Rapid color change in a group-hunting pelagic predator attacking schooling prey.

A major challenge for group-hunting predators is coordinating movement at high speed. Billfish - large predators with an elongated rostrum (bill) - include some of the fastest animals in the ocean and often form groups when hunting. This presents a challenge: how do fast-moving predators wielding dangerous weaponry reliably coordinate their attacks to avoid injury? We report a possible solution to this problem through rapid colour change in group-hunting striped marlin (Kajikia audax) as they hunt schools of Pacific sardines (Sardinops sagax). By analysing high-resolution drone footage of marlin attacks, we found that individual marlin intensified the contrast of their body stripes immediately prior to striking prey schools, before rapidly decreasing intensity after their attack. This suggests that color change may be a reliable signal of motivation to attack, potentially deterring conspecifics from attacking.

Thermal tolerance in an extremophile fish from Mexico is not affected by environmental hypoxia.

The thermal ecology of ectotherm animals has gained considerable attention in the face of human-induced climate change. Particularly in aquatic species, the experimental assessment of critical thermal limits (CTmin and CTmax) may help to predict possible effects of global warming on habitat suitability and ultimately species survival. Here we present data on the thermal limits of two endemic and endangered extremophile fish species, inhabiting a geothermally heated and sulfur-rich spring system in southern Mexico: The sulfur molly (Poecilia sulphuraria) and the widemouth gambusia (Gambusia eurystoma). Besides physiological challenges induced by toxic hydrogen sulfide and related severe hypoxia during the day, water temperatures have been previously reported to exceed those of nearby clearwater streams. We now present temperature data for various locations and years in the sulfur spring complex and conducted laboratory thermal tolerance tests (CTmin and CTmax) both under normoxic and severe hypoxic conditions in both species. Average CTmax limits did not differ between species when dissolved oxygen was present. However, critical temperature (CTmax=43.2°C) in P. sulphuraria did not change when tested under hypoxic conditions, while G. eurystoma on average had a lower CTmax when oxygen was absent. Based on this data we calculated both species' thermal safety margins and used a TDT (thermal death time) model framework to relate our experimental data to observed temperatures in the natural habitat. Our findings suggest that both species live near their thermal limits during the annual dry season and are locally already exposed to temperatures above their critical thermal limits. We discuss these findings in the light of possible physiological adaptions of the sulfur-adapted fish species and the anthropogenic threats for this unique system.

Reproductive individuality of clonal fish raised in near-identical environments and its link to early-life behavioral individuality.

Recent studies have documented among-individual phenotypic variation that emerges in the absence of apparent genetic and environmental differences, but it remains an open question whether such seemingly stochastic variation has fitness consequences. We perform a life-history experiment with naturally clonal fish, separated directly after birth into near-identical (i.e., highly standardized) environments, quantifying 2522 offspring from 152 broods over 280 days. We find that (i) individuals differ consistently in the size of offspring and broods produced over consecutive broods, (ii) these differences are observed even when controlling for trade-offs between brood size, offspring size and reproductive onset, indicating individual differences in life-history productivity and (iii) early-life behavioral individuality in activity and feeding patterns, with among-individual differences in feeding being predictive of growth, and consequently offspring size. Thus, our study provides experimental evidence that even when minimizing genetic and environmental differences, systematic individual differences in life-history measures and ultimately fitness can emerge.

The rostral micro-tooth morphology of blue marlin, Makaira nigricans.

Billfish rostra potentially have several functions; however, their role in feeding is unequivocal in some species. Recent work linked morphological variation in rostral micro-teeth to differences in feeding behavior in two billfish species, the striped marlin (Kajikia audax) and the sailfish (Istiophorus platypterus). Here, we present the rostral micro-tooth morphology for a third billfish species, the blue marlin (Makaira nigricans), for which the use of the rostrum in feeding behavior is still undocumented from systematic observations in the wild. We measured the micro-teeth on rostrum tips of blue marlin, striped marlin, and sailfish using a micro-computed tomography approach and compared the tooth morphology among the three species. This was done after an analysis of video-recorded hunting behavior of striped marlin and sailfish revealed that both species strike prey predominantly with the first third of the rostrum, which provided the justification to focus our analysis on the rostrum tips. In blue marlin, intact micro-teeth were longer compared to striped marlin but not to sailfish. Blue marlin had a higher fraction of broken teeth than both striped marlin and sailfish, and broken teeth were distributed more evenly on the rostrum. Micro-tooth regrowth was equally low in both marlin species but higher in sailfish. Based on the differences and similarities in the micro-tooth morphology between the billfish species, we discuss potential feeding-related rostrum use in blue marlin. We put forward the hypothesis that blue marlin might use their rostra in high-speed dashes as observed in striped marlin, rather than in the high-precision rostral strikes described for sailfish, possibly focusing on larger prey organisms.

Situational social influence leading to non-compliance with conservation rules.

It is well established that the decisions that we make can be strongly influenced by the behaviour of others. However, testing how social influence can lead to non-compliance with conservation rules during an individual's decision-making process has received little research attention. We synthesise advances in understanding of conformity and rule-breaking in individuals and in groups, and take a situational approach to studying the social dynamics and ensuing social identity changes that can lead to non-compliant decision-making. We focus on situational social influence contagion that are copresent (i.e., same space and same time) or trace-based (i.e., behavioural traces in the same space). We then suggest approaches for testing how situational social influence can lead to certain behaviours in non-compliance with conservation rules.

Mechanisms of group-hunting in vertebrates.

Group-hunting is ubiquitous across animal taxa and has received considerable attention in the context of its functions. By contrast much less is known about the mechanisms by which grouping predators hunt their prey. This is primarily due to a lack of experimental manipulation alongside logistical difficulties quantifying the behaviour of multiple predators at high spatiotemporal resolution as they search, select, and capture wild prey. However, the use of new remote-sensing technologies and a broadening of the focal taxa beyond apex predators provides researchers with a great opportunity to discern accurately how multiple predators hunt together and not just whether doing so provides hunters with a per capita benefit. We incorporate many ideas from collective behaviour and locomotion throughout this review to make testable predictions for future researchers and pay particular attention to the role that computer simulation can play in a feedback loop with empirical data collection. Our review of the literature showed that the breadth of predator:prey size ratios among the taxa that can be considered to hunt as a group is very large (<100 to >102 ). We therefore synthesised the literature with respect to these predator:prey ratios and found that they promoted different hunting mechanisms. Additionally, these different hunting mechanisms are also related to particular stages of the hunt (search, selection, capture) and thus we structure our review in accordance with these two factors (stage of the hunt and predator:prey size ratio). We identify several novel group-hunting mechanisms which are largely untested, particularly under field conditions, and we also highlight a range of potential study organisms that are amenable to experimental testing of these mechanisms in connection with tracking technology. We believe that a combination of new hypotheses, study systems and methodological approaches should help push the field of group-hunting in new directions.

Social competence improves the performance of biomimetic robots leading live fish.

Collective motion is commonly modeled with static interaction rules between agents. Substantial empirical evidence indicates, however, that animals may adapt their interaction rules depending on a variety of factors and social contexts. Here, we hypothesized that leadership performance is linked to the leader's responsiveness to the follower's actions and we predicted that a leader is followed longer if it adapts to the follower's avoidance movements. We tested this prediction with live guppies that interacted with a biomimetic robotic fish programmed to act as a 'socially competent' leader. Fish that were avoiding the robot were approached more carefully in future approaches. In two separate experiments we then asked how the leadership performance of the socially competent robot leader differed to that of a robot leader that either approached all fish in the same, non-responsive, way or one that did change its approach behavior randomly, irrespective of the fish's actions. We found that (1) behavioral variability itself appears attractive and that socially competent robots are better leaders which (2) require fewer approach attempts to (3) elicit longer average following behavior than non-competent agents. This work provides evidence that social responsiveness to avoidance reactions plays a role in the social dynamics of guppies. We showcase how social responsiveness can be modeled and tested directly embedded in a living animal model using adaptive, interactive robots.

Leveraging big data to uncover the eco-evolutionary factors shaping behavioural development.

Mapping the eco-evolutionary factors shaping the development of animals' behavioural phenotypes remains a great challenge. Recent advances in 'big behavioural data' research-the high-resolution tracking of individuals and the harnessing of that data with powerful analytical tools-have vastly improved our ability to measure and model developing behavioural phenotypes. Applied to the study of behavioural ontogeny, the unfolding of whole behavioural repertoires can be mapped in unprecedented detail with relative ease. This overcomes long-standing experimental bottlenecks and heralds a surge of studies that more finely define and explore behavioural-experiential trajectories across development. In this review, we first provide a brief guide to state-of-the-art approaches that allow the collection and analysis of high-resolution behavioural data across development. We then outline how such approaches can be used to address key issues regarding the ecological and evolutionary factors shaping behavioural development: developmental feedbacks between behaviour and underlying states, early life effects and behavioural transitions, and information integration across development.

Multispecies collective waving behaviour in fish.

Collective behaviour is widely accepted to provide a variety of antipredator benefits. Acting collectively requires not only strong coordination among group members, but also the integration of among-individual phenotypic variation. Therefore, groups composed of more than one species offer a unique opportunity to look into the evolution of both mechanistic and functional aspects of collective behaviour. Here, we present data on mixed-species fish shoals that perform collective dives. These repeated dives produce water waves capable of delaying and/or reducing the success of piscivorous bird attacks. The large majority of the fish in these shoals consist of the sulphur molly, Poecilia sulphuraria, but we regularly also found a second species, the widemouth gambusia, Gambusia eurystoma, making these shoals mixed-species aggregations. In a set of laboratory experiments, we found that gambusia were much less inclined to dive after an attack as compared with mollies, which almost always dive, though mollies dived less deep when paired with gambusia that did not dive. By contrast, the behaviour of gambusia was not influenced by the presence of diving mollies. The dampening effect of less responsive gambusia on molly diving behaviour can have strong evolutionary consequences on the overall collective waving behaviour as we expect shoals with a high proportion of unresponsive gambusia to be less effective at producing repeated waves. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Live fish learn to anticipate the movement of a fish-like robot.

The ability of an individual to predict the outcome of the actions of others and to change their own behavior adaptively is called anticipation. There are many examples from mammalian species-including humans-that show anticipatory abilities in a social context, however, it is not clear to what extent fishes can anticipate the actions of their interaction partners or what the underlying mechanisms are for that anticipation. To answer these questions, we let live guppies (Poecilia reticulata) interact repeatedly with an open-loop (noninteractive) biomimetic robot that has previously been shown to be an accepted conspecific. The robot always performed the same zigzag trajectory in the experimental tank that ended in one of the corners, giving the live fish the opportunity to learn both the location of the final destination as well as the specific turning movement of the robot over three consecutive trials. The live fish's reactions were categorized into a global anticipation, which we defined as relative time to reach the robot's final corner, and a local anticipation which was the relative time and location of the live fish's turns relative to robofish turns. As a proxy for global anticipation, we found that live fish in the last trial reached the robot's destination corner significantly earlier than the robot. Overall, more than 50% of all fish arrived at the destination before the robot. This is more than a random walk model would predict and significantly more compared to all other equidistant, yet unvisited, corners. As a proxy for local anticipation, we found fish change their turning behavior in response to the robot over the course of the trials. Initially, the fish would turn after the robot, which was reversed in the end, as they began to turn slightly before the robot in the final trial. Our results indicate that live fish are able to anticipate predictably behaving social partners both in regard to final movement locations as well as movement dynamics. Given that fish have been found to exhibit consistent behavioral differences, anticipation in fish could have evolved as a mechanism to adapt to different social interaction partners.

A cAMP signalosome in primary cilia drives gene expression and kidney cyst formation.

The primary cilium constitutes an organelle that orchestrates signal transduction independently from the cell body. Dysregulation of this intricate molecular architecture leads to severe human diseases, commonly referred to as ciliopathies. However, the molecular underpinnings how ciliary signaling orchestrates a specific cellular output remain elusive. By combining spatially resolved optogenetics with RNA sequencing and imaging, we reveal a novel cAMP signalosome that is functionally distinct from the cytoplasm. We identify the genes and pathways targeted by the ciliary cAMP signalosome and shed light on the underlying mechanisms and downstream signaling. We reveal that chronic stimulation of the ciliary cAMP signalosome transforms kidney epithelia from tubules into cysts. Counteracting this chronic cAMP elevation in the cilium by small molecules targeting activation of phosphodiesterase-4 long isoforms inhibits cyst growth. Thereby, we identify a novel concept of how the primary cilium controls cellular functions and maintains tissue integrity in a specific and spatially distinct manner and reveal novel molecular components that might be involved in the development of one of the most common genetic diseases, polycystic kidney disease.

Self-organization and information transfer in Antarctic krill swarms.

Antarctic krill swarms are one of the largest known animal aggregations, and yet, despite being the keystone species of the Southern Ocean, little is known about how swarms are formed and maintained. Understanding the local interactions between individuals that provide the basis for these swarms is fundamental to knowing how swarms arise in nature, and what potential factors might lead to their breakdown. Here, we analysed the trajectories of captive, wild-caught krill in 3D to determine individual-level interaction rules and quantify patterns of information flow. Our results demonstrate that krill align with near neighbours and that they regulate both their direction and speed relative to the positions of groupmates. These results suggest that social factors are vital to the formation and maintenance of swarms. Furthermore, krill operate a novel form of collective organization, with measures of information flow and individual movement adjustments expressed most strongly in the vertical dimension, a finding not seen in other swarming species. This research represents a vital step in understanding the fundamentally important swarming behaviour of krill.

Lacunae rostralis: A new structure on the rostrum of sailfish Istiophorus platypterus.

Recent comparative studies of billfishes (Istiophoridae and Xiphiidae) have provided evidence of differences in the form and function of the rostra (bill) among species. Here, we report the discovery of a new structure, lacuna rostralis, on the rostra of sailfish Istiophorus platypterus, which is absent on the rostra of swordfish Xiphias gladius, striped marlin Kajikia audax and blue marlin Makaira nigricans. The lacunae rostralis are small cavities that contain teeth. They were found on the ventral rostrum surface of all I. platypterus specimens examined and dorsally in half of them. Ventrally, the lacunae rostralis were most prominent in the mid-section of the rostrum. Dorsally, they occurred closer to the tip. The density of lacunae rostralis increased towards the rostrum tip but, because they are smaller in size, the percentage of rostrum coverage decreased. The teeth located within the lacunae rostralis were found to be different in size, location and orientation from the previously identified micro-teeth of billfish. We propose two potential functions of the lacunae rostralis that both relate to the use of the bill in feeding: mechanoreception of prey before tapping it with the bill and more efficient prey handling via the creation of suction, or physical grip.

Fish waves as emergent collective antipredator behavior.

The collective behavior of animals has attracted considerable attention in recent years, with many studies exploring how local interactions between individuals can give rise to global group properties.1-3 The functional aspects of collective behavior are less well studied, especially in the field,4 and relatively few studies have investigated the adaptive benefits of collective behavior in situations where prey are attacked by predators.5,6 This paucity of studies is unsurprising because predator-prey interactions in the field are difficult to observe. Furthermore, the focus in recent studies on predator-prey interactions has been on the collective behavior of the prey7-10 rather than on the behavior of the predator (but see Ioannou et al.11 and Handegard et al.12). Here we present a field study that investigated the anti-predator benefits of waves produced by fish at the water surface when diving down collectively in response to attacks of avian predators. Fish engaged in surface waves that were highly conspicuous, repetitive, and rhythmic involving many thousands of individuals for up to 2 min. Experimentally induced fish waves doubled the time birds waited until their next attack, therefore substantially reducing attack frequency. In one avian predator, capture probability, too, decreased with wave number and birds switched perches in response to wave displays more often than in control treatments, suggesting that they directed their attacks elsewhere. Taken together, these results support an anti-predator function of fish waves. The attack delay could be a result of a confusion effect or a consequence of waves acting as a perception advertisement, which requires further exploration.

Acoustic and visual stimuli combined promote stronger responses to aerial predation in fish.

Bird predation poses a strong selection pressure on fish. Since birds must enter the water to catch fish, a combination of visual and mechano-acoustic cues (multimodal) characterize an immediate attack, while single cues (unimodal) may represent less dangerous disturbances. We investigated whether fish could use this information to distinguish between non-threatening and dangerous events and adjust their antipredator response to the perceived level of risk. To do so, we investigated the antipredator behavior of the sulphur molly (Poecilia sulphuraria), a small freshwater fish which is almost exclusively preyed on by piscivorous birds in its endemic sulfide spring habitat. In a field survey, we confirmed that these fish frequently have to distinguish between disturbances stemming from attacking birds (multimodal) and those which pose no (immediate) threat such as bird overflights (unimodal). In a laboratory experiment, we then exposed fish to artificial visual and/or acoustic stimuli presented separately or combined. Sensitivity was high regardless of stimulus type and number (more than 96% of fish initiated diving), but fish dove deeper, faster, and for longer when both stimuli were available simultaneously. Based on the system's high rates of bird activity, we argue that such an unselective dive initiation with subsequent fine-tuning of diving parameters in accordance to cue modality represents an optimal strategy for these fish to save energy necessary to respond to future attacks. Ultimately, our study shows that fish anticipate the imminent risk posed by disturbances linked to bird predation through integrating information from both visual and acoustic cues.

Collective rule-breaking.

Rules form an important part of our everyday lives. Here we explore the role of social influence in rule-breaking. In particular, we identify some of the cognitive mechanisms underlying rule-breaking and propose approaches for how they can be scaled up to the level of groups or crowds to better understand the emergence of collective rule-breaking. Social contagion plays an important role in such processes and different dynamics such as linear or rapid nonlinear spreading can have important consequences for interventions in rule-breaking. A closer integration of cognitive psychology, microsociology and mathematical modelling will be key to a deeper understanding of collective rule-breaking to turn this field of research into a predictive science.

Pooling decisions decreases variation in response bias and accuracy.

Decision makers in contexts as diverse as medical, judicial, and political decision making are known to differ substantially in response bias and accuracy, and these differences are a major factor undermining the reliability and fairness of the respective decision systems. Using theoretical modeling and empirical testing across five domains, we show that collective systems based on pooling decisions robustly overcome this important but as of now unresolved problem of experts' heterogeneity. In breast and skin cancer diagnostics and fingerprint analysis, we find that pooling the decisions of five experts reduces the variation in sensitivity among decision makers by 52%, 54%, and 41%, respectively. Similar reductions are achieved for specificity and response bias, and in other domains. Thus, although outcomes in individual decision systems are highly variable and at the mercy of individual decision makers, collective systems based on pooling decrease this variation, thereby promoting reliability, fairness, and possibly even trust.

Evolving a New Efficient Mode of Fructose Utilization for Improved Bioproduction in Corynebacterium glutamicum.

Fructose utilization in Corynebacterium glutamicum starts with its uptake and concomitant phosphorylation via the phosphotransferase system (PTS) to yield intracellular fructose 1-phosphate, which enters glycolysis upon ATP-dependent phosphorylation to fructose 1,6-bisphosphate by 1-phosphofructokinase. This is known to result in a significantly reduced oxidative pentose phosphate pathway (oxPPP) flux on fructose (∼10%) compared to glucose (∼60%). Consequently, the biosynthesis of NADPH demanding products, e.g., L-lysine, by C. glutamicum is largely decreased when fructose is the only carbon source. Previous works reported that fructose is partially utilized via the glucose-specific PTS presumably generating fructose 6-phosphate. This closer proximity to the entry point of the oxPPP might increase oxPPP flux and, consequently, NADPH availability. Here, we generated deletion strains lacking either the fructose-specific PTS or 1-phosphofructokinase activity. We used these strains in short-term evolution experiments on fructose minimal medium and isolated mutant strains, which regained the ability of fast growth on fructose as a sole carbon source. In these fructose mutants, the deletion of the glucose-specific PTS as well as the 6-phosphofructokinase gene, abolished growth, unequivocally showing fructose phosphorylation via glucose-specific PTS to fructose 6-phosphate. Gene sequencing revealed three independent amino acid substitutions in PtsG (M260V, M260T, and P318S). These three PtsG variants mediated faster fructose uptake and utilization compared to native PtsG. In-depth analysis of the effects of fructose utilization via these PtsG variants revealed significantly increased ODs, reduced side-product accumulation, and increased L-lysine production by 50%.

Male Sexual Preference for Female Swimming Activity in the Guppy (Poecilia reticulata).

Mate choice that is based on behavioural traits is a common feature in the animal kingdom. Using the Trinidadian guppy, a species with mutual mate choice, we investigated whether males use female swimming activity-a behavioural trait known to differ consistently among individuals in many species-as a trait relevant for their mate choice. In the first experiment, we assessed male and female activity in an open field test alone (two repeated measures) and afterwards in heterosexual pairs (two repeated measures). In these pairs, we simultaneously assessed males' mating efforts by counting the number of sexual behaviours (courtship displays and copulations). Male and female guppies showed consistent individual differences in their swimming activity when tested both alone and in a pair, and these differences were maintained across both test situations. When controlling for male swimming behaviour and both male and female body size, males performed more courtship displays towards females with higher swimming activity. In a second experiment, we tested for a directional male preference for swimming activity by presenting males video animations of low- and high-active females in a dichotomous choice test. In congruence with experiment 1, we found males to spend significantly more time in association with the high-active female stimulus. Both experiments thus point towards a directional male preference for higher activity levels in females. We discuss the adaptive significance of this preference as activity patterns might indicate individual female quality, health or reproductive state while, mechanistically, females that are more active might be more detectable to males as well.

Causal evidence for the adaptive benefits of social foraging in the wild.

Sociality is a fundamental organizing principle across taxa, thought to come with a suite of adaptive benefits. However, making causal inferences about these adaptive benefits requires experimental manipulation of the social environment, which is rarely feasible in the field. Here we manipulated the number of conspecifics in Trinidadian guppies (Poecilia reticulata) in the wild, and quantified how this affected a key benefit of sociality, social foraging, by investigating several components of foraging success. As adaptive benefits of social foraging may differ between sexes, we studied males and females separately, expecting females, the more social and risk-averse sex in guppies, to benefit more from conspecifics. Conducting over 1600 foraging trials, we found that in both sexes, increasing the number of conspecifics led to faster detection of novel food patches and a higher probability of feeding following detection of the patch, resulting in greater individual resource consumption. The extent of the latter relationship differed between the sexes, with males unexpectedly exhibiting a stronger social benefit. Our study provides rare causal evidence for the adaptive benefits of social foraging in the wild, and highlights that sex differences in sociality do not necessarily imply an unequal ability to profit from the presence of others.