Artificial flowers as a tool for investigating multimodal flower choice in wild insects.

Flowers come in a variety of colours, shapes, sizes and odours. Flowers also differ in the quality and quantity of nutritional reward they provide to entice potential pollinators to visit. Given this diversity, generalist flower-visiting insects face the considerable challenge of deciding which flowers to feed on and which to ignore. Working with real flowers poses logistical challenges due to correlations between flower traits, maintenance costs and uncontrolled variables. Here, we overcome this challenge by designing multimodal artificial flowers that varied in visual, olfactory and reward attributes. We used artificial flowers to investigate the impact of seven floral attributes (three visual cues, two olfactory cues and two rewarding attributes) on flower visitation and species richness. We investigated how flower attributes influenced two phases of the decision-making process: the decision to land on a flower, and the decision to feed on a flower. Artificial flowers attracted 890 individual insects representing 15 morphospecies spanning seven arthropod orders. Honeybees were the most common visitors accounting for 46% of visitors. Higher visitation rates were driven by the presence of nectar, the presence of linalool, flower shape and flower colour and was negatively impacted by the presence of citral. Species richness was driven by the presence of nectar, the presence of linalool and flower colour. For hymenopterans, the probability of landing on the artificial flowers was influenced by the presence of nectar or pollen, shape and the presence of citral and/or linalool. The probability of feeding increased when flowers contained nectar. For dipterans, the probability of landing on artificial flowers increased when the flower was yellow and contained linalool. The probability of feeding increased when flowers contained pollen, nectar and linalool. Our results demonstrate the multi-attribute nature of flower preferences and highlight the usefulness of artificial flowers as tools for studying flower visitation in wild insects.

To eat, or not to eat: a phantom decoy affects information-gathering behavior by a free-ranging mammalian herbivore.

When foraging, making appropriate food choices is crucial to an animal's fitness. Classic foraging ecology theories assume animals choose food of greatest benefit based on their absolute value across multiple dimensions. Consequently, poorer options are considered irrelevant alternatives that should not influence decision-making among better options. But heuristic studies demonstrate that irrelevant alternatives (termed decoys) can influence the decisions of some animals, indicating they use a relative rather than absolute evaluation system. Our aim was to test whether a decoy influenced the decision-making process-that is, information-gathering and food choice-of a free-ranging mammalian herbivore. We tested swamp wallabies, Wallabia bicolor, comparing their behavior toward, and choice of, two available food options over time in the absence or presence of the decoy. We used a phantom decoy-unavailable option-and ran two trials in different locations and seasons. Binary preferences (decoy absent) for the two available food options differed between trials. Irrespective of this difference, across both trials the presence of the decoy resulted in animals more likely to overtly investigate available food options. But, the decoy only shifted food choice, weakly, in one trial. Our results indicate that the decoy influenced the information-gathering behavior during decision-making, providing the first evidence that decoys can affect decision-making process of free-ranging mammalian herbivores in an ecologically realistic context. It is premature to say these findings confirm the use of relative evaluation systems. Whether the foraging outcome is more strongly affected by other decoys, food dimensions, or ecological contexts, is yet to be determined.

Urbanisation generates multiple trait syndromes for terrestrial animal taxa worldwide.

Cities can host significant biological diversity. Yet, urbanisation leads to the loss of habitats, species, and functional groups. Understanding how multiple taxa respond to urbanisation globally is essential to promote and conserve biodiversity in cities. Using a dataset encompassing six terrestrial faunal taxa (amphibians, bats, bees, birds, carabid beetles and reptiles) across 379 cities on 6 continents, we show that urbanisation produces taxon-specific changes in trait composition, with traits related to reproductive strategy showing the strongest response. Our findings suggest that urbanisation results in four trait syndromes (mobile generalists, site specialists, central place foragers, and mobile specialists), with resources associated with reproduction and diet likely driving patterns in traits associated with mobility and body size. Functional diversity measures showed varied responses, leading to shifts in trait space likely driven by critical resource distribution and abundance, and taxon-specific trait syndromes. Maximising opportunities to support taxa with different urban trait syndromes should be pivotal in conservation and management programmes within and among cities. This will reduce the likelihood of biotic homogenisation and helps ensure that urban environments have the capacity to respond to future challenges. These actions are critical to reframe the role of cities in global biodiversity loss.

Modelling daily weight variation in honey bee hives.

A quantitative understanding of the dynamics of bee colonies is important to support global efforts to improve bee health and enhance pollination services. Traditional approaches focus either on theoretical models or data-centred statistical analyses. Here we argue that the combination of these two approaches is essential to obtain interpretable information on the state of bee colonies and show how this can be achieved in the case of time series of intra-day weight variation. We model how the foraging and food processing activities of bees affect global hive weight through a set of ordinary differential equations and show how to estimate the parameters of this model from measurements on a single day. Our analysis of 10 hives at different times shows that the estimation of crucial indicators of the health of honey bee colonies are statistically reliable and fall in ranges compatible with previously reported results. The crucial indicators, which include the amount of food collected (foraging success) and the number of active foragers, may be used to develop early warning indicators of colony failure.

Heightened condition dependent expression of structural coloration in the faces, but not wings, of male and female flies.

Structurally colored sexual signals are a conspicuous and widespread class of ornament used in mate choice, though the extent to which they encode information on the quality of their bearers is not fully resolved. Theory predicts that signaling traits under strong sexual selection as honest indicators should evolve to be more developmentally integrated and exaggerated than nonsexual traits, thereby leading to heightened condition dependence. Here, we test this prediction through examination of the sexually dimorphic faces and wings of the cursorial fly Lispe cana. Males and females possess structural UV-white and golden faces, respectively, and males present their faces and wings to females during close-range, ground-based courtship displays, thereby creating the opportunity for mutual inspection. Across a field-collected sample of individuals, we found that the appearance of the faces of both sexes scaled positively with individual condition, though along separate axes. Males in better condition expressed brighter faces as modeled according to conspecific flies, whereas condition scaled with facial saturation in females. We found no such relationships for their wing interference pattern nor abdomens, with the latter included as a nonsexual control. Our results suggest that the structurally colored faces, but not the iridescent wings, of male and female L. cana are reliable guides to individual quality and support the broader potential for structural colors as honest signals. They also highlight the potential for mutual mate choice in this system, while arguing for 1 of several alternate signaling roles for wing interferences patterns among the myriad taxa which bear them.

The exploitation of sexual signals by predators: a meta-analysis.

Sexual signals are often central to reproduction, and their expression is thought to strike a balance between advertising to mates and avoiding detection by predatory eavesdroppers. Tests of the predicted predation costs have produced mixed results, however. Here we synthesized 187 effects from 78 experimental studies in a meta-analytic test of two questions; namely, whether predators, parasites and parasitoids express preferences for the sexual signals of prey, and whether sexual signals increase realized predation risk in the wild. We found that predators and parasitoids express strong and consistent preferences for signals in forced-choice contexts. We found a similarly strong overall increase in predation on sexual signallers in the wild, though here it was modality specific. Olfactory and acoustic signals increased the incidence of eavesdropping relative to visual signals, which experienced no greater risk than controls on average. Variation in outcome measures was universally high, suggesting that contexts in which sexual signalling may incur no cost, or even reduce the incidence of predation, are common. Our results reveal unexpected complexity in a central viability cost to sexual signalling, while also speaking to applied problems in invasion biology and pest management where signal exploitation holds promise for bio-inspired solutions.

Understanding dietary carbohydrates in black soldier fly larvae treatment of organic waste in the circular economy.

Black soldier fly larvae (BSFL) treatment is promising for organic waste valorisation in the circular economy; however, waste variability impacts the process performance and quality of produced larvae. Specifically, variation in the carbohydrate profile of treated wastes has been suggested to have a significant impact on BSFL treatment performance and quality of produced larvae, with particular carbohydrates either positively or negatively influencing these variables. This study examines the hypothesis that the types of carbohydrates within the substrate can have significant influence on larval survival, waste reduction, bioconversion, and waste conversion efficiency, as well as the crude lipid content and fatty acid profiles of the produced larvae. The carbohydrates explored were D glucose, sucrose, D (-) fructose, corn and wheat starch, D (+) galactose, D (+) mannose, D (+) xylose, D (-) arabinose and xylan from beechwood. Young larvae were grown for 9 days on chicken feed-based diets containing various carbohydrate additives each at 20 dry mass %. Treatments containing hemicellulose constituents galactose and arabinose produced the most adverse effects on process performance relative to the benchmark. Xylan was significantly detrimental to bioconversion (-14.7 ± 3.8%) and waste conversion efficiencies (-19.0 ± 4.4%). There were minimal significant effects on performance from mono- and di-saccharides and starch additives. Larvae crude lipid contents were significantly increased by wheat starch (+12.6 ± 3.0%) and decreased by galactose (-15.0 ± 1.4%) and xylan additives (-27.5 ± 3.4%), however fatty acid profiles were largely unaffected and were dominated by lauric acid. These results indicate that despite an otherwise balanced and nutritious substrate, the carbohydrate profile of organic waste should be an important consideration in BSFL treatment when ensuring process performance and larval lipid contents. The consequences of these results for BSFL treatment of real wastes are discussed. Large scale treatment facilities should formulate substrates accordingly and identify methods to mitigate the anti-nutritional effects of poor carbohydrate profiles, particularly those high in hemicelluloses and their constituents.

How do insects choose flowers? A review of multi-attribute flower choice and decoy effects in flower-visiting insects.

Understanding why animals (including humans) choose one thing over another is one of the key questions underlying the fields of behavioural ecology, behavioural economics and psychology. Most traditional studies of food choice in animals focus on simple, single-attribute decision tasks. However, animals in the wild are often faced with multi-attribute choice tasks where options in the choice set vary across multiple dimensions. Multi-attribute decision-making is particularly relevant for flower-visiting insects faced with deciding between flowers that may differ in reward attributes such as sugar concentration, nectar volume and pollen composition as well as non-rewarding attributes such as colour, symmetry and odour. How do flower-visiting insects deal with complex multi-attribute decision tasks? Here we review and synthesise research on the decision strategies used by flower-visiting insects when making multi-attribute decisions. In particular, we review how different types of foraging frameworks (classic optimal foraging theory, nutritional ecology, heuristics) conceptualise multi-attribute choice and we discuss how phenomena such as innate preferences, flower constancy and context dependence influence our understanding of flower choice. We find that multi-attribute decision-making is a complex process that can be influenced by innate preferences, flower constancy, the composition of the choice set and economic reward value. We argue that to understand and predict flower choice in flower-visiting insects, we need to move beyond simplified choice sets towards a view of multi-attribute choice which integrates the role of non-rewarding attributes and which includes flower constancy, innate preferences and context dependence. We further caution that behavioural experiments need to consider the possibility of context dependence in the design and interpretation of preference experiments. We conclude with a discussion of outstanding questions for future research. We also present a conceptual framework that incorporates the multiple dimensions of choice behaviour.

Irreversible sterility of workers and high-volume egg production by queens in the stingless bee Tetragonula carbonaria.

Social insects are characterised by a reproductive division of labour between queens and workers. However, in the majority of social insect species, the workers are only facultatively sterile. The Australian stingless bee Tetragonula carbonaria is noteworthy as workers never lay eggs. Here, we describe the reproductive anatomy of Tcarbonaria workers, virgin queens and mated queens. We then conduct the first experimental test of absolute worker sterility in the social insects. Using a controlled microcolony environment, we investigate whether the reproductive capacity of adult workers can be rescued by manipulating the workers' social environment and diet. The ovaries of T. carbonaria workers that are queenless and fed unrestricted, highly nutritious royal jelly remain non-functional, indicating they are irreversibly sterile and that ovary degeneration is fixed prior to adulthood. We suggest that Tcarbonaria might have evolved absolute worker sterility because colonies are unlikely to ever be queenless.

Dual ecosystem services of syrphid flies (Diptera: Syrphidae): pollinators and biological control agents.

With increasing worldwide pressure on bee pollinator populations and an increase in insecticide resistance amongst pest insects, there is a growing need for diversification of pollinator and pest control systems. Syrphid flies (Diptera: Syrphidae) contribute ecosystem services to agroecosystems through their supporting roles as crop pollinators and predators of pests. Adult syrphids are important pollinators with high floral visitation rates and pollen carrying capacity, while predatory syrphid larvae are natural biological control agents, reducing aphid populations in both field and laboratory conditions. The present challenge is to determine whether syrphid flies have the potential for application as pollinators and in integrated pest management schemes as biological control agents. Currently, there are gaps in research that are hindering the use of syrphids as dual service providers. Such gaps include a lack of knowledge of syrphid floral preferences, the role and viability of adult syrphids as pollinators in natural and agro-ecological pollinator networks, and the predatory efficiency of larvae in field and glasshouse conditions. By reviewing relevant literature, we demonstrate syrphid flies have the potential to be used as pollinators and biological control agents. © 2020 Society of Chemical Industry.

Meat ants cut more trail shortcuts when facing long detours.

Engineered paths increase efficiency and safety but also incur construction and maintenance costs, leading to a trade-off between investment and gain. Such a trade-off is faced by Australian meat ants, which create and maintain vegetation-free trails between nests and food sources, and thus their trails are expected to be constructed selectively. To test this, we placed an artificial obstacle consisting of 300 paper grass blades between a sucrose feeder and the colony, flanked by walls either 10 cm or 80 cm long. To exploit the feeder, ants could detour around the walls or take a direct route by traversing through the obstacle. We found that, when confronted with a long alternative detour, 76% of colonies removed more grass blades and ants were also 60% more likely to traverse the obstacle instead of detouring, with clearing activity favouring higher ant flow or vice versa. An analysis of cut patterns revealed that ants did not cut randomly, but instead concentrated on creating a trail to the food source. Meat ants were thus able to collectively deploy their trail-clearing efforts in a directed manner when detour costs were high, and rapidly established cleared trails to the food source by focusing on completing a central, vertically aligned trail which was then followed by the ants.

Network growth models: A behavioural basis for attachment proportional to fitness.

Several growth models have been proposed in the literature for scale-free complex networks, with a range of fitness-based attachment models gaining prominence recently. However, the processes by which such fitness-based attachment behaviour can arise are less well understood, making it difficult to compare the relative merits of such models. This paper analyses an evolutionary mechanism that would give rise to a fitness-based attachment process. In particular, it is proven by analytical and numerical methods that in homogeneous networks, the minimisation of maximum exposure to node unfitness leads to attachment probabilities that are proportional to node fitness. This result is then extended to heterogeneous networks, with supply chain networks being used as an example.

Argentine ants (Linepithema humile) use adaptable transportation networks to track changes in resource quality.

Transportation networks play a crucial role in human and animal societies. For a transportation network to be efficient, it must have adequate capacity to meet traffic demand. Network design becomes increasingly difficult in situations where traffic demand can change unexpectedly. In humans, network design is often constrained by path dependency because it is difficult to move a road once it is built. A similar issue theoretically faces pheromone-trail-laying social insects; once a trail has been laid, positive feedback makes re-routing difficult because new trails cannot compete with continually reinforced pre-existing trails. In the present study, we examined the response of Argentine ant colonies and their trail networks to variable environments where resources differ in quality and change unexpectedly. We found that Argentine ant colonies effectively tracked changes in food quality such that colonies allocated the highest proportion of foragers to the most rewarding feeder. Ant colonies maximised access to high concentration feeders by building additional trails and routes connecting the nest to the feeder. Trail networks appeared to form via a pruning process in which lower traffic trails were gradually removed from the network. At the same time, we observed several instances where new trails appear to have been built to accommodate a surge in demand. The combination of trail building when traffic demand is high and trail pruning when traffic demand is low results in a demand-driven network formation system that allows ants to monopolise multiple dynamic resources.

Decision-making without a brain: how an amoeboid organism solves the two-armed bandit.

Several recent studies hint at shared patterns in decision-making between taxonomically distant organisms, yet few studies demonstrate and dissect mechanisms of decision-making in simpler organisms. We examine decision-making in the unicellular slime mould Physarum polycephalum using a classical decision problem adapted from human and animal decision-making studies: the two-armed bandit problem. This problem has previously only been used to study organisms with brains, yet here we demonstrate that a brainless unicellular organism compares the relative qualities of multiple options, integrates over repeated samplings to perform well in random environments, and combines information on reward frequency and magnitude in order to make correct and adaptive decisions. We extend our inquiry by using Bayesian model selection to determine the most likely algorithm used by the cell when making decisions. We deduce that this algorithm centres around a tendency to exploit environments in proportion to their reward experienced through past sampling. The algorithm is intermediate in computational complexity between simple, reactionary heuristics and calculation-intensive optimal performance algorithms, yet it has very good relative performance. Our study provides insight into ancestral mechanisms of decision-making and suggests that fundamental principles of decision-making, information processing and even cognition are shared among diverse biological systems.

Resilience in social insect infrastructure systems.

Both human and insect societies depend on complex and highly coordinated infrastructure systems, such as communication networks, supply chains and transportation networks. Like human-designed infrastructure systems, those of social insects are regularly subject to disruptions such as natural disasters, blockages or breaks in the transportation network, fluctuations in supply and/or demand, outbreaks of disease and loss of individuals. Unlike human-designed systems, there is no deliberate planning or centralized control system; rather, individual insects make simple decisions based on local information. How do these highly decentralized, leaderless systems deal with disruption? What factors make a social insect system resilient, and which factors lead to its collapse? In this review, we bring together literature on resilience in three key social insect infrastructure systems: transportation networks, supply chains and communication networks. We describe how systems differentially invest in three pathways to resilience: resistance, redirection or reconstruction. We suggest that investment in particular resistance pathways is related to the severity and frequency of disturbance. In the final section, we lay out a prospectus for future research. Human infrastructure networks are rapidly becoming decentralized and interconnected; indeed, more like social insect infrastructures. Human infrastructure management might therefore learn from social insect researchers, who can in turn make use of the mature analytical and simulation tools developed for the study of human infrastructure resilience.

Collective behaviour and swarm intelligence in slime moulds.

The study of collective behaviour aims to understand how individual-level behaviours can lead to complex group-level patterns. Collective behaviour has primarily been studied in animal groups such as colonies of insects, flocks of birds and schools of fish. Although less studied, collective behaviour also occurs in microorganisms. Here, we argue that slime moulds are powerful model systems for solving several outstanding questions in collective behaviour. In particular, slime mould may hold the key to linking individual-level mechanisms to colony-level behaviours. Using well-established principles of collective animal behaviour as a framework, we discuss the extent to which slime mould collectives are comparable to animal groups, and we highlight some potentially fruitful areas for future research.

Individual honey bee (Apis cerana) foragers adjust their fuel load to match variability in forage reward.

Animals may adjust their behavior according to their perception of risk. Here we show that free-flying honey bee (Apis cerana) foragers mitigate the risk of starvation in the field when foraging on a food source that offers variable rewards by carrying more 'fuel' food on their outward journey. We trained foragers to a feeder located 1.2 km from each of four colonies. On average foragers carried 12.7% greater volume of fuel, equivalent to 30.2% more glucose when foraging on a variable source (a random sequence of 0.5, 1.5 and 2.5 M sucrose solution, average sucrose content 1.5 M) than when forging on a consistent source (constant 1.5 M sucrose solution). Our findings complement an earlier study that showed that foragers decrease their fuel load as they become more familiar with a foraging place. We suggest that honey bee foragers are risk sensitive, and carry more fuel to minimize the risk of starvation in the field when a foraging trip is perceived as being risky, either because the forager is unfamiliar with the foraging site, or because the forage available at a familiar site offers variable rewards.