26/10: Nest architecture and collective building in social insects

PROGRAMME (London time, pm)

ABSTRACTS:

Nest building in leaf-cutting ants: information use and regulatory feedback loops involved in the control of nest climate

Flavio Roces

Department of Behavioral Physiology and Sociobiology, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany.

roces@biozentrum.uni-wuerzburg.de

Leaf-cutting ants build the largest and most complex nests among ants, which may include up to five million workers and up to 8000 chambers containing fungus gardens. Workers need to provide the fungus gardens not only with appropriate plants, but also with sufficient space and suitable microclimate to allow their growth. Since workers have no overview of the whole nest and only use local information for its construction, it is unclear what information workers use to organize collective nest building, and how local this information actually is. To answer these questions, we focused on the influence of nest architectural features on climate control at both mechanistic and functional levels. At the mechanistic level, we explored the use of environmental and social information for the construction of nest turrets that promote air exchanges. At the functional level, we comparatively characterized architectural features such as nest depth, spatial arrangement of nest chambers, and their connectivity to the outside, and explored their influence on climate control in an evolutionary framework. It will be argued that leaf-cutting ants as a group represent a tractable system to investigate the behavioral mechanisms underlying collective building, as well as the consequences of nest design for colony fitness.

Behavioral mechanism and its evolutionary history of termite tunnel excavation

Nobuaki Mizumoto

Evolutionary Genomics Unit, Okinawa Institute of Science and Technology Graduate University (OIST)

The structures built by social insects are group-level patterns that emerge from interactions among individuals following simple behavioral rules. Because of the complex relationship between variation in collective patterns and individual behaviors, it is essential to know how actual behavior evolves to change pattern formation. I have studied the interspecific variation of termite tunneling at both collective and individual levels. First, I show that two species share the same behavioral repertoire but its regulation results in tunnels with distinct branching patterns. Second, two species that evolved tunneling independently produce similar branching patterns with distinct behavior. Thus, there are cryptic interspecific variations in their collective excavation process. By expanding the comparative study across termite phylogeny, I will overview the origin and evolution of tunneling behaviors in termites.

Nest architecture and its relevance to nest choice during colony relocation in a tropical ant Diacamma indicum.

Sumana Annagiri

Indian Institute of Science Education and Research Kolkata

Nests impact the survival and fitness of organisms as they not only provide protection from harsh abiotic features, predators and parasites they also provide a platform for the care of the next generation and the organization of tasks involved in their care. Using the model organism Diacamma indicum, a ponerine ant that lives mostly in subterrain nests together with a small number of colony members in the Indian subcontinent, we wanted to understand the importance of nests. In this presentation we will start by delineating the architectural design of nests in their natural habitat across different seasons using aluminium and wax casts. In the next step we will probe the design adaptations to prevent nest flooding during monsoons. Finally, we will examine the importance of different architectural features like entrance tunnel, chamber volume in the selection of new nest during colony relocation using controlled choice tests within the lab. Together this will give us an overview of the challenges that these organisms face and how they overcome them in context of their dwelling.

Collective construction: Adjustment of underground foraging tunnels in leaf-cutting ants

Sheethal Vepur Ramamurthy, Flavio Roces

Friedrich Schiller University Jena, University of Würzburg

Leaf cutting ants build underground nest chambers connected to each other through various tunnels, and also connecting outside the nest – to foraging areas. Mechanisms like self-organization through local interactions and stigmeric communication explain the emergence of global structures. However, most studies have focused on nest chamber construction as a whole, whereas very few studies have looked into emergence of tunnels and the related feedback mechanisms. The aim of our study was to investigate how do leaf-cutting ants assess space within a tunnel. We investigated by presenting a two-dimenional digging arena with a tunnel whose width varied between 1 cm (narrow) and 4 cm (wide), along the entire length of the tunnel. The rationale is that there would be high congestion among individuals due to narrow tunnel as compared to wider parts of the tunnel, which would lead to an initial low traffic flow. The high encounter rate among individuals would therefore lead to widening only narrow parts of the tunnel through digging such that the tunnel widens over time, causing traffic flow and speed of the individuals traversing the tunnel to fall back to normalcy. We empirically found that traffic flow was low initially, increased gradually as the tunnel widened and remained constant. We also found a significant positive correlation between traffic flow and width of the tunnel. Finally, the overall tunnel width remained to be regulated over time such that it did not widen more than needed. These results suggest that there are positive and negative feedbacks at play which controls the overall tunnel width that emerges over time. We also speculate that encounter rate acts as a mechanism for the amplification and regulation of tunnel width.

Nest construction by Australian weaver ant

Michal Roitman, Ehud Fonio and Ofer Feinerman

The department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel

While most ant species construct soil nests, some species are very different. Arboreal weaver ants group and weave together leaves into hollow structures in which they then reside. In the process of nest construction the ants start by gathering on a localized group of leaves, then they connect to each in chain-like structures that link and bend the leaves into location. Finally, adult ants hold silk producing larvae to glue the leaves together. This magnificent process is highly general: the ants transform a huge variety of tree leaves with different size, shape, stiffness, number and density into viable nests. Yet, little is known about how the ants achieve this robustness or about the architecture plan and how the ants collectively execute it. To address these questions we constructed a novel 3D imaging system that captures the process of nest construction in the lab which will be described in this talk. We aim to use the resulting measurements to uncover patterns in the ants' self-organzied patterns, the dynamics of leaf motion, and the structure and mechanical properties of the complete nest. We expect our work could further our understanding of biological emergence and hope to introduce weaver ant nest construction as a model system for collective cognition.

Number of nest entrances and collective foraging in ants

Detrain Claire, Lehue Marine, Collignon Bertrand

Service d’écologie Sociale. Université Libre de Bruxelles. Avenue F Roosevelt 50, 1050 Brussels, Belgium

The main entrance of the ant nest is the key location at which information about resources is shared  between recruiting foragers and inner workers. Additional nest entrances, which increase the number of sites where recruitment takes place,  make the synchronization of foraging activity more difficult to achieve,  lead to signals  becoming locally weaker and impede the emergence of collective responses. By comparing one-entrance and two-entrance nests of the red ant  Myrmica rubra, we found that an additional nest entrance segregated the pool of recruiters, hampered the formation of a collective foraging trail and decreased  the ants’ ability to discriminate between two food sources of different sucrose concentration (1M and 0.1M). Ultimately, multiple nest entrances could reduce the foraging efficiency of ant colonies that consumed significantly less sugar out of the two available resources. This study opens new insights on how the physical interface between the nest interior and the outside environment can act upon the foraging efficiency of these self-organized ant societies and can impede the ant’s ability to process information about environmental opportunities in order to select the most rewarding resources.

Nest architectures of myrmecophilous stingless bees, Trigona cfr. clipes and Paratrigona sp., from Peruvian Amazon

M. Marconi, A. Modesti, C. D. Vecco Giove, E. Mancini, A. Di Giulio

Department of Science, Roma Tre University, Viale Guglielmo Marconi, 446, 00146 Rome, Italy, e-mail:

marilena.marconi@uniroma3.it; andrea.digiulio@uniroma3.it

Department of Biology and Biotechnology "Charles Darwin”, Sapienza University of Rome, Viale dell'Universit., 32,

00185 Rome, Italy, e-mail: modesti.1712957@studenti.uniroma1.it; emiliano.mancini@uniroma1.it

National University of San Martín, Jr. Maynas, 177, 22200 Tarapoto, Peru, e-mail: cdvecco@unsm.edu.pe

Stingless bees (Hymenoptera: Meliponini) are corbiculate and eusocial bees, including over 500 species distributed in the tropical and sub-tropical regions of the world. They establish perennial colonies using a large variety of nesting sites, as well as colonies of ants, wasps and termites. In these associations, the nests present complex architectures and the relationships between the colonies of social insects ranging from the sole exploitation of ant nest cavities to parasitism and parabiotic interactions. Compared to termitophily, myrmecophily is an uncommon feature and little studied aspect among Meliponini. In Peru there are few records relating to these types of associations, and in general little is known about the architecture of the nests of bees and ants that live together. For the first time, the nest architecture of Trigona cfr. clipes in association with Dolichoderus quadridenticulatus is described from the Peruvian Amazon. The record of another association, Paratrigona sp.-Camponotus sp. is also reported. As the nests are arranged, the types of building materials used and a morphometric analysis of the nests of ants and bees are also provided.

Is an ant mound a fortress for some fungi?
Mucoromycota community of the Formica polyctena nest

Kochanowski Michał¹*, Siedlecki Igor¹ , Wrzosek Marta¹

⁽¹⁾Botanic Garden, Faculty of Biology, University of Warsaw, Al. Ujazdowskie 4, 00−478 Warsaw, Poland

author's e-mail address to correspondence: mj.kochanowski@student.uw.edu.pl

Mounds of red wood ants are unique microenvironments. They are composed mostly of organic matter (mainly coniferous needles) and are rich in antifungal substances (resin and formic acid). Such specific properties create a niche which could be beneficial only for some fungi present in temperate forests. Recent publications link Entomortierella and Umbelopsis with the red wood ant’s environment^1,2.In our study we wanted to determine the species of Mucoromycota characteristic for mounds of Formica polyctena ants. In order to do that we collected samples twice, in pine forests in Poland. Samples were collected from the surface and inside of two F. polyctena mounds, together with surrounding forest litter as a control sample. In our study, a culture-based method was employed with morphological identification for most analyzed taxa and molecular identification (ITS) for Mortierellacae representatives. Our results show that Entomortierella and the ‘Absidia cylindrospora’ group are the indicator taxa for the mound environment. Interestingly, representatives of those fungal taxa have been previously isolated from ants or nest material^2,3,4, which suggests their adaptation to an ant-made environment. Additionally, representatives of common saprotrophs belonging to Mucor and Rhizopus were rarely isolated from the mound microenvironment.

Bibliography:

Ants Reign over a Distinct Microbiome in Forest Soil. Lindström, S.; Timonen, S.; Sundström, L.; Johansson, H. Soil Biol. Biochem. 2019, 139, 107529

Fungi Associated with the Infrabuccal Pockets of Camponotus Pennsylvanicus and Other Formicine Ants. Clark, D.W., 2003, ISBN 0-612-73803-5.

Chance or Necessity—The Fungi Co−Occurring with Formica polyctena Ants, Siedlecki I., Gorczak M.,  Okrasińska A., Wrzosek M., Insects 2021, 12(3), 204

Biodiversity of Fungi in Red Imported Fire Ant (Hymenoptera: Formicidae) Mounds. Zettler, J.;  McInnis T.; Allen, C.; Spira, T. Annals of the Entomological Society of America, Volume 95, Issue 4, 2002, Pages 487–491

Ventilation and drainage in termite nests: a micro-scale study combining X-ray imaging with 3D flow field simulations

Kamaljit Singh¹, Bagus, P. Muljadi², Ali Q. Raeini³, Veerle Vandeginste², Martin J. Blunt³, Christian Jost⁴, Guy Theraulaz⁴, and Pierre Degond⁵

¹ Institute of GeoEnergy Engineering, Heriot-Watt University, EH14 4AS, Edinburgh, U.K.

² Department of Chemical and Environmental Engineering, The University of Nottingham, NG7 2RD, Nottingham, U.K.

³ Department of Earth Science and Engineering, Imperial College London, SW7 2AZ, London, U.K.

⁴ Centre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, CNRS, Université Paul Sabatier, F-31062 Toulouse, Cedex 9, France

⁵ Institut de Mathématiques de Toulouse, CNRS, Université Paul Sabatier, F-31062 Toulouse, Cedex 9, France

Termite nests have been widely studied for thermoregulation and ventilation. Their architecture maintains a stable temperature throughout the year and permits self-sustainable CO₂ exchange with the atmosphere for ventilation. These self-sustaining properties have been a key motivation for designing eco-friendly buildings. In this study, we investigate the CO₂ exchange and water drainage properties of Trinervitermes geminatus termite nests by analyzing the three-dimensional micro-structure of nest walls using X-ray micro-tomography and performing 3D flow field simulations. We show that the microscale structure of nest walls contains both small and large pores. The 3D network of interconnected larger pores provides enhanced ventilation through advective and diffusive CO₂ exchange. The larger pores and the resultant higher porosity in the nest walls also help to reduce the thermal conductivity and temperature exchange between the atmospheric and internal air, therefore providing enhanced thermal insulation to the inner parts of the nest. Moreover, we show that the interconnected microscale larger pores allow rapid drainage of rainwater, which is useful for re-establishing CO₂ exchange after rainy periods. Overall, our study reveals unidentified micro-structural properties of the nest walls, and their role in controlling ventilation, water drainage and thermal exchange. Future work could focus on similar analyses of the porous walls of other non-fungus and fungus-growing termite nests.

Old and new buildings: what collective building rules help mitigate the effect of individual mutations on architectural quality?

Presenter’s name: Edith Invernizzi

Co-authors: Takao Sasaki (University of Georgia), Théo Michelot (University of St Andrews)

Institution: University of St Andrews (Scotland)

Email: edith.invernizzi@outlook.com

Twitter: @invernie

I will start my talk by introducing a new finding in the behavioural model of Temnothorax albipennis wall building, first developed by Franks et al. (1992). Using a combination of agent-based modelling and laboratory data, I show that the stigmergic response of workers to stones guides both wall expansion and termination. The interaction between ants and deposited stones has a mechanical component, but is also guided either by recognition of wall conformation or by the change in other environmental factors that are affected by stone distribution (e.g., air currents). After this premise, I will present the results of an evolutionary simulation study. I used the model to explore wall robustness to inter-worker variation in distance-template perception, which causes workers to preferentially build at different distances. Through an agent-based simulation, I looked at the impact of three types of inter-worker variation on wall quality: I. normally distributed individual phenotypes (corresponding to epigenetic differences or to a combination of epigenetic and genetic effects underlying worker behaviour); II. co-existence of four distinct parental lines (i.e., either matrilines or patrilines), each expressing a parental-line specific phenotype and with or without parental-line specific spatial specialisation in building activity; III. gradual substitution of the workforce that causes the progressive introduction of a new phenotype (e.g., following queen replacement). I find that this collective architecture is predicted to be robust to most types of inter-worker variation. Stigmergy and overlap among the template distributions generated by different variants are necessary mechanisms leading to the convergence of otherwise divergent phenotypes. This enables colonies in which very different building phenotypes are expressed to still produce a functional architecture. Importantly, these findings suggest that beneficial mutations can be expressed in a mixed context before reaching colony-level expression without diminishing colony fitness returns.

Surface curvature guides early construction activity in mound-building termites

Daniel S. Calovi, Nicole Carey, Paul Bardunias, Scott Turner, Radhika Nagpal and Justin Werfel

Termites are able to construct complex meter-high mounds, which are able to passively regulate atmospheric conditions while at the same time protecting the colony from predators. To construct these mounds, millions of independent decentralized workers organise themselves in ways we are still not able to fully grasp and that is orders of magnitude larger when put in comparison to human engineering. In order to elucidate the principles involved in this coordination we have performed experiments at a field site in Namibia using Macrotermes michaelseni, where we investigated the role of different cues that trigger and influence termite construction. While it has been hypothesized that a cement pheromone would be responsible for this construction behaviour, our previous results indicate that construction is greatly influenced by previous digging activity, local soil geometry and humidity. In this talk I will present the results on how surface curvature is a strong predictor of where construction activity occurs. These results led to new experimental designs aimed to reduce the influence of the arena local topography on our following study measuring the role of humidity in termite construction.

A model driven by curvature reproduces geometric features of arboreal termite nests.

Giulio Facchini, Alexandre Lazarescu, Andrea Perna, Stéphane Douady

Termites are known to collectively build complex and intricate nests from self-organised collective behaviour. Here we aim at finding minimal organizing principles of nest morphogenesis, focusing in particular on the arboreal nests of Nasutitermes. Inspired by field observations we design a simple three-dimensional model to describe the autonomous expansion of a substrate which grows driven by the local mean curvature of its surface. Our hypothesis is that termite coordination is mediated by the shape of the structure they are walking on, i.e. focusing the building activity of termites where local mean curvature is high. We adopt a phase-field model where the nest is described by one continuous scalar field and its growth can be described with a single non-linear equation with one adjustable parameter d. When d is large enough the equation is linearly unstable and fairly reproduces a growth process where the initial walls expand, branch and merge, while progressively invading all the available space, which is consistent with the intricate structures of real nests. We validate our model by collecting nests of two species of arboreal Nasutitermes from the field and imaging their structure with a micro-CT scanner. We find a strong resemblance between real and simulated nests, characterised by the emergence of a characteristic length-scale and by the abundance of saddle-shaped surfaces with zero-mean curvature which validates the choice of the driving mechanism of our growth model. An analogous curvature distribution was observed in spinodal materials and proved to confer important mechanical properties as graceful failure under compression which may protect the nest core in the case of extreme weather events. While other physical and biochemical cues are likely involved in guiding termite construction, our study highlights the importance of local curvature as a powerful geometric cue to organise termite activity, and an important ingredient determining the mechanical properties of nests.

Honeycomb base structure results from an optimum balance of effort from dual sided construction

Vince Gallo and Lars Chittka

Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

Honeycomb, the wax fabrication by Apis melifera, is a double-sided sheet of tessellated, near-horizontal hexagonal cells that share a common base. Honeycomb is beautiful, but not perfect, and much is revealed by irregularities that result from construction errors, structural adaptations, or purposeful distortion. Our work has focused on irregularities of the trihedral pyramid that forms the base of each cell. We offered the bees three different forms of wax foundation. One where access was possible from only one side, a second that was overly thick preventing interaction between the working of both faces and thirdly foundation with stimuli to cause cells to be formed directly opposite each other. Sequential non-destructive measurement of the base profile has allowed us to show that the bases of individual cells, worked from one side only, are begun with a curved base, and remains thus while access is restricted. Once the conditions permit for access to workers from both sides then the typical faceted bases are formed. For opposing cells, the bases are atypical forming a single face orthogonal to the cell walls.  Our results show that the normal flat faces of honeycomb walls are produced through a balance of construction effort.

Effect of temperature on nest digging activity and nest morphology in the yellow meadow ant Lasius flavus

Alann Rathery, Giulio Facchini, Lewis Halsey & Andrea Perna

Roehampton University, Holybourne Avenue, London, UK

Ants are ectothermic individuals and cannot regulate their own body temperature, so the regulation process are done through behavioural processes. Nests of ants are defined as extended phenotypes as they can play a role on the behaviour of the colony members. However, nests are dependent on the environmental factors such as humidity or temperature. For this reason, changes in environmental temperature are likely to have a major impact on colony activity. Here, we studied the nest digging activity of yellow-meadow ants Lasius flavus, constrained to dig in a 2-dimensional setup in laboratory conditions under controlled temperature conditions. Warmer temperatures induced a faster digging rate, consistent with the typical increase of activity of ectotherms with increasing temperature. A morphological characterisation of the shape of nests excavated at different temperature conditions revealed that some parameters of nest shape were also affected by temperature. We discuss these effects in terms of mechanisms of nest-digging behaviour, and in terms of the possible adaptative value of different nest shapes.

Modularity and connectivity of nest structure scale with colony size

Julie Miller, Sean O’Fallon, Emma Wan, Noa Pinter-Wollman

Department of Ecology and Evolutionary Biology, University of California – Los Angeles

Large body sizes have evolved structures to facilitate resource transport. Like unitary organisms, social insect colonies must transport information and resources, and larger colonies may experience transport challenges similar to large-bodied organisms. In ant colonies, transport is constrained by the nest, but the nest may also facilitate movement. We examine three structural attributes of nests that could mitigate transport challenges related to colony size: (1) subdivision - nests of species with large colonies are more subdivided to reduce crowd viscosity; (2) branching - nest tunnels increase branching in species with large colonies to reduce travel distances; and (3) short-cuts – nests of species with large colonies have cross-linking tunnels to connect distant parts of the nest and create alternative routes. We test these hypotheses by comparing nest structures of species with different colony sizes in phylogenetically controlled meta-analyses. Our findings support the subdivision and branching hypotheses. The nests of species with large colonies contain more, but not larger, chambers and reduce travel distances by increasing branching frequency. Increased subdivision and branching of transportation networks are also characteristic of how unitary organisms change with increasing body size, suggesting these structural features provide common solutions to the transport challenges created by large size across levels of biological organization.