Biology Letters

Do kea parrots infer the weight of objects from their movement in a breeze?
Temeroli E, Jelbert SA and Lambert ML
Weight, though it cannot be seen directly, pervades nearly every aspect of an animal's life. However, the extent to which non-human animals reason about the property of weight remains poorly understood. Recent evidence highlights birds as a promising group for testing this ability: for example, New Caledonian crows can infer the weight of objects after observing their movements in a breeze. Here, we tested for similar weight inference abilities in kea (), a parrot species known for its sophisticated problem-solving skills. Subjects were trained to exchange objects of a target weight (light or heavy) for a food reward. They were then allowed to observe pairs of novel objects (one light and one heavy) hung in front of an electric fan in both an experimental condition (fan on, light object moving) and a control condition (fan off, both objects motionless). The birds were subsequently presented with test trials in which they could use the information from the demonstration to select an object of their target weight. We found that, unlike New Caledonian crows, kea did not perform significantly better on trials in which they observed the objects' movements and discussed our findings within the context of the kea's highly explorative nature.
Ionizing radiation has negligible effects on the age, telomere length and corticosterone levels of Chornobyl tree frogs
Burraco P, Gabor C, Bryant A, Gardette V, Lengagne T, Bonzom JM and Orizaola G
The accident that occurred at the Chornobyl nuclear power plant (Ukraine, 1986) contaminated a large extension of territory after the deposition of radioactive material. It is still under debate whether the chronic exposure to the radiation levels currently present in the area has long-term effects on organisms, such as decreases in longevity. Here, we investigate whether current levels of radiation in Chornobyl negatively impact the age of the Eastern tree frog . We also explore whether radiation induces changes in an ageing marker, telomere length or the stress hormone corticosterone. We found no effect of total individual absorbed radiation (including both external and internal exposure) on frog age ( = 197 individuals sampled in 3 consecutive years). We also did not find any relationship between individual absorbed radiation and telomere length, nor between individual absorbed radiation and corticosterone levels. Our results suggest that radiation levels currently experienced by Chornobyl tree frogs may not be high enough to cause severe chronic damage to semi-aquatic vertebrates such as this species. This is the first study addressing age and stress hormones in Chornobyl wildlife, and thus future research will confirm if these results can be extended to other taxa.
Breed function and behaviour correlate with endocranial volume in domestic dogs
Balcarcel AM, Sánchez-Villagra MR, Evin A, Nussbaumer M, Hemelsdaël A and Geiger M
Domestic dogs display a remarkable diversity of functions, morphologies and cognitive abilities. Using data from 1682 dogs representing 172 breeds, we tested for variation in relative endocranial volume (REV), a proxy for brain size and a basic measure of cognitive ability, in relation to breed function, phylogenetic classification, cranial shape, cooperative behaviour and temperament. Function, body size, phylogenetic clade and cranial shape correlate with REV. Toy dogs, functioning mainly as companions, have the largest endocranial volumes relative to their body size. Working dogs, bred to perform complex human-assistance skills and reportedly possessing higher cognitive abilities, have the smallest. Our results thus show that complex skills and cooperative behaviour-a hallmark of social cognition-do not predict larger REV in dogs. However, REV increases with fear and aggression, attention-seeking and separation anxiety and decreases with trainability. Significant correlations between REV and behavioural traits underscore the evolutionary plasticity of mammalian brain size under domestication and artificial selection and provide support for hypotheses linking the modulation of fear and aggression to brain size change under domestication.
Fisheries-induced life-history changes recover in experimentally harvested fish populations
van Dijk SN, Sadler DE, Watts PC and Uusi-Heikkilä S
Overfishing is one of the greatest threats to fish populations. Size-selective harvesting favours faster juvenile growth, younger maturation, small adult body size and low reproductive output. Such changes might be slow to recover and ultimately threaten population fitness and survival. To study the recovery potential of exploited experimental populations, we compared life-history traits in three differently size-selected experimental lines (large-selected, small-selected and random-selected) after five generations of harvesting and 10 subsequent generations of recovery (i.e. cessation of harvesting). We show that after a recovery period twice as long as the harvesting period, the differences in adult body size among the selection lines have eroded. While there was still a significant body size difference among the selection lines, this did not translate to differences in reproductive success. Although size-selective harvesting causes phenotypic changes in exploited fish populations, we show that such changes are reversible if the recovery period is long enough.
Constant companions: wild zebra finch pairs display extreme spatial cohesion
Tyson C, Loning H, Griffith SC and Naguib M
Many animals maintain long-term monogamous partnerships, but the extent to which partners associate varies substantially and has implications for the scope of cooperation between pair members. Zebra finches () are monogamously paired for life and maintain continuous partnerships, raising questions as to if and how they maintain pair cohesion despite being non-territorial and having only short-range acoustic signals. While zebra finches are the best-studied songbird in captivity, their social and spatial behaviour in the wild is poorly understood. Determining pair cohesion in songbirds to date has almost exclusively been studied at specific locations where pairs would be expected to meet, such as nesting or feeding sites, without quantifying broader movements. Here, we used solar-powered automated tracking to simultaneously monitor the movements of radio-tagged zebra finch pairs during periods of breeding activity. We reveal extremely high spatial cohesion with pairs using nearly identical home ranges and maintaining close spatial proximity across large areas. This characterization of extremely high spatio-temporal coordination of zebra finch pairs provides important insights into the operation and benefits of monogamous relationships in highly mobile taxa, such as birds.
Parrots live in smaller groups on islands
Beauchamp G
Species living on islands are predictably different from their mainland counterparts in morphology and behaviour, but the source of these differences is still debated. Islands, in particular, are characterized by depauperate predator communities. Relaxed predation pressure might explain why living in groups, a common anti-predator adaptation in animals, is considered less likely on islands. However, the empirical evidence for this effect is scant and alternative explanations have been overlooked. For instance, smaller groups might be more common because island species are less studied, because a more stable food supply associated with benign climate on islands favours territoriality, or because the population density is too low to allow the formation of larger groups. I examined the determinants of foraging group size in parrots, a large worldwide avian order with many island populations. Using a multivariable phylogenetic framework, I found that foraging group size was smaller on islands than on the continents controlling for ecological variables known to influence group size such as diet and body size. In addition, the island effect persisted after controlling for research effort, climate variables and population density, suggesting that impoverished predator communities are an important driver of group size on islands.
butterfly flashiness crucially depends on wing scale curvature
Sosa Espinosa J, Stavenga DG, van der Kooi CJ and Giraldo MA
butterflies are widely known for their brilliant blue and flashy colours, which are produced by intricate wing scale structures. Not all species display a vibrant structural coloration; some are whitish or even brown. This suggests that there is considerable interspecific variation in wing scale anatomy, pigmentation and flashiness. As evidenced by numerous studies, the optical mechanism that creates the bright structural colours resides in the multilayered ridges of the wing scales, but the interspecific variation in flashiness has so far received little attention. Here, we investigate the wing components that influence the directional wing reflectivity. We therefore selected three species that greatly vary in colour and flashy appearance, , and . Applying morphological analyses, (micro-)spectrophotometry and imaging scatterometry on wing pieces and individual wing scales, we demonstrate that wings with flat scales produce highly directional reflections, whereas wings stacked with curved scales scatter light into a wider angular space, resulting in a spatially more diffuse appearance. We thus find that the curvature of the wing scales crucially determines the directionality of 's visual display. We discuss how the visual ecology of butterflies and environmental conditions can drive the evolution of flashy visual displays.
Pulsed artificial light at night alters moth flight behaviour
Fabusova M, Gaston KJ and Troscianko J
Vehicle headlights create pulsed artificial light at night (pALAN) that is unpredictable, intense and extends into previously dark areas. Nocturnal insects often have remarkable low-light vision, but their slow pupillary light responses may leave them vulnerable to pALAN, which has important ecological consequences. To test this, we exposed nocturnal moths-important pollinators and prey-to four pALAN treatments. These comprised 'cool' and 'warm' lights, either emitted from phosphor-coated light-emitting diodes (LEDs) or RGB (red-green-blue) LEDs, matched in colour (CCT) and intensity to human vision. We assessed the initial behavioural response, likely crucial to the survival of an organism, of 428 wild-caught moths comprising 64 species. We found that exposure to a cool phosphor-coated LED light pulse increased instances of erratic flight and flight-to-light that are likely detrimental as they increase the risks of impact with a vehicle, predation or excess energy expenditure. Our findings suggest that pALAN can cause a wide range of behavioural responses in nocturnal moths, but that the most harmful effects could be minimized by reversing the current shift towards high CCT (cool) phosphor-coated LED car headlights. Lower CCT or RGB alternatives are likely to provide benefits for road safety while reducing ecological harm.
Predation affects the evolution of sex-specific longevity
Pennell TM, Katsuki M, Archer CR, Sharma MD, Okada K and Hosken DJ
Predation, a major cause of natural selection, is classically thought to target the weak and sick. However, predators can target animals with condition-dependent sexual traits, and therefore, high-quality individuals can also be the focus of predation. Thus, it is not always clear which individuals are the foci of predators or how this affects trait evolution. Here, we tested for evolutionary effects of sex-specific predation on male and female longevity using replicate populations of the broad-horned flour beetle . We found that male-limited predation resulted in the evolution of reduced male and increased female longevity, while female-limited predation had no effects on the longevity of either sex. We also document the costs of reproduction. Coupled with other findings, our results suggest that predation impacts high-quality males and, because of negative intersexual genetic correlations, this increases female longevity.
The macroecology of Mesozoic dinosaurs
Chiarenza AA
Dinosaurs thrived for over 160 million years in Mesozoic ecosystems, displaying diverse ecological and evolutionary adaptations. Their ecology was shaped by large-scale climatic and biogeographic changes, calling for a 'deep-time' macroecological investigation. These factors include temperature fluctuations and the break up of Pangaea, influencing species richness, ecological diversity and biogeographic history. Recent improvements in the dinosaur fossil record have enabled large-scale studies of their responses to tectonic, geographic and climatic shifts. Trends in species diversity, body size and reproductive traits can now be analysed using quantitative approaches like phylogenetic comparative methods, machine learning and Bayesian inference. These patterns sometimes align with, but also deviate from, first-order macroecological rules (e.g. species-area relationship, latitudinal biodiversity gradient, Bergmann's rule). Accurate reconstructions of palaeobiodiversity and niche partitioning require ongoing taxonomic revisions and detailed anatomical descriptions. Interdisciplinary research combining sedimentology, geochemistry and palaeoclimatology helps uncover the environmental conditions driving dinosaur adaptations. Fieldwork in under-sampled regions, particularly at latitudinal extremes, is crucial for understanding the spatial heterogeneity of dinosaur ecosystems across the planet. Open science initiatives and online databases play a key role in advancing this field, enriching our understanding of deep-time ecological processes, and offering new insights into dinosaur macroecology and its broader implications.
Metabolic complementation between cells drives the evolution of tissues and organs
Pavlicev M, DiFrisco J, Love AC and Wagner GP
Although evolutionary transitions of individuality have been extensively theorized, little attention has been paid to the origin of levels of organization within organisms. How and why do specialized cells become organized into specialized tissues or organs? What spurs a transition in organizational level in cases where the function is already present in constituent cell types? We propose a hypothesis for this kind of evolutionary transition based on two features of cellular metabolism: metabolic constraints on functional performance and the capacity for metabolic complementation between parenchymal and supporting cells. These features suggest a scenario whereby pre-existing specialized cell types are integrated into tissues when changes to the internal or external environment favour offloading metabolic burdens from a primary specialized cell type onto supporting cells. We illustrate this process of 'supra-functionalization' using the nervous system and pancreas.
Uropygial secretion changes mouth colouration in starling nestlings
García-Núñez AJ, Soler JJ, Martínez-Renau E and Tomás G
Cosmetic colourations of animals have been mainly studied in scenarios of sexual selection, while there has been no assessment of the partial contribution of cosmetics to the final colouration of begging-related traits. In birds, the uropygial gland is functional soon after hatching, and we experimentally investigated the effects of uropygial secretion on mouth-flange colouration in spotless starling () nestlings. Nestlings' flange colouration was measured with a spectrophotometer before and after being either cleaned of, or painted with, its own uropygial secretion. After cleaning, flanges were brighter, more UV and less yellow-red coloured (chroma). Instead, painting the mouth flanges of nestlings with their own uropygial secretion did not modify any of the considered colour components. Our findings therefore show that the uropygial secretion of nestlings alters their beak colouration and open the possibility for future research to investigate the role of uropygial secretion in reinforcing the signalling role of begging-related traits involved in parent-offspring communication.
Tickling induces a unique type of spontaneous laughter
Kamiloğlu RG, Sun R, Bos P, Huber F, Attema JJ and Sauter DA
Laughing is ubiquitous in human life, yet what causes it and how it sounds is highly variable. Considering this diversity, we sought to test whether there are fundamentally different kinds of laughter. Here, we sampled spontaneous laughs ( = 887) from a wide range of everyday situations (e.g. comedic performances and playful pranks). Machine learning analyses showed that laughs produced during tickling are acoustically distinct from laughs triggered by other kinds of events (verbal jokes, watching something funny or witnessing someone else's misfortune). In a listening experiment ( = 201), participants could accurately identify tickling-induced laughter, validating that such laughter is not only acoustically but also perceptually distinct. A second listening study ( = 210) combined with acoustic analyses indicates that tickling-induced laughter involves less vocal control than laughter produced in other contexts. Together, our results reveal a unique acoustic and perceptual profile of laughter induced by tickling, an evolutionarily ancient play behaviour, distinguishing it clearly from laughter caused by other triggers. This study showcases the power of machine learning in uncovering patterns within complex behavioural phenomena, providing a window into the evolutionary significance of ticking-induced laughter.
Vampire bats rapidly fuel running with essential or non-essential amino acids from a blood meal
Rossi GS and Welch KC
In most mammals, running is fuelled by oxidization of endogenous carbohydrates and lipids while amino acids contribute little (< 5-10%). Common vampire bats (), however, specialize on a unique, protein-rich blood diet. Therefore, we hypothesized that (i) vampire bats would rapidly begin utilizing dietary amino acids to support running metabolism, and (ii) that relative reliance on essential and non-essential amino acids would be similar. We fed bats cow's blood enriched either with isotopically labelled glycine (non-essential amino acid) or leucine (essential amino acid). Bats were exercised at speeds of 10, 20 and 30 m min on a respirometry treadmill, allowing us to assess metabolic rate (i.e. O consumption and CO production) and track the oxidation of labelled amino acids in exhaled CO. Vampire bats oxidized amino acids as their primary fuel as indicated by a respiratory exchange ratio (RER = ratio of CO production to O consumption rates) of approximately 0.8-0.9 at all speeds, with the labelled meal accounting for as much as 60% of oxidized fuels at peak usage. Similar oxidation rates indicated bats did not discriminate between essential and non-essential amino acid use. These findings reiterate how strongly metabolism can be shaped by a specialized diet.
A feminine advantage in the domain of harm: a review and path forward
Graso M and Reynolds T
Despite well-documented disparities disadvantaging women (e.g. discrepancies between men and women in salaries and leadership roles), we argue that there are contexts in which disparities disadvantage men. We review the literature suggesting harm to women is perceived as more severe and unacceptable than identical harm to men, a bias potentially rooted in evolutionary, base rate, stereotype-based and cultural shift explanations. We explore how these biases manifest in protective responses toward women and harsher judgements toward men, particularly in contexts of victimization and perpetration. Our review aims to complement the existing literature on gender biases by presenting a balanced view that acknowledges men and women face unique challenges. By understanding these biases, we hope to foster a more equitable discourse on gender and harm, encouraging empathy and validation of suffering irrespective of gender. This holistic approach aims to de-escalate gender-based conflicts and promote effective interventions for both men and women.
The significance of social interactions in synchronized swarming flight in a termite
Mizumoto N and Nozaki T
In social insects, individuals of working caste coordinate their actions to manage various collective tasks. Such collective behaviours exist not only in workers but also in winged reproductives (alates). During certain seasons, newly emerged alates fly from the nest to disperse and find mating partners in a synchronized manner. This 'swarming' behaviour is one of the collective behaviours that involve the greatest number of individuals in social insects. However, such synchronization is considered to be caused by the response to specific environmental cues rather than behavioural coordination among colony members. Here, we show that a termite shows synchronized dispersal flight among alates within the same colony even under the constant temperature environment. Under the semi-field environment with fluctuating temperatures, alates within the same colony synchronized their dispersal flight under higher temperatures, while flight was suppressed under lower temperatures. We observed that termites synchronized their dispersal flights even under constant temperature conditions in the laboratory (20℃), indicating that environmental cues are not always necessary for synchronization. In either case, higher synchronization happened with a larger number of alates. These results suggest that social factors interplay with environmental cues to enable the synchronized swarming flight of social insects.
A brief review of non-avian dinosaur biogeography: state-of-the-art and prospectus
Upchurch P and Chiarenza AA
Dinosaurs potentially originated in the mid-palaeolatitudes of Gondwana 245-235 million years ago (Ma) and may have been restricted to cooler, humid areas by low-latitude arid zones until climatic amelioration made northern dispersals feasible 215 Ma. However, this scenario is challenged by new Carnian Laurasian fossils and evidence that even the earliest dinosaurs had adaptations for arid conditions. After becoming globally distributed in the Early-Middle Jurassic (200-160 Ma), dinosaurs experienced vicariance driven by Pangaean fragmentation. Regional extinctions and trans-oceanic dispersals also played a role, and the formation of ephemeral land connections meant that older vicariance patterns were repeatedly overprinted by younger ones, creating a reticulate biogeographic history. Palaeoclimates shaped dispersal barriers and corridors, including filters that had differential effects on different types of dinosaurs. Dinosaurian biogeographic research faces many challenges, not the least of which is the patchiness of the fossil record. However, new fossils, extensive databasing and improved analytical methods help distinguish signal from noise and generate fresh perspectives. In the future, developing techniques for quantifying and ameliorating sampling biases and modelling the dispersal capacities of dinosaurs are likely to be two of the key components in our modern research programme.
Evidence for inbreeding depression in captive Damaraland mole-rats
Seager D, Leedale AE, Thorley JB, Vullioud P, Zöttl M and Clutton-Brock T
Mating between closely related individuals can result in a reduction in offspring fitness, known as inbreeding depression. Here, we investigate whether breeding with close relatives affects the reproductive output of parents and the development of their offspring in Damaraland mole-rats (), a cooperatively breeding species where females avoid mating with familiar individuals. By cross-fostering litters of pups soon after birth, we were able to form breeding pairs from full siblings that were reared apart. We compared the reproductive output of these sibling pairs and the survival and growth of their pups with that of unrelated pairs over a period of 4 years. The litter sizes and interbirth intervals of sibling pairs did not differ from those of unrelated pairs, but the growth and survival of inbred offspring were lower, showing that breeding between close relatives is associated with substantial fitness costs. This study suggests that inbreeding depression is an important driver of the extreme reproductive skew observed in social mole-rats. Studies of the costs of inbred matings are now needed in similar species, such as naked mole-rats (), where captive females more commonly breed with close relatives, to determine whether these costs are lower than in Damaraland mole-rats.
Reproduction results in parallel changes of oxidative stress and immunocompetence in a wild long-living mammal-edible dormouse
Iwińska K, Boratyński JS, Książek A, Błońska J, Borowski Z and Konarzewski M
Oxidative stress (OS) and impaired immune function (IF) have been proposed as key physiological costs of reproduction. The relationship between OS and IF remains unresolved, particularly in long-living iteroparous species. We studied physiological markers of maintenance (OS, IF markers) in lactating, post-lactating and non-lactating females of edible dormice-a long-living rodent. We predicted the OS balance and IF to be compromised by lactation, especially in older females expected to face stronger trade-offs between life functions. We found that the age predictor (body size) correlated negatively with white blood cell level (WBC), positively with neutrophils to lymphocytes ratio and had no effect on OS markers. Oxidative damage markers (reactive oxygen metabolites (ROMs); but not antioxidant capacity) and body size-adjusted WBC were the lowest in lactating, higher in post-lactating and the highest in non-lactating females. Body size/age did not affect this correlation suggesting a similar age-independent allocation strategy during reproduction in this species. The path analysis testing the causal relationship between ROMs and WBC revealed that IF is more likely to affect OS than . Our study indicates the trade-off between crucial life functions during reproduction and suggests that immunosuppression reduces the risk of OS; therefore, mitigating oxidative costs of reproduction.
Density-dependent dispersal reduces conflict over the sex ratio
Chokechaipaisarn C and Gardner A
Haplodiploids-in particular, wasps-are the workhorses of sex-allocation research. This is owing to their unusual system of sex determination, which provides a ready means of sex ratio adjustment. Notably, their sexually asymmetrical mode of genetic inheritance leads mothers and fathers to come into conflict over the sex ratio of their offspring. In the simplest outbreeding scenario, a mother is favoured to employ an even sex ratio while a father prefers that all his mate's offspring are female. An important modulator of evolutionary conflict between mating partners is genetic relatedness, raising the possibility that this sex ratio conflict is reduced in low-dispersal settings with mating occurring between relatives. However, the impact of population viscosity on sex ratio conflict in haplodiploids remains unknown. Here, we develop and analyse a kin-selection model to investigate how the rate of dispersal modulates sex ratio conflict in a haplodiploid, viscous population setting. We find that population viscosity is associated with a reduction in the extent of sex ratio conflict-the effect being very weak under density-independent dispersal and much stronger under density-dependent dispersal.
Molecular correlates of swarming behaviour in males
Devilliers J, Marshall H, Warren B, Kyriacou CP, Araripe LO, Bruno RV, Rosato E and Feuda R
Mosquitoes are the deadliest vectors of diseases. They impose a huge health burden on human populations spreading parasites as disparate as protozoans (malaria), viruses (yellow fever and more) and nematodes (filariasis) that cause life-threatening conditions. In recent years, mating has been proposed as a putative target for population control. Mosquitoes mate mid-air, in swarms initiated by males and triggered by a combination of internal and external stimuli. As the number of females in a swarm is limited, there is intense competition among males, and they 'retune' their physiology for this demanding behaviour. There is limited knowledge on the 'genetic reprogramming' required to enable swarming. Interestingly, recent evidence indicates that the upregulation of circadian clock genes may be involved in the swarming of malaria mosquitoes of the genus . Here, we use whole-head RNA-seq to identify gene expression changes in males that are engaged in swarming in a laboratory setting. Our results suggest that in preparation to swarming, males tend to lower some housekeeping functions while increasing remodelling of the cytoskeleton and neuronal connectivity; the transcription of circadian clock genes is unaffected.