential coevolutionary relationship between nest type and habitat, and used phylogenetic mixed models to determine possible ecological and environmental correlates of nest design. The Tyrannida ancestor probably built a cup nest in a closed habitat, and dome nests independently evolved at least 15 times within this group. Both cup- and dome-nesting species diversified into semi-open and open habitats, and we did not detect a coevolutionary relationship between nest type and habitat. Furthermore, nest type was not significantly correlated with several key ecological, life-history and environmental traits, suggesting that broad variation in Tyrannida nest architecture may not easily be explained by a single factor. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Passive heat diffusion in nests with downward-facing cells: Implications for early colony development in social wasps.

Social insects employ a variety of active and passive mechanisms for nest thermoregulation. Many social wasp species exhibit a particular nest-architecture by building their nests with cells facing downward. By using thermal imaging to characterize the heat diffusion throughout Oriental hornet nests from different angular positions, we show that the heat diffusion along the vertical gradient of nests is more efficient when the cell openings face downward than when facing sideways or upward, demonstrating the efficiency of this specific architecture in increasing the nest temperature. This passive thermoregulation mechanism could be especially important during the initial stage of the colony, when the queen is alone to rear her first brood. Among the social insects that build cells to raise their brood, we suggest that wasps can take advantage of the thermal benefits of this particular architecture of their cells as, unlike bees, they do not usually store food in them.

Manipulating nest architecture reveals three-dimensional building strategies and colony resilience in honeybees.

Form follows function throughout the development of an organism. This principle should apply beyond the organism to the nests they build, but empirical studies are lacking. Honeybees provide a uniquely suited system to study nest form and function throughout development because we can image the three-dimensional structure repeatedly and non-destructively. Here, we tracked nest-wide comb growth in six colonies over 45 days (control colonies) and found that colonies have a stereotypical process of development that maintains a spheroid nest shape. To experimentally test if nest structure is important for colony function, we shuffled the nests of an additional six colonies, weekly rearranging the comb positions and orientations (shuffled colonies). Surprisingly, we found no differences between control and shuffled colonies in multiple colony performance metrics-worker population, comb area, hive weight and nest temperature. However, using predictive modelling to examine how workers allocate comb to expand their nests, we show that shuffled colonies compensate for these disruptions by accounting for the three-dimensional structure to reconnect their nest. This suggests that nest architecture is more flexible than previously thought, and that superorganisms have mechanisms to compensate for drastic architectural perturbations and maintain colony function.

Harvester ant nest architecture is more strongly affected by intrinsic than extrinsic factors.

Behavior is shaped by genes, environment, and evolutionary history in different ways. Nest architecture is an extended phenotype that results from the interaction between the behavior of animals and their environment. Nests built by ants are extended phenotypes that differ in structure among species and among colonies within a species, but the source of these differences remains an open question. To investigate the impact of colony identity (genetics), evolutionary history (species), and the environment on nest architecture, we compared how two species of harvester ants, Pogonomyrmex californicus and Veromessor andrei, construct their nests under different environmental conditions. For each species, we allowed workers from four colonies to excavate nests in environments that differed in temperature and humidity for seven days. We then created casts of each nest to compare nest structures among colonies, between species, and across environmental conditions. We found differences in nest structure among colonies of the same species and between species. Interestingly, however, environmental conditions did not have a strong influence on nest structure in either species. Our results suggest that extended phenotypes are shaped more strongly by internal factors, such as genes and evolutionary history, and are less plastic in response to the abiotic environment, like many physical and physiological phenotypes.

Climate Change Influences Basidiome Emergence of Leaf-Cutting Ant Cultivars.

Maintaining symbiosis homeostasis is essential for mutualistic partners. Leaf-cutting ants evolved a long-term symbiotic mutualism with fungal cultivars for nourishment while using vertical asexual transmission across generations. Despite the ants' efforts to suppress fungal sexual reproduction, scattered occurrences of cultivar basidiomes have been reported. Here, we review the literature for basidiome occurrences and associated climate data. We hypothesized that more basidiome events could be expected in scenarios with an increase in temperature and precipitation. Our field observations and climate data analyses indeed suggest that Acromyrmex coronatus colonies are prone to basidiome occurrences in warmer and wetter seasons. Even though our study partly depended on historical records, occurrences have increased, correlating with climate change. A nest architecture with low (or even the lack of) insulation might be the cause of this phenomenon. The nature of basidiome occurrences in the A. coronatus-fungus mutualism can be useful to elucidate how resilient mutualistic symbioses are in light of climate change scenarios.

Evolution of eggshell structure in relation to nesting ecology in non-avian reptiles.

Amniotic eggs are multifunctional structures that enabled early tetrapods to colonize the land millions of years ago, and are now the reproductive mode of over 70% of all terrestrial amniotes. Eggshell morphology is at the core of animal survival, mediating the interactions between embryos and their environment, and has evolved into a massive diversity of forms and functions in modern reptiles. These functions are critical to embryonic survival and may serve as models for new antimicrobial and/or breathable membranes. However, we still lack critical data on the basic structural and functional properties of eggs, particularly of reptiles. Here, we first characterized egg shape, shell thickness, porosity, and mineralization of eggs from 91 reptile species using optical images, scanning electron microscopy, and micro computed tomography, and collected data on nesting ecology from the literature. We then used comparative analyses to test hypotheses on the selective pressures driving their evolution. We hypothesized that eggshell morphology has evolved to protect shells from physical damage and desiccation, and, in support, found a positive relationship between thickness and precipitation, and a negative relationship between porosity and temperature. Although mineralization varied extensively, it was not correlated with nesting ecology variables. Ancestral state reconstructions show thinning and increased porosity over evolutionary time in squamates, but the opposite in turtles and crocodilians. Egg shape, size, porosity and calcification were correlated, suggesting potential structural or developmental tradeoffs. This study provides new data and insights into the morphology and evolution of reptile eggs, and raises numerous questions for additional research.

A 3D model to illustrate the nest architecture of Acromyrmex balzani (Hymenoptera; Formicidae)

ABSTRACT For eusocial insects, the nest is a place where the main social interactions occur. The nest architecture ensures protection from predators and the environment, as well as suitable conditions for brood rearing, food storage, and in some cases the cultivation of fungus farms. Variations in nest architecture can occur, according to the environmental conditions. In order to elucidate the internal organization of nests, most studies use 2D schemes and photographs to illustrate the nest architecture models. However, 3D models can provide a different and more realistic view of the nest architecture. The aim of this study was to describe the nest architecture and colony size of the grass-cutting ant Acromyrmex balzani (Emery), using 3D models to illustrate these features. The structures of eight colonies were measured and the data were used to create a 3D model of each nest. Externally, the nests had one or more piles of loose soil and waste, with a single straw turret over the entrance. Underground, the nests had from 2 to 6 chambers, at a maximum depth of 122 cm. It could be concluded that the observed nest architecture of Acromyrmex balzani followed, at least in part, the pattern already reported in the literature. However, this is the first report of connection between two chambers made by two shafts, as well as the presence of the turret at the nest entrance/exit, regardless of the season of the year. These differences evidence that the nest structures may vary, depending on intrinsic or local environmental conditions.

Marasmioid rhizomorphs in bird nests: Species diversity, functional specificity, and new species from the tropics.

In tropical and subtropical rainforests, vegetative fungal rhizomorphs from the Marasmiineae are routinely used as construction material in bird nests. Because rhizomorphs seldom produce mushrooms within nests, the fungal species involved remain largely unknown. In turn, this limitation has prevented us from resolving broader questions such as whether specific fungal species are selected by birds for different functional roles (i.e., attachment, or parasite control). To fill some of these gaps, we collected 74 rhizomorph-containing bird nests from the Neo- and Afrotropics and used nuc rDNA internal transcribed spacer ITS1-5.8S-ITS2 (ITS) sequences to discriminate between rhizomorph-forming species. In total we recovered 25 Marasmiineae species used by birds in nest construction, none of which were shared between the Neotropics and the Afrotropics. We also collected Marasmiineae basidiomes in the vicinity of nests and used ITS sequences to match these sporulating morphs with nest rhizomorphs for nine species. Basidiomes from an additional five species were found fruiting from rhizomorphs incorporated within bird nests. Finally, an additional six species were putatively identified based on publicly available sequence data. Rhizomorphs of five species were found to be utilized almost exclusively as lining material in nests. Lining material comes in direct contact with nestlings and is hypothesized to play a role in parasite control. Rhizomorphs from 10 species were used to attach and anchor nests to substrates; we matched six of those to fruiting litter trap-forming species collected in the understory. Litter traps hold large quantities of fallen litter material, suggesting that birds may preferentially use rhizomorphs that are adapted to bearing heavy loads for nest attachment. Finally, we describe two species of Marasmius-M. neocrinis-equi, sp. nov., and M. nidus-avis, sp. nov.-that are commonly found associated with bird nests and show that rhizomorph production is common across the genus.

Flexible Piezoresistive Sensors with Wide-Range Pressure Measurements Based on a Graded Nest-like Architecture.

Flexible pressure sensors present great potential in the application of human health monitoring, tactile function of prosthesis, and electronic skin for robotics. These applications require different trade-off between the sensitivity and sensing range, therefore, it is imperative to develop range-specific sensitivities in a single sensor. In this paper, a bioinspired strategy for a resistive pressure sensor using a graded porous material is proposed to measure pressures from several pascals to megapascals. Its fabrication is based on an easily accessible template method. The nest-architecture-based wide-range pressure sensor exhibits adequate sensitivity under an extensive pressure regime (20 Pa to 1.2 MPa). In addition, with rational structural design and subtle engineering of the material properties, the sensor achieves remarkable mechanical stability. To prove the concept, sensors were attached on a bicycle wheel to monitor the tire-pavement pressure and on human skin to detect biosignals such as venous and arterial blood pressure pulses.

Nest Entrances, Spatial Fidelity, and Foraging Patterns in the Red Ant Myrmica rubra: A Field and Theoretical Study.

The nest architecture of social insects deeply impacts the spatial distribution of nestmates their interactions, information exchanges and collective responses. In particular, the number of nest entrances can influence the interactions taking place beyond the nest boundaries and the emergence of collective structures like foraging trails. Here, we investigated in the field how the number of nest entrances impacted the foraging dynamics of Myrmica rubra ant colonies. We located the nest entrances where recruitment occurred towards sugar feeders placed in their surroundings. The nests showed one or multiple entrance(s) aggregated in clusters spaced by at least 15 cm. Foragers from colonies with two clusters of entrances were distributed more homogeneously among the feeders than those of colonies with one cluster. In addition, foragers always returned to the first discovered feeder and demonstrated a high fidelity to their original entrance. Finally, a multi-agent model highlighted that additional entrances and clusters of entrances delayed the mobilisation of workers but favoured the simultaneous exploitation of several sources, which was further enhanced by the spatial fidelity of foragers. Multiple nest entrances seem to be a way for medium-sized colonies to benefit from advantages conferred by polydomy while avoiding associated costs to maintain social cohesion.

Nest Architecture Development of Grass-Cutting Ants, Atta capiguara (Hymenoptera: Formicidae)

ABSTRACT Atta capiguara grass-cutting ants are commonly found in the Cerrado biome, in open fields. Although grass-cutting ants build giant nests, little has been elucidated about this building pattern and when chambers and tunnels emerge. The present study describes the nest architecture development of A. capiguara grass-cutting ants from data on 31 cement-molded nests. A. capiguara nests grow with increases in the number of fungus chambers and emergence and increase of waste chambers and foraging tunnels. The structural growth of A. capiguara nests in the first year and a half of age (18 months) is vertical, with the building of the first chambers in the soil profile. After 18 months, the nests grow sideways with the addition of chambers and tunnels, and the first waste chambers appear. Between 18 and 54 months, the number of fungus chambers increases from 1-3 to 21-32, and the chambers are concentrated at the soil surface, although they can be found more than 3 m deep. In addition, the total volume of the waste chambers increases with the increment in the fungus chambers volume. Thus, this study contributes to understanding the nest architecture development of A. capiguara grass-cutting ants and demonstrates that the total volume of waste chambers is proportional to the total volume of fungus chambers suitable for the colony.

Gall-Colonizing Ants and Their Role as Plant Defenders: From 'Bad Job' to 'Useful Service'.

Galls are neoformed structures on host plant tissues caused by the attack of insects or other organisms. They support different communities of specialized parasitic insects (the gall inducers), and can also provide refuge to other insects, such as moths, beetles and ants, referred to as secondary occupants. This study focuses on galls induced by the oak gall wasp Andricus quercustozae and secondarily colonized by ants in a mixed oak forest. A field survey and two experiments were carried out to a) study ant (species-specific) preferences for different features of the galls, b) describe differences in gall architecture due to ant activity, c) analyse the effects of the presence of gall-dwelling ants on plant health. The results show that there are differences between ant species in gall colonization and in the alteration of gall opening and inner structure. We verified that gall-dwelling ants protect their host plants efficiently, offering them an indirect defence mechanism against enemies (predators and pathogens). The data suggest a new paradigm in ant-plant relationships mediated by the presence of galls on the plants whose ecological and evolutionary implications are discussed.

The non-additive effects of body size on nest architecture in a polymorphic ant.

Like traditional organisms, eusocial insect societies express traits that are the target of natural selection. Variation at the colony level emerges from the combined attributes of thousands of workers and may yield characteristics not predicted from individual phenotypes. By manipulating the ratios of worker types, the basis of complex, colony-level traits can be reduced to the additive and non-additive interactions of their component parts. In this study, we investigated the independent and synergistic effects of body size on nest architecture in a seasonally polymorphic harvester ant, Veromessor pergandei Using network analysis, we compared wax casts of nests, and found that mixed-size groups built longer nests, excavated more sand and produced greater architectural complexity than single-sized worker groups. The nests built by polymorphic groups were not only larger in absolute terms, but larger than expected based on the combined contributions of both size classes in isolation. In effect, the interactions of different worker types yielded a colony-level trait that was not predicted from the sum of its parts. In nature, V. pergandei colonies with fewer fathers produce smaller workers each summer, and produce more workers annually. Because body size is linked to multiple colony-level traits, our findings demonstrate how selection acting on one characteristic, like mating frequency, could also shape unrelated characteristics, like nest architecture.This article is part of the theme issue 'Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour'.

Exploring nest structures of acorn dwelling ants with X-ray microtomography and surface-based three-dimensional visibility graph analysis.

The physical spaces within which organisms live affect their biology and in many cases can be considered part of their extended phenotype. The nests of social insect societies have a fundamental impact on their ability to function as complex superorganisms. Ants in many species excavate elaborate subterranean nests, but others inhabit relatively small pre-formed cavities within rock crevices and hollow seeds. Temnothorax ants, which often nest within acorns, have become a model system for studying collective decision making. While these ants have demonstrated remarkable degrees of rationality and consistent precision with regard to their nest choices, never before has the fine scale internal architecture and spatial organization of their nests been investigated. We used X-ray microtomography to record high-resolution three-dimensional (3D) scans of Temnothorax colonies within their acorns. These data were then quantified using image segmentation and surface-based 3D visibility graph analysis, a new computational methodology for analysing spatial structures. The visibility graph analysis method integrates knowledge from the field of architecture with the empirical study of animal-built structures, thus providing the first methodological cross-disciplinary synergy of these two research areas. We found a surprisingly high surface area and degree of spatial heterogeneity within the acorn nests. Specific regions, such as those associated with the locations of queens and brood, were significantly more conducive to connectivity than others. From an architect's point of view, spatial analysis research has never focused on all-surface 3D movement, as we describe within ant nests. Therefore, we believe our approach will provide new methods for understanding both human design and the comparative biology of habitat spaces.This article is part of the theme issue 'Interdisciplinary approaches for uncovering the impacts of architecture on collective behaviour'.

Notes on the nest of the social wasp Pseudopolybia langi (Hym., Vespidae, Polistinae)

Abstract Detailed descriptions of the architecture of Pseudopolybia langi nests are presented for the first time. Structural variations in the arrangements of nest parts are described and compared with features observed in other species of Pseudopolybia and other epiponine genera.