An Analysis of Variability in the Feeding Motor Program of the Honey Bee; the Role of Learning in Releasing a Modal Action Pattern

Sequences of behavior are highly predictable (stereotyped) during some segments and less predictable during transitions between those segments. Statistical characterization of behavior must involve observation of the behavior under different stimulus conditions, which includes how stimuli associated with behavioral releasers come to trigger behavior during learning. For example, the feeding motor program (FMP) of the honey bee Apis mellifera (Hymenoptera: Apidae) during proboscis extension can be divided into three response phases (Rehder 1987). We conditioned honey bees in an olfactory conditioning paradigm with one or several rewarded trials during which an odorant was paired with the sugar-water unconditioned stimulus (US); the latter elicits proboscis extension and feeding in properly motivated bees. By recording electromyogram activity from one of the muscles that move the proboscis during feeding, we quantified the bees' responses during an unrewarded test with either the conditioned odorant, a different (novel) odorant, or the sugar-water US. Various parameters of the response phases of the FMP varied in a consistent manner across these experimental treatments, with certain stimuli eliciting stronger, more consistent responses. The different response phases followed one another in time with some variability and statistical uncertainty. For example, the length of an individual licking movement with the glossa was relatively invariant, and may indicate that this parameter can be used to differentiate the FMP into more basic, independent units. Our work shows how learned information may release action patterns in ways slightly different from traditional sign-stimuli releasers.     

Collective animal behavior from Bayesian estimation and probability matching

Animals living in groups make movement decisions that depend, among other factors, on social interactions with other group members. Our present understanding of social rules in animal collectives is mainly based on empirical fits to observations, with less emphasis in obtaining first-principles approaches that allow their derivation. Here we show that patterns of collective decisions can be derived from the basic ability of animals to make probabilistic estimations in the presence of uncertainty. We build a decision-making model with two stages: Bayesian estimation and probabilistic matching. In the first stage, each animal makes a Bayesian estimation of which behavior is best to perform taking into account personal information about the environment and social information collected by observing the behaviors of other animals. In the probability matching stage, each animal chooses a behavior with a probability equal to the Bayesian-estimated probability that this behavior is the most appropriate one. This model derives very simple rules of interaction in animal collectives that depend only on two types of reliability parameters, one that each animal assigns to the other animals and another given by the quality of the non-social information. We test our model by obtaining theoretically a rich set of observed collective patterns of decisions in three-spined sticklebacks, Gasterosteus aculeatus, a shoaling fish species. The quantitative link shown between probabilistic estimation and collective rules of behavior allows a better contact with other fields such as foraging, mate selection, neurobiology and psychology, and gives predictions for experiments directly testing the relationship between estimation and collective behavior.     

Social Behavior of Captive Indochinese and Insular Long-Tailed Macaques (Macaca fascicularis) Following Transfer to a New Facility

There are measurable differences in behavior, physiology, social organization, and geographic distribution within and between various species of macaques. We collected information on the social behavior of captive Macaca fascicularis from Indochina and island populations after they had been transferred to a new environment and new social groups. While some changes in behavior occurred over time, we found no decrease in high levels of agonistic behaviors. We interpret this finding in light of previous research reporting that long-tailed macaques show low levels of habitatuation to novelty and are highly aroused in comparison to other macaque species. We found predictable differences in behavior for males, females, and infants, in which infants played more, females had higher levels of contact proximity to other individuals, and males exhibited more sexual and threat behavior. A comparison of social behavior in long-tailed macaques from different origins indicate that Indochinese macaques are generally less affiliative and Indochinese males are more aggressive than their insular counterparts. Differences among macaque species, and within the fascicularis-group, should be considered in management of captive colonies and when interpreting research data.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Choice of baseline climate data impacts projected species' responses to climate change

Climate data created from historic climate observations are integral to most assessments of potential climate change impacts, and frequently comprise the baseline period used to infer species‐climate relationships. They are often also central to downscaling coarse resolution climate simulations from General Circulation Models (GCMs) to project future climate scenarios at ecologically relevant spatial scales. Uncertainty in these baseline data can be large, particularly where weather observations are sparse and climate dynamics are complex (e.g. over mountainous or coastal regions). Yet, importantly, this uncertainty is almost universally overlooked when assessing potential responses of species to climate change. Here, we assessed the importance of historic baseline climate uncertainty for projections of species' responses to future climate change. We built species distribution models (SDMs) for 895 African bird species of conservation concern, using six different climate baselines. We projected these models to two future periods (2040–2069, 2070–2099), using downscaled climate projections, and calculated species turnover and changes in species‐specific climate suitability. We found that the choice of baseline climate data constituted an important source of uncertainty in projections of both species turnover and species‐specific climate suitability, often comparable with, or more important than, uncertainty arising from the choice of GCM. Importantly, the relative contribution of these factors to projection uncertainty varied spatially. Moreover, when projecting SDMs to sites of biodiversity importance (Important Bird and Biodiversity Areas), these uncertainties altered site‐level impacts, which could affect conservation prioritization. Our results highlight that projections of species' responses to climate change are sensitive to uncertainty in the baseline climatology. We recommend that this should be considered routinely in such analyses.     

Inheritance of Acquired Behaviour Adaptations and Brain Gene Expression in Chickens

Background

Environmental challenges may affect both the exposed individuals and their offspring. We investigated possible adaptive aspects of such cross-generation transmissions, and hypothesized that chronic unpredictable food access would cause chickens to show a more conservative feeding strategy and to be more dominant, and that these adaptations would be transmitted to the offspring.

Methodology/Principal Findings

Parents were raised in an unpredictable (UL) or in predictable diurnal light rhythm (PL, 12∶12 h light∶dark). In a foraging test, UL birds pecked more at freely available, rather than at hidden and more attractive food, compared to birds from the PL group. Female offspring of UL birds, raised in predictable light conditions without parental contact, showed a similar foraging behavior, differing from offspring of PL birds. Furthermore, adult offspring of UL birds performed more food pecks in a dominance test, showed a higher preference for high energy food, survived better, and were heavier than offspring of PL parents. Using cDNA microarrays, we found that the differential brain gene expression caused by the challenge was mirrored in the offspring. In particular, several immunoglobulin genes seemed to be affected similarly in both UL parents and their offspring. Estradiol levels were significantly higher in egg yolk from UL birds, suggesting one possible mechanism for these effects.

Conclusions/Significance

Our findings suggest that unpredictable food access caused seemingly adaptive responses in feeding behavior, which may have been transmitted to the offspring by means of epigenetic mechanisms, including regulation of immune genes. This may have prepared the offspring for coping with an unpredictable environment.     

Outlier Responses Reflect Sensitivity to Statistical Structure in the Human Brain

We constantly look for patterns in the environment that allow us to learn its key regularities. These regularities are fundamental in enabling us to make predictions about what is likely to happen next. The physiological study of regularity extraction has focused primarily on repetitive sequence-based rules within the sensory environment, or on stimulus-outcome associations in the context of reward-based decision-making. Here we ask whether we implicitly encode non-sequential stochastic regularities, and detect violations therein. We addressed this question using a novel experimental design and both behavioural and magnetoencephalographic (MEG) metrics associated with responses to pure-tone sounds with frequencies sampled from a Gaussian distribution. We observed that sounds in the tail of the distribution evoked a larger response than those that fell at the centre. This response resembled the mismatch negativity (MMN) evoked by surprising or unlikely events in traditional oddball paradigms. Crucially, responses to physically identical outliers were greater when the distribution was narrower. These results show that humans implicitly keep track of the uncertainty induced by apparently random distributions of sensory events. Source reconstruction suggested that the statistical-context-sensitive responses arose in a temporo-parietal network, areas that have been associated with attention orientation to unexpected events. Our results demonstrate a very early neurophysiological marker of the brain''s ability to implicitly encode complex statistical structure in the environment. We suggest that this sensitivity provides a computational basis for our ability to make perceptual inferences in noisy environments and to make decisions in an uncertain world.     

An ecological framework of neophobia: from cells to organisms to populations

Neophobia is the fear of novel stimuli or situations. This phenotype has recently received much ecological attention, primarily in the context of decision making. Here, we explore neophobia across biological levels of organisation, first describing types of neophobia among animals and the underlying causes of neophobia, highlighting high levels of risk and uncertainty as key drivers. We place neophobia in the framework of Error Management Theory and Signal Detection Theory, showing how increases in overall risk and uncertainty can lead to costly non‐responses towards novel threats unless individuals lower their response threshold and become neophobic. We then discuss how neophobic behaviour translates into population and evolutionary consequences before introducing neophobia‐like processes at the cellular level, where some phenomena such as allergy and autoimmunity can parallel neophobic behaviour. Finally, we discuss neophobia attenuation, considering how a sudden change in the environment from dangerous to safe can lead to problematic over‐responses (i.e. the ‘maladaptive defensive carry‐over’ hypothesis), and discuss treatment methods for such over‐responses. We anticipate that bridging the concept of neophobia with a process‐centered perspective can facilitate a transfer of insight across organisational levels.     

Asymmetric evolution of egg laying behavior following reciprocal host shifts by a seed-feeding beetle

Colonization of new environments can lead to rapid changes in fitness-related traits. For herbivorous insects, switching to a new host plant can be comparable to invading a new habitat. Behavioral, physiological, and life-history traits commonly vary among insect populations associated with different plants, but how host shifts cause trait divergence is often unclear. We investigated whether experimental host shifts would modify a key insect trait, egg-laying behavior, in a seed beetle. Beetle populations associated long-term with either a small-seeded host (mung bean) or a large-seeded host (cowpea) were switched to each other’s host. After 36–55 generations, we assayed three aspects of oviposition behavior known to differ between the mung bean- and cowpea-adapted populations. Responses to the host shifts were asymmetrical. Females from lines transferred from mung bean to cowpea produced less uniform distributions of eggs among seeds, were more likely to add an egg to an occupied seed, and were more likely to “dump” eggs when seeds were absent. These lines thus converged toward the cowpea-adapted population. In contrast, the reciprocal host shift had no effect; oviposition behavior was unchanged in lines transferred from cowpea to mung bean. We suggest that these results reflect an asymmetry in the fitness consequences of each host shift, which in turn depended on differences in larval competitiveness in the original populations. Interactions among multiple fitness components are likely to make evolutionary responses less predictable in novel environments.     

Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans

The nematode C. elegans is an excellent model organism for studying behavior at the neuronal level. Because of the organism's small size, it is challenging to deliver stimuli to C. elegans and monitor neuronal activity in a controlled environment. To address this problem, we developed two microfluidic chips, the 'behavior' chip and the 'olfactory' chip for imaging of neuronal and behavioral responses in C. elegans. We used the behavior chip to correlate the activity of AVA command interneurons with the worm locomotion pattern. We used the olfactory chip to record responses from ASH sensory neurons exposed to high-osmotic-strength stimulus. Observation of neuronal responses in these devices revealed previously unknown properties of AVA and ASH neurons. The use of these chips can be extended to correlate the activity of sensory neurons, interneurons and motor neurons with the worm's behavior.     

Mass regulation in response to predation risk can indicate population declines

In theory, survival rates and consequent population status might be predictable from instantaneous behavioural measures of how animals prioritize foraging vs. avoiding predation. We show, for the 30 most common small bird species ringed in the UK, that one quarter respond to higher predation risk as if it is mass-dependent and lose mass. Half respond to predation risk as if it only interrupts their foraging and gain mass thus avoiding consequent increased starvation risk from reduced foraging time. These mass responses to higher predation risk are correlated with population and conservation status both within and between species (and independently of foraging habitat, foraging guild, sociality index and size) over the last 30 years in Britain, with mass loss being associated with declining populations and mass gain with increasing populations. If individuals show an interrupted foraging response to higher predation risk, they are likely to be experiencing a high quality foraging environment that should lead to higher survival. Whereas individuals that show a mass-dependent foraging response are likely to be in lower quality foraging environments, leading to relatively lower survival.     

Species Sensitivity Distributions Revisited: A Critical Appraisal

We revisit the assumptions associated with the derivation and application of species sensitivity distributions (SSDs). Our questions are (1) Do SSDs clarify or obscure the setting of ecological effects thresholds for risk assessment? and (2) Do SSDs reduce or introduce uncertainty into risk assessment? Our conclusions are that if we could determine a community sensitivity distribution, this would provide a better estimate of an ecologically relevant effects threshold and therefore be an improvement for risk assessment. However, the distributions generated are typically based on haphazard collections of species and endpoints and by adjusting these to reflect more realistic trophic structures we show that effects thresholds can be shifted but in a direction and to an extent that is not predictable. Despite claims that the SSD approach uses all available data to assess effects, we demonstrate that in certain frequently used applications only a small fraction of the species going into the SSD determine the effects threshold. If the SSD approach is to lead to better risk assessments, improvements are needed in how the theory is put into practice. This requires careful definition of the risk assessment targets and of the species and endpoints selected for use in generating SSDs.     

Identifying the microbial taxa that consistently respond to soil warming across time and space

Soil microbial communities are the key drivers of many terrestrial biogeochemical processes. However, we currently lack a generalizable understanding of how these soil communities will change in response to predicted increases in global temperatures and which microbial lineages will be most impacted. Here, using high‐throughput marker gene sequencing of soils collected from 18 sites throughout North America included in a 100‐day laboratory incubation experiment, we identified a core group of abundant and nearly ubiquitous soil microbes that shift in relative abundance with elevated soil temperatures. We then validated and narrowed our list of temperature‐sensitive microbes by comparing the results from this laboratory experiment with data compiled from 210 soils representing multiple, independent global field studies sampled across spatial gradients with a wide range in mean annual temperatures. Our results reveal predictable and consistent responses to temperature for a core group of 189 ubiquitous soil bacterial and archaeal taxa, with these taxa exhibiting similar temperature responses across a broad range of soil types. These microbial ‘bioindicators’ are useful for understanding how soil microbial communities respond to warming and to discriminate between the direct and indirect effects of soil warming on microbial communities. Those taxa that were found to be sensitive to temperature represented a wide range of lineages and the direction of the temperature responses were not predictable from phylogeny alone, indicating that temperature responses are difficult to predict from simply describing soil microbial communities at broad taxonomic or phylogenetic levels of resolution. Together, these results lay the foundation for a more predictive understanding of how soil microbial communities respond to soil warming and how warming may ultimately lead to changes in soil biogeochemical processes.     

Novelty Responses in a Bird Assemblage Inhabiting an Urban Area

Neophobia, or the hesitancy to approach a novel food item, object, or place, is an important factor influencing the foraging behavior of animals. Environmental factors (e.g. rapid anthropogenic changes, migration into new habitats) are associated with novelty in feeding ecology and may affect neophobic responses. Mechanisms that underlie the differential neophobic response may involve complex interactions with the environment: post-fledging experience in a greater diversity of habitats or in habitats that are more complex may contribute to reduced neophobia. In a previous study, it was observed that some urbanized species, in particular house sparrows ( Passer domesticus ) and shiny cowbirds ( Molothrus bonariensis ) show high levels of neophobia. This study was carried out in a suburban marsh of Cortaderia selloana , a relatively simple and predictable ecosystem as compared to urban areas. For this reason, in the present study, we explored novelty responses of bird species inhabiting an urban area, representing a complex environment. The results were compared to those obtained previously in the suburban marsh. We found unexpectedly high levels of neophobia in house sparrows, but shiny cowbirds showed a somewhat neophilic response. In the presence of novel objects, house sparrows tended to enter the feeders alone, while shiny cowbirds tended to forage in groups. We found no differences in latencies to forage or in visit duration between habitat types, but the proportion of individuals that visited the feeders when novel objects were present was lower in the urban area for house sparrows and eared doves ( Zenaida auriculata ). The results are discussed in the context of invasion success and feeding innovation in shiny cowbirds.     

Where is positional uncertainty a problem for species distribution modelling?

Species data held in museum and herbaria, survey data and opportunistically observed data are a substantial information resource. A key challenge in using these data is the uncertainty about where an observation is located. This is important when the data are used for species distribution modelling (SDM), because the coordinates are used to extract the environmental variables and thus, positional error may lead to inaccurate estimation of the species–environment relationship. The magnitude of this effect is related to the level of spatial autocorrelation in the environmental variables. Using local spatial association can be relevant because it can lead to the identification of the specific occurrence records that cause the largest drop in SDM accuracy. Therefore, in this study, we tested whether the SDM predictions are more affected by positional uncertainty originating from locations that have lower local spatial association in their predictors. We performed this experiment for Spain and the Netherlands, using simulated datasets derived from well known species distribution models (SDMs). We used the K statistic to quantify the local spatial association in the predictors at each species occurrence location. A probabilistic approach using Monte Carlo simulations was employed to introduce the error in the species locations. The results revealed that positional uncertainty in species occurrence data at locations with low local spatial association in predictors reduced the prediction accuracy of the SDMs. We propose that local spatial association is a way to identify the species occurrence records that require treatment for positional uncertainty. We also developed and present a tool in the R environment to target observations that are likely to create error in the output from SDMs as a result of positional uncertainty.     

Landscape influences on climate‐related lake shrinkage at high latitudes

Climate‐related declines in lake area have been identified across circumpolar regions and have been characterized by substantial spatial heterogeneity. An improved understanding of the mechanisms underlying lake area trends is necessary to predict where change is most likely to occur and to identify implications for high latitude reservoirs of carbon. Here, using a population of ca. 2300 lakes with statistically significant increasing and decreasing lake area trends spanning longitudinal and latitudinal gradients of ca. 1000 km in Alaska, we present evidence for a mechanism of lake area decline that involves the loss of surface water to groundwater systems. We show that lakes with significant declines in lake area were more likely to be located: (1) in burned areas; (2) on coarser, well‐drained soils; and (3) farther from rivers compared to lakes that were increasing. These results indicate that postfire processes such as permafrost degradation, which also results from a warming climate, may promote lake drainage, particularly in coarse‐textured soils and farther from rivers where overland flooding is less likely and downslope flow paths and negative hydraulic gradients between surface water and groundwater systems are more common. Movement of surface water to groundwater systems may lead to a deepening of subsurface flow paths and longer hydraulic residence time which has been linked to increased soil respiration and CO₂ release to the atmosphere. By quantifying relationships between statewide coarse resolution maps of landscape characteristics and spatially heterogeneous responses of lakes to environmental change, we provide a means to identify at‐risk lakes and landscapes and plan for a changing climate.     

Corvids avoid odd evaluation by following simple rules in a risky exchange task

In their natural environment, animals often make decisions crucial for survival, such as choosing the best patch or food, or the best partner to cooperate. The choice can be compared to a gamble with an outcome that is predictable but not certain, such as rolling a dice. In economics, such a situation is called a risky context. Several models show that although individuals can generally evaluate the odds of each potential outcome, they can be subject to errors of judgment or choose according to decision-making heuristics (simple decision rules). In non-human primates, similar errors of judgment have been reported and we have recently shown that they also use a decisional heuristics when confronted with a risky choice in an exchange task. This suggests a common evolutionary origin to the mechanisms underlying decision-making under risk in primates. However, whether the same mechanisms are also present in more distantly related taxa needs to be further investigated. Other social species, like corvids, are renowned for their advanced cognitive skills and may show similar responses. Here, we analyse data on corvids (carrion crows, hooded crows, common ravens and rooks) tested in a risky exchange task comparable to the one used in non-human primates. We investigated whether corvids could exchange according to the odds of success or, alternatively, whether they used a heuristic similar to the one used by non-human primates. Instead, most corvids chose a course of action (either a low or high exchange rate) that remained constant throughout the study. In general, corvids’ mean exchange rates were lower compared to non-human primates, indicating that they were either risk-adverse or that they do not possess the cognitive capabilities to evaluate odds. Further studies are required to evaluate the flexibility in exchange abilities of these birds in exchange abilities of these birds.     

Local orientation and the evolution of foraging: changes in decision making can eliminate evolutionary trade-offs

Information processing is a major aspect of the evolution of animal behavior. In foraging, responsiveness to local feeding opportunities can generate patterns of behavior which reflect or "recognize patterns" in the environment beyond the perception of individuals. Theory on the evolution of behavior generally neglects such opportunity-based adaptation. Using a spatial individual-based model we study the role of opportunity-based adaptation in the evolution of foraging, and how it depends on local decision making. We compare two model variants which differ in the individual decision making that can evolve (restricted and extended model), and study the evolution of simple foraging behavior in environments where food is distributed either uniformly or in patches. We find that opportunity-based adaptation and the pattern recognition it generates, plays an important role in foraging success, particularly in patchy environments where one of the main challenges is "staying in patches". In the restricted model this is achieved by genetic adaptation of move and search behavior, in light of a trade-off on within- and between-patch behavior. In the extended model this trade-off does not arise because decision making capabilities allow for differentiated behavioral patterns. As a consequence, it becomes possible for properties of movement to be specialized for detection of patches with more food, a larger scale information processing not present in the restricted model. Our results show that changes in decision making abilities can alter what kinds of pattern recognition are possible, eliminate an evolutionary trade-off and change the adaptive landscape.     

Task Uncertainty Can Account for Mixing and Switch Costs in Task-Switching

Cognitive control is required in situations that involve uncertainty or change, such as when resolving conflict, selecting responses and switching tasks. Recently, it has been suggested that cognitive control can be conceptualised as a mechanism which prioritises goal-relevant information to deal with uncertainty. This hypothesis has been supported using a paradigm that requires conflict resolution. In this study, we examine whether cognitive control during task switching is also consistent with this notion. We used information theory to quantify the level of uncertainty in different trial types during a cued task-switching paradigm. We test the hypothesis that differences in uncertainty between task repeat and task switch trials can account for typical behavioural effects in task-switching. Increasing uncertainty was associated with less efficient performance (i.e., slower and less accurate), particularly on switch trials and trials that afford little opportunity for advance preparation. Interestingly, both mixing and switch costs were associated with a common episodic control process. These results support the notion that cognitive control may be conceptualised as an information processor that serves to resolve uncertainty in the environment.