Publications by year
In Press
Higginson AD, Munafò M (In Press). Current Incentives for Scientists Lead to Underpowered Studies with Erroneous Conclusions.
PLoS Biology Full text.
Higginson AD (In Press). Identifying reliable fitness proxies for growing animals responding to anthropogenic changes.
Abstract:
Identifying reliable fitness proxies for growing animals responding to anthropogenic changes
ABSTRACTAnthropogenic influences on habitats often affect predation on species by introducing novel predators, supporting additional predators, or reducing animals’ ability to detect or avoid predators. Other changes may reduce the ability of animals to feed, or alter their energy use. An increase in predation risk is assumed to reduce prey populations by increasing mortality, reducing foraging and growth. Often animals don’t appear to have been adversely affected, or may even increase growth rate. However, theoretical predictions that may have been overlooked suggest that optimal foraging rate, mortality rate and growth rate may change in counter-intuitive ways, depending on exactly how predation risk or costs have been increased. Increasing predator density may increase mortality rate when foraging, reduce the safety of refuges, or alter the relationship between vigilance and attack likelihood. Increasing temperature may increase metabolic costs in ectotherms and reduce thermogenesis costs in endotherms, which affects the costs of active foraging and inactivity differently. Here, I review the theory on how predation risk and metabolic costs should affect foraging behaviour, mortality and growth in order to explain the great variation in behavioural responses. I show that in some situations animals may not respond behaviourally even though a change severely affects survival, and the mortality may be a poor metric of the impact of a change on population viability. In other situations a fitness proxy may change dramatically whilst fitness is unaffected due to compensatory changes in behaviour or life history. Other measures may change in a positive way whilst fitness declines. I describe how to identify the situations in the field and thereby make reliable measure of fitness in particular study systems. Overall, this work shows how behavioural theory can help understand the impacts of environmental change and highlights promising directions to better understand and mitigate their effects on ecosystems.
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Higginson A, Fawcett TW, Houston A, McNamara J (In Press). Trust your gut: using physiological states as a source of information is almost as effective as optimal Bayesian learning.
Proceedings of the Royal Society B: Biological SciencesAbstract:
Trust your gut: using physiological states as a source of information is almost as effective as optimal Bayesian learning
Approaches to understanding adaptive behaviour often assume that animals have perfect information about environmental conditions or are capable of sophisticated learning. If such learning abilities are costly, however, natural selection will favour simpler mechanisms for controlling behaviour when faced with uncertain conditions. Here we show that, in a foraging context, a strategy based only on current energy reserves often performs almost as well as a Bayesian learning strategy that integrates all previous experiences to form an optimal estimate of environmental conditions. We find that Bayesian learning gives a strong advantage only if fluctuations in the food supply are very strong and reasonably frequent. The performance of both the Bayesian and the reserve-based strategy are more robust to inaccurate knowledge of the temporal pattern of environmental conditions than a strategy that has perfect knowledge about current conditions. Studies assuming Bayesian learning are often accused of being unrealistic; our results suggest that animals can achieve a similar level of performance to Bayesians using much simpler mechanisms based on their physiological state. More broadly, our work suggests that the ability to use internal states as a source of information about recent environmental conditions will have weakened selection for sophisticated learning and decision-making systems.
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2018
Kennedy P, Higginson AD, Radford AR, Sumner S (2018). Altruism in a volatile world.
Nature Full text.
2017
Rosenström T, Fawcett TW, Higginson AD, Metsä-Simola N, Hagen EH, Houston AI, Martikainen P (2017). Adaptive and non-adaptive models of depression: a comparison using register data on antidepressant medication during divorce.
PLoS ONE,
12, e0179495-e0179495.
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Higginson AD (2017). Conflict over non-partitioned resources may explain between-species differences in declines: the anthropogenic competition hypothesis.
Behavioral Ecology and Sociobiology,
71(7).
Abstract:
Conflict over non-partitioned resources may explain between-species differences in declines: the anthropogenic competition hypothesis
© 2017, the Author(s). Abstract: Human alterations of habitats are causing declines in many species worldwide. The extent of declines varies greatly among closely related species, for often unknown reasons that must be understood in order to maintain biodiversity. An overlooked factor is that seasonally breeding species compete for nest sites, which are increasingly limited in many anthropogenically degraded environments. I used evolutionary game theory to predict the outcome of competition between individuals that differ in their competitive ability and timing of nesting. A range of species following evolutionarily stable strategies can co-exist when there are sufficient nest sites, but my model predicts that a reduction in nest site availability has greater impacts on late-nesting species, especially the stronger competitors, whereas early-nesting, stronger species decline only slightly. These predictions are supported by data on 221 bird and 43 bumblebee species worldwide. Restoration and provision of nest sites should be an urgent priority in conservation efforts. More broadly, these results indicate a new ecological principle of potentially widespread importance: rapid reductions in the abundance of resources for which species’ preferences have not diversified will result in unprecedented conflicts that reduce the potential for species co-existence. Significance statement: Understanding the causes of species declines is crucial to preventing the losses. Whilst much work on species vulnerability shows broad scale effects, an enduring mystery is the variation in population trends between closely related species. I combined evolutionary modelling with three global-scale long-term data sets to reveal that competition for scarce nest sites causes variation in declines. The impact of the loss of nest sites on differential declines among closely related species from very different taxa indicates a new ecological principle of widespread importance: the effect of habitat degradation on competition among species. A lack of differentiation of nest site preferences means that—now nest sites are more limited—some species may be driving others to extinction. This phenomenon is likely to occur for any other non-partitioned resources that rapidly, on an evolutionary timescale, are now limiting population sizes.
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Ito K, McNamara JM, Yamauchi A, Higginson AD (2017). The evolution of cooperation by negotiation in a noisy world.
J Evol Biol,
30(3), 603-615.
Abstract:
The evolution of cooperation by negotiation in a noisy world.
Cooperative interactions among individuals are ubiquitous despite the possibility of exploitation by selfish free riders. One mechanism that may promote cooperation is 'negotiation': individuals altering their behaviour in response to the behaviour of others. Negotiating individuals decide their actions through a recursive process of reciprocal observation, thereby reducing the possibility of free riding. Evolutionary games with response rules have shown that infinitely many forms of the rule can be evolutionarily stable simultaneously, unless there is variation in individual quality. This potentially restricts the conditions under which negotiation could maintain cooperation. Organisms interact with one another in a noisy world in which cooperative effort and the assessment of effort may be subject to error. Here, we show that such noise can make the number of evolutionarily stable rules finite, even without quality variation, and so noise could help maintain cooperative behaviour. We show that the curvature of the benefit function is the key factor determining whether individuals invest more or less as their partner's investment increases, investing less when the benefit to investment has diminishing returns. If the benefits of low investment are very small then behavioural flexibility tends to promote cooperation, because negotiation enables cooperators to reach large benefits. Under some conditions, this leads to a repeating cycle in which cooperative behaviour rises and falls over time, which may explain between-population differences in cooperative behaviour. In other conditions, negotiation leads to extremely high levels of cooperative behaviour, suggesting that behavioural flexibility could facilitate the evolution of eusociality in the absence of high relatedness.
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Halpin CG, Skelhorn J, Rowe C, Ruxton GD, Higginson AD (2017). The impact of detoxification costs and predation risk on foraging: Implications for mimicry dynamics.
PLoS ONE,
12(1).
Abstract:
The impact of detoxification costs and predation risk on foraging: Implications for mimicry dynamics
© 2017 Halpin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Prey often evolve defences to deter predators, such as noxious chemicals including toxins. Toxic species often advertise their defence to potential predators by distinctive sensory signals. Predators learn to associate toxicity with the signals of these so-called aposematic prey, and may avoid them in future. In turn, this selects for mildly toxic prey to mimic the appearance of more toxic prey. Empirical evidence shows that mimicry could be either beneficial ('Mullerian') or detrimental ('quasi-Batesian') to the highly toxic prey, but the factors determining which are unknown. Here, we use state-dependent models to explore how tritrophic interactions could influence the evolution of prey defences. We consider how predation risk affects predators' optimal foraging strategies on aposematic prey, and explore the resultant impact this has on mimicry dynamics between unequally defended species. In addition, we also investigate how the potential energetic cost of metabolising a toxin can alter the benefits to eating toxic prey and thus impact on predators' foraging decisions. Our model predicts that both how predators perceive their own predation risk, and the cost of detoxification, can have significant, sometimes counterintuitive, effects on the foraging decisions of predators. For example, in some conditions predators should: (i) avoid prey they know to be undefended, (ii) eat more mildly toxic prey as detoxification costs increase, (iii) increase their intake of highly toxic prey as the abundance of undefended prey increases. These effects mean that the relationship between a mimic and its model can qualitatively depend on the density of alternative prey and the cost of metabolising toxins. In addition, these effects are mediated by the predators' own predation risk, which demonstrates that, higher trophic levels than previously considered can have fundamental impacts on interactions among aposematic prey species.
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Higginson AD, McNamara JM, Dall SRX (2017). Towards a behavioural ecology of obesity.
Behavioral and Brain Sciences,
40, e118-e118.
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2016
English S, Fawcett TW, Higginson AD, Trimmer PC, Uller T (2016). Adaptive Use of Information during Growth can Explain Long-Term Effects of Early Life Experiences.
The American Naturalist,
187(5), 620-632.
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Higginson AD, McNamara JM (2016). An adaptive response to uncertainty can lead to weight gain during dieting attempts.
Evolution, Medicine, and Public Health,
2016(1), 369-380.
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Higginson AD, Fawcett TW (2016). Comment on 'Are physicists afraid of mathematics?'.
New Journal of Physics Full text.
Higginson AD, McNamara JM, Houston AI (2016). Fatness and fitness: Exposing the logic of evolutionary explanations for obesity.
Proceedings of the Royal Society B: Biological Sciences,
283(1822), 1-9.
Abstract:
Fatness and fitness: Exposing the logic of evolutionary explanations for obesity
© 2016 the Author(s) Published by the Royal Society. All rights reserved. To explore the logic of evolutionary explanations of obesity we modelled food consumption in an animal that minimizes mortality (starvation plus predation) by switching between activities that differ in energy gain and predation. We show that if switching does not incur extra predation risk, the animal should have a single threshold level of reserves above which it performs the safe activity and below which it performs the dangerous activity. The value of the threshold is determined by the environmental conditions, implying that animals should have variable ‘set points’. Selection pressure to prevent energy stores exceeding the optimal level is usually weak, suggesting that immediate rewards might easily overcome the controls against becoming overweight. The risk of starvation can have a strong influence on the strategy even when starvation is extremely uncommon, so the incidence of mortality during famine in human history may be unimportant for explanations for obesity. If there is an extra risk of switching between activities, the animal should have two distinct thresholds: one to initiate weight gain and one to initiate weight loss. Contrary to the dual intervention point model, these thresholds will be inter-dependent, such that altering the predation risk alters the location of both thresholds; a result that undermines the evolutionary basis of the drifty genes hypothesis. Our work implies that understanding the causes of obesity can benefit from a better understanding of how evolution shapes the mechanisms that control body weight.
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Higginson AD, Fawcett TW (2016). Statistical Analysis of the Effect of Equations on Citations.
Abstract:
Statistical Analysis of the Effect of Equations on Citations
Statistical analysis of a data set of number of equations and number of citations of papers published in volumes 94 and 104 of the journal Physical Review Letters. This analysis is referred to by the paper Equation-dense papers receive fewer citations—in physics as well as biology in the New Journal of Physics (vol. 18, article 118003) by Andrew D Higginson and Tim W Fawcett. http://iopscience.iop.org/article/10.1088/1367-2630/18/11/118003
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Mcnamara JM, Higginson AD, Verhulst S (2016). The influence of the starvation-predation trade-off on the relationship between ambient temperature and body size among endotherms.
Journal of Biogeography,
43(4), 809-819.
Abstract:
The influence of the starvation-predation trade-off on the relationship between ambient temperature and body size among endotherms
© 2016 John Wiley. &. Sons Ltd. Aim: the tendency for animals at higher latitudes to be larger (Bergmann's rule) is generally explained by recourse to latitudinal effects on ambient temperature and the food supply, but these receive only mixed support and do not explain observations of the inverse to Bergmann's rule. Our aim was to better understand how ecological variables might influence body size and thereby explain this mixed support. Location: World-wide. Methods: Previous explanations do not allow for the selective pressure exerted by the trade-off between predation and starvation, which we incorporate in a model of optimal body size and energy storage of a generalized homeotherm. In contrast to existing arguments, we concentrate on survival over winter when the food supply is poor and can be interrupted for short periods. Results: We use our model to assess the logical validity of the heat conservation hypothesis and show that it must allow for the roles of both food availability and predation risk. We find that whether the effect of temperature on body size is positive or negative depends on temperature range, predator density, and the likelihood of long interruptions to foraging. Furthermore, changing day length explains differing effects of altitude and latitude on body size, leading to opposite predictions for nocturnal and diurnal endotherms. Food availability and ambient temperature can have counteracting selective pressures on body mass, and can lead to a non-monotonic relationship between latitude and size, as observed in several studies. Main conclusions: Our work provides a theoretical framework for understanding the relationships between the costs and benefits of large body size and eco-geographical patterns among endotherms world-wide.
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2015
Trimmer PC, Higginson AD, Fawcett TW, McNamara JM, Houston AI (2015). Adaptive learning can result in a failure to profit from good conditions: implications for understanding depression.
Evol Med Public Health,
2015(1), 123-135.
Abstract:
Adaptive learning can result in a failure to profit from good conditions: implications for understanding depression.
BACKGROUND AND OBJECTIVES: Depression is a major medical problem diagnosed in an increasing proportion of people and for which commonly prescribed psychoactive drugs are frequently ineffective. Development of treatment options may be facilitated by an evolutionary perspective; several adaptive reasons for proneness to depression have been proposed. A common feature of many explanations is that depressive behaviour is a way to avoid costly effort where benefits are small and/or unlikely. However, this viewpoint fails to explain why low mood persists when the situation improves. We investigate whether a behavioural rule that is adapted to a stochastically changing world can cause inactivity which appears similar to the effect of depression, in that it persists after the situation has improved. METHODOLOGY: We develop an adaptive learning model in which an individual has repeated choices of whether to invest costly effort that may result in a net benefit. Investing effort also provides information about the current conditions and rates of change of the conditions. RESULTS: an individual following the optimal behavioural strategy may sometimes remain inactive when conditions are favourable (i.e. when it would be better to invest effort) when it is poorly informed about the current environmental state. Initially benign conditions can predispose an individual to inactivity after a relatively brief period of negative experiences. CONCLUSIONS AND IMPLICATIONS: Our approach suggests that the antecedent factors causing depressed behaviour could go much further back in an individual s history than is currently appreciated. The insights from our approach have implications for the ongoing debate about best treatment options for patients with depressive symptoms.
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McNamara JM, Houston AI, Higginson AD (2015). Costs of foraging predispose animals to obesity-related mortality when food is constantly abundant.
PLoS ONE,
10(11).
Abstract:
Costs of foraging predispose animals to obesity-related mortality when food is constantly abundant
© 2015 McNamara et al.This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Obesity is an important medical problem affecting humans and animals in the developed world, but the evolutionary origins of the behaviours that cause obesity are poorly understood. The potential role of occasional gluts of food in determining fat-storage strategies for avoiding mortality have been overlooked, even though animals experienced such conditions in the recent evolutionary past and may follow the same strategies in the modern environment. Humans, domestic, and captive animals in the developed world are exposed to a surplus of calorie-rich food, conditions characterised as 'constant-glut'. Here, we use a mathematical model to demonstrate that obesity-related mortality from poor health in a constant-glut environment should equal the average mortality rate in the 'pre-modern' environment when predation risk was more closely linked with foraging. It should therefore not be surprising that animals exposed to abundant food often over-eat to the point of ill-health. Our work suggests that individuals tend to defend a given excessive level of reserves because this level was adaptive when gluts were short-lived. The model predicts that mortality rate in constant-glut conditions can increase as the assumed health cost of being overweight decreases, meaning that any adaptation that reduced such health costs would have counter-intuitively led to an increase in mortality in the modern environment. Taken together, these results imply that efforts to reduce the incidence of obesity that are focussed on altering individual behaviour are likely to be ineffective because modern, constant-glut conditions trigger previously adaptive behavioural responses.
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Higginson AD, Fawcett TW, Houston AI (2015). Evolution of a flexible rule for foraging that copes with environmental variation.
Current Zoology,
61(2), 303-312.
Abstract:
Evolution of a flexible rule for foraging that copes with environmental variation
© 2015 Current Zoology. Models of adaptive behaviour typically assume that animals behave as though they have highly complex, detailed strategies for making decisions. In reality, selection favours the optimal balance between the costs and benefits of complexity. Here we investigate this trade-off for an animal that has to decide whether or not to forage for food - and so how much energy reserves to store - depending on the food availability in its environment. We evolve a decision rule that controls the target reserve level for different ranges of food availability, but where increasing complexity is costly in that metabolic rate increases with the sensitivity of the rule. The evolved rule tends to be much less complex than the optimal strategy but performs almost as well, while being less costly to implement. It achieves this by being highly sensitive to changing food availability at low food abun-dance - where it provides a close fit to the optimal strategy - but insensitive when food is plentiful. When food availability is high, the target reserve level that evolves is much higher than under the optimal strategy, which has implications for our under-standing of obesity. Our work highlights the important principle of generalisability of simple decision-making mechanisms, which enables animals to respond reasonably well to conditions not directly experienced by themselves or their ancestors.
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Higginson AD, Speed MP, Ruxton GD (2015). Florivory as an Opportunity Benefit of Aposematism. The American Naturalist, 186(6), 728-741.
Higginson AD, Ruxton GD (2015). Foraging mode switching: the importance of prey distribution and foraging currency.
Animal Behaviour,
105, 121-137.
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Fawcett TW, Marshall JAR, Higginson AD (2015). The evolution of mechanisms underlying behaviour.
Current Zoology,
61(2), 221-225.
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Higginson AD, Houston AI (2015). The influence of the food–predation trade-off on the foraging behaviour of central-place foragers.
Behavioral Ecology and Sociobiology,
69(4), 551-561.
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Wilkinson GS, Breden F, Mank JE, Ritchie MG, Higginson AD, Radwan J, Jaquiery J, Salzburger W, Arriero E, Barribeau SM, et al (2015). The locus of sexual selection: moving sexual selection studies into the post-genomics era.
J Evol Biol,
28(4), 739-755.
Abstract:
The locus of sexual selection: moving sexual selection studies into the post-genomics era.
Sexual selection drives fundamental evolutionary processes such as trait elaboration and speciation. Despite this importance, there are surprisingly few examples of genes unequivocally responsible for variation in sexually selected phenotypes. This lack of information inhibits our ability to predict phenotypic change due to universal behaviours, such as fighting over mates and mate choice. Here, we discuss reasons for this apparent gap and provide recommendations for how it can be overcome by adopting contemporary genomic methods, exploiting underutilized taxa that may be ideal for detecting the effects of sexual selection and adopting appropriate experimental paradigms. Identifying genes that determine variation in sexually selected traits has the potential to improve theoretical models and reveal whether the genetic changes underlying phenotypic novelty utilize common or unique molecular mechanisms. Such a genomic approach to sexual selection will help answer questions in the evolution of sexually selected phenotypes that were first asked by Darwin and can furthermore serve as a model for the application of genomics in all areas of evolutionary biology.
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2014
Fawcett TW, Fallenstein B, Higginson AD, Houston AI, Mallpress DEW, Trimmer PC, McNamara JM, Grp MAD (2014). The evolution of decision rules in complex environments.
TRENDS IN COGNITIVE SCIENCES,
18(3), 153-161.
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Higginson AD, McNamara JM, Houston AI (2014). The starvation–predation trade-off shapes the strategic use of protein for energy during fasting. Journal of Theoretical Biology, 359, 208-219.
2012
Higginson AD, Fawcett TW, Trimmer PC, McNamara JM, Houston AI (2012). Generalized Optimal Risk Allocation: Foraging and Antipredator Behavior in a Fluctuating Environment.
AMERICAN NATURALIST,
180(5), 589-603.
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Fawcett TW, Higginson AD (2012). Heavy use of equations impedes communication among biologists.
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA,
109(29), 11735-11739.
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Houston AI, Trimmer PC, Fawcett TW, Higginson AD, Marshall JAR, McNamara JM (2012). Is optimism optimal? Functional causes of apparent behavioural biases.
BEHAVIOURAL PROCESSES,
89(2), 172-178.
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Fawcett TW, Higginson AD (2012). Reply to Chitnis and Smith, Fernandes, Gibbons, and Kane: Communicating theory effectively requires more explanation, not fewer equations.
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA,
109(45), E3058-E3059.
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2010
Higginson AD, Ruxton GD, Skelhorn J (2010). The impact of flower-dwelling predators on host plant reproductive success.
Oecologia,
164(2), 411-421.
Abstract:
The impact of flower-dwelling predators on host plant reproductive success.
Flowers attract insects and so are commonly exploited as foraging sites by sit-and-wait predators. Such predators can be costly to their host plant by consuming pollinators. However, sit-and-wait predators are often prey generalists that also consume plant antagonists such as herbivores, nectar robbers and granivores, so may also provide benefits to their host plant. Here we present a simple, but general, model that provides novel predictions about how costs and benefits interact in different ecological circumstances. The model predicts that the ecological conditions in which flower-dwelling predators are found can generate either net benefits to their host plants, net costs to their host plants, or can have no effect on the fitness of their host plants. The net effect is influenced by the relative densities of mutualists and antagonists. The flower-dwelling predator has a strong positive effect on the plant if both the pollinators and the granivores are at high density. Further, the range of density combinations that yield a positive net outcome for the plant increases if the performance of pollinators is negatively density dependent, if the predator is only moderately effective at influencing flower visitor rates by its potential prey, and if pollinators are very effective. If plants of a given species find themselves consistently in conditions where they benefit from the presence of a predator then we predict that natural selection could favour the evolution of plant traits that increase the likelihood of predator recruitment and retention, especially where plants are served by highly effective pollinators.
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