Multinational evaluation of genetic diversity indicators for the Kunming-Montreal Global Biodiversity Framework.

Under the recently adopted Kunming-Montreal Global Biodiversity Framework, 196 Parties committed to reporting the status of genetic diversity for all species. To facilitate reporting, three genetic diversity indicators were developed, two of which focus on processes contributing to genetic diversity conservation: maintaining genetically distinct populations and ensuring populations are large enough to maintain genetic diversity. The major advantage of these indicators is that they can be estimated with or without DNA-based data. However, demonstrating their feasibility requires addressing the methodological challenges of using data gathered from diverse sources, across diverse taxonomic groups, and for countries of varying socio-economic status and biodiversity levels. Here, we assess the genetic indicators for 919 taxa, representing 5271 populations across nine countries, including megadiverse countries and developing economies. Eighty-three percent of the taxa assessed had data available to calculate at least one indicator. Our results show that although the majority of species maintain most populations, 58% of species have populations too small to maintain genetic diversity. Moreover, genetic indicator values suggest that IUCN Red List status and other initiatives fail to assess genetic status, highlighting the critical importance of genetic indicators.

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.

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.

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.

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.

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.

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.

Slime moulds use heuristics based on within-patch experience to decide when to leave.

Animals foraging in patchy, non-renewing or slowly renewing environments must make decisions about how long to remain within a patch. Organisms can use heuristics ('rules of thumb') based on available information to decide when to leave the patch. Here, we investigated proximate patch-departure heuristics in two species of giant, brainless amoeba: the slime moulds Didymium bahiense and Physarum polycephalum. We explicitly tested the importance of information obtained through experience by eliminating chemosensory cues of patch quality. In P. polycephalum, patch departure was influenced by the consumption of high, and to a much lesser extent low, quality food items such that engulfing a food item increased patch-residency time. Physarum polycephalum also tended to forage for longer in darkened, 'safe' patches. In D. bahiense, engulfment of any food item increased patch residency irrespective of that food item's quality. Exposure to light had no effect on the patch-residency time of D. bahiense. Given that these organisms lack a brain, our results illustrate how the use of simple heuristics can give the impression that individuals make sophisticated foraging decisions.

Phantom alternatives influence food preferences in the eastern honeybee Apis cerana.

Most models of animal choice behaviour assume that desirable but unavailable options, such as a high quality, but inhabited nest sites, do not influence an individual's preferences for the remaining options. However, experiments suggest that in mammals, the mere presence of such 'phantom' alternatives can alter, and even reverse, an individual's preferences for other items in a choice set. Phantom alternatives may be widespread in nature, as they occur whenever a resource is visible, but unavailable at the time of choice. They are particularly relevant for nectar-foraging animals, where previously rewarding flowers may sometimes be empty. Here, we investigate the effect of phantom alternatives on feeder preferences in the eastern honeybee, Apis cerana. First, we tested the effects of unattractive and attractive phantom alternatives by presenting individual bees with either a binary choice set containing two feeders that differed strongly in two qualities, but were equally preferred overall ('option 1' and 'option 2'), or a ternary choice set containing option 1, option 2 and one of two phantom types (unattractive and attractive). Secondly, we determined whether phantoms increase (similarity effect) or decrease (dissimilarity effect) preference for phantom-similar choices. In binary trials, bees had no significant preference for option 1 or option 2. However, after encountering an attractive phantom alternative, individual bees preferred option 2. The unattractive phantom did not influence bee preferences. Phantoms consistently changed individual bee preferences in favour of the phantom-similar choice. This means that the presence of an attractive food source, even if it is unavailable, can influence preference relationships between remaining items in the choice set. Our findings highlight the importance of considering the potential for phantom effects when studying the foraging behaviour of animals. Our results are particularly relevant for nectarivores, where empty but previously rewarding flowers are a common occurrence. Since an increase in pollinator visits can result in higher seed set, our results open up the possibility that by shifting pollinator preferences, empty flowers could have otherwise-unpredicted influences on community composition, plant-pollinator interactions and pollinator behaviour.

Slime mold uses an externalized spatial "memory" to navigate in complex environments.

Spatial memory enhances an organism's navigational ability. Memory typically resides within the brain, but what if an organism has no brain? We show that the brainless slime mold Physarum polycephalum constructs a form of spatial memory by avoiding areas it has previously explored. This mechanism allows the slime mold to solve the U-shaped trap problem--a classic test of autonomous navigational ability commonly used in robotics--requiring the slime mold to reach a chemoattractive goal behind a U-shaped barrier. Drawn into the trap, the organism must rely on other methods than gradient-following to escape and reach the goal. Our data show that spatial memory enhances the organism's ability to navigate in complex environments. We provide a unique demonstration of a spatial memory system in a nonneuronal organism, supporting the theory that an externalized spatial memory may be the functional precursor to the internal memory of higher organisms.

Amoeboid organism solves complex nutritional challenges.

A fundamental question in nutritional biology is how distributed systems maintain an optimal supply of multiple nutrients essential for life and reproduction. In the case of animals, the nutritional requirements of the cells within the body are coordinated by the brain in neural and chemical dialogue with sensory systems and peripheral organs. At the level of an insect society, the requirements for the entire colony are met by the foraging efforts of a minority of workers responding to cues emanating from the brood. Both examples involve components specialized to deal with nutrient supply and demand (brains and peripheral organs, foragers and brood). However, some of the most species-rich, largest, and ecologically significant heterotrophic organisms on earth, such as the vast mycelial networks of fungi, comprise distributed networks without specialized centers: How do these organisms coordinate the search for multiple nutrients? We address this question in the acellular slime mold Physarum polycephalum and show that this extraordinary organism can make complex nutritional decisions, despite lacking a coordination center and comprising only a single vast multinucleate cell. We show that a single slime mold is able to grow to contact patches of different nutrient quality in the precise proportions necessary to compose an optimal diet. That such organisms have the capacity to maintain the balance of carbon- and nitrogen-based nutrients by selective foraging has considerable implications not only for our understanding of nutrient balancing in distributed systems but for the functional ecology of soils, nutrient cycling, and carbon sequestration.

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.

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.

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.

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.

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.

Irrational decision-making in an amoeboid organism: transitivity and context-dependent preferences.

Most models of animal foraging and consumer choice assume that individuals make choices based on the absolute value of items and are therefore 'economically rational'. However, frequent violations of rationality by animals, including humans, suggest that animals use comparative valuation rules. Are comparative valuation strategies a consequence of the way brains process information, or are they an intrinsic feature of biological decision-making? Here, we examine the principles of rationality in an organism with radically different information-processing mechanisms: the brainless, unicellular, slime mould Physarum polycephalum. We offered P. polycephalum amoebas a choice between food options that varied in food quality and light exposure (P. polycephalum is photophobic). The use of an absolute valuation rule will lead to two properties: transitivity and independence of irrelevant alternatives (IIA). Transitivity is satisfied if preferences have a consistent, linear ordering, while IIA states that a decision maker's preference for an item should not change if the choice set is expanded. A violation of either of these principles suggests the use of comparative rather than absolute valuation rules. Physarum polycephalum satisfied transitivity by having linear preference rankings. However, P. polycephalum's preference for a focal alternative increased when a third, inferior quality option was added to the choice set, thus violating IIA and suggesting the use of a comparative valuation process. The discovery of comparative valuation rules in a unicellular organism suggests that comparative valuation rules are ubiquitous, if not universal, among biological decision makers.

Speed-accuracy trade-offs during foraging decisions in the acellular slime mould Physarum polycephalum.

Speed-accuracy trade-offs (SATs) are thought to be a fundamental feature of biological information processing, yet most evidence of SATs comes from animals. Here, we examine SATs in the foraging decisions of an acellular, amoeboid organism: the slime mould Physarum polycephalum. Slime moulds were given a simple discrimination task: selecting the highest-quality food item from a set of three options. We investigated the effect of two stressors, light exposure and hunger, on the speed and accuracy of decision-making. We also examined the effect of task difficulty. When given a difficult discrimination task, stressed individuals tend to make faster decisions than non-stressed individuals. This effect was reversed in plasmodia given easy discrimination tasks, where stressed individuals made slower decisions than non-stressed individuals. We found evidence of SATs, such that individuals who made fast decisions were more likely to make costly errors by selecting the worst possible food option. Our results suggest that SATs occur in a wider range of taxa than previously considered.

Food quality and the risk of light exposure affect patch-choice decisions in the slime mold Physarum polycephalum.

How individuals deal with multiple conflicting demands is an important aspect of foraging ecology, yet work on foraging behavior has typically neglected neurologically simple organisms. Here we examine the impact of an abiotic risk (light) and energetic status on the foraging decisions of a protist, the slime mold Physarum polycephalum. We examined patch choice in a "non-risky" environment by presenting starved and non-starved P. polycephalum amoebas with a choice between two shaded food patches (one high quality, one low quality). We next examined patch choice in the presence of a conflict between foraging risk (light exposure) and food quality by presenting amoebas with a choice between a shaded, low-quality patch, and a light-exposed, high-quality patch. When both patches were shaded, 100% of amoebas selected the higher quality food patch, irrespective of food-quality differences or the individual's energetic status. When light exposure and food quality conflicted, amoebas selected the patch with the higher food quality when the quality difference between the patches was high. When the quality difference between patches was small, amoebas selected the shaded, lower quality patch.