Marginal value theorem (MVT) is an archetypal model discussed in every behavioural ecology textbook. Its popularity is largely explained but the fact that it is possible to solve it graphically (at least in its simplest form) with the minimal amount of equations, which is a sensible strategy for an introductory course in behavioural ecology [1]. Apart from this heuristic value, one may be tempted to disregard it as a naive toy model. After a burst of interest in the 70's and the 80's, the once vivid literature about optimal foraging theory (OFT) has lost its momentum [2]. Yet, OFT and MVT have remained an active field of research in the parasitoidologists community, mostly because the sampling strategy of a parasitoid in patches of hosts and its resulting fitness gain are straightforward to evaluate, which eases both experimental and theoretical investigations [3].
This preprint [4] is in line with the long-established literature on OFT. It follows two theoretical articles [5,6] in which Vincent Calcagno and co-authors assessed the effect of changes in the environmental conditions on optimal foraging strategy. This time, they did not modify the shape of the gain function (describing the diminishing return of the cumulative intake as a function of the residency time in a patch) but the relative frequencies of good and bad patches. At first sight, that sounds like a minor modification of their earlier models. Actually, even the authors initially were fooled by the similarities before spotting the pitfalls. Here, they genuinely point out the erroneous verbal prediction in their previous paper in which some non-trivial effects of the change in patch frequencies have been overlooked. The present study indeed provides a striking example of ecological fallacy, and more specifically of Simpson's paradox which occurs when the aggregation of subgroups modifies the apparent pattern at the scale of the entire population [7,8]. In the case of MVT under constraints of habitat conversion, the increase of the residency times in both bad and good patches can result in a decrease of the average residency time at the level of the population. This apparently counter-intuitive property can be observed, for instance, when the proportion of bad quality patches strongly increases, which increases the probability that the individual forages on theses quickly exploited patches, and thus decreases its average residency time on the long run.
The authors thus put the model on the drawing board again. Proper assessment of the effect of change in the frequency of patch quality is more mathematically challenging than when one considers only changes in the shape of the gain function. The expected gain must be evaluated at the scale of the entire habitat instead of single patch. Overall, this study, which is based on a rigorous formalism, stands out as a warning against too rapid interpretations of theoretical outputs. It is not straightforward to generalize the predictions of previous models without careful evaluating their underlying hypotheses. The devil is in the details: some slight, seemingly minor, adjustments of the assumptions may have some major consequences.
The authors discussed the general conditions leading to changes in residency times or movement rates. Yet, it is worth pointing out again that it would be a mistake to blindly consider these theoretical results as forecasts for the foragers' behaviour in natura. OFT models has for a long time been criticized for sweeping under the carpet the key questions of the evolutionary dynamics and the maintenance of the optimal strategy in a population [9,10]. The distribution of available options is susceptible to change rapidly due to modifications of the environmental conditions or, even more simply, the presence of competitors which continuously remove the best options from the pool of available options [11]. The key point here is that the constant monitoring of available options implies cognitive (neural tissue is one of the most metabolically expensive tissues) and ecological costs: assessment and adjustment to the environmental conditions requires time, energy, and occasional mistakes (cost of naiveté, [12]). While rarely considered in optimal analyses, these costs should severely constraint the evolution of the subtle decision rules. Under rapidly fluctuating conditions, it could be more profitable to maintain a sub-optimal strategy (but performing reasonably well on the long run) than paying the far from negligible costs implied by the pursuit of optimal strategies [13,14]. For instance, in the analysis presented in this preprint, it is striking how close the fitness gains of the plastic and the non-plastic forager are, particularly if one remembers that the last-mentioned cognitive and ecological costs have been neglected in these calculations.
Yet, even if one can arguably question its descriptive value, such models are worth more than a cursory glance. They still have normative value insofar that they provide upper bounds for the response to modifications of the environmental conditions. Such insights are precious to design future experiments on the question. Being able to compare experimentally measured behaviours with the extremes of the null model (stubborn non-plastic forager) and the optimal strategy (only achievable by an omniscient daemon) informs about the cognitive bias or ecological costs experienced by real life foragers. I thus consider that this model, and more generally most OFT models, are still a valuable framework which deserves further examination.

References

[1] Fawcett, T. W. & Higginson, A. D. 2012 Heavy use of equations impedes communication among biologists. Proc. Natl. Acad. Sci. 109, 11735–11739. doi: 10.1073/pnas.1205259109
[2] Owens, I. P. F. 2006 Where is behavioural ecology going? Trends Ecol. Evol. 21, 356–361. doi: 10.1016/j.tree.2006.03.014
[3] Louâpre, P., Fauvergue, X., van Baaren, J. & Martel, V. 2015 The male mate search: an optimal foraging issue? Curr. Opin. Insect Sci. 9, 91–95. doi: 10.1016/j.cois.2015.02.012
[4] Calcagno, V., Hamelin, F., Mailleret, L., & Grognard, F. (2018). How optimal foragers should respond to habitat changes? On the consequences of habitat conversion. bioRxiv, 273557, ver. 4 peer-reviewed and recommended by PCI Ecol. doi: 10.1101/273557
[5] Calcagno, V., Grognard, F., Hamelin, F. M., Wajnberg, É. & Mailleret, L. 2014 The functional response predicts the effect of resource distribution on the optimal movement rate of consumers. Ecol. Lett. 17, 1570–1579. doi: 10.1111/ele.12379
[6] Calcagno, V., Mailleret, L., Wajnberg, É. & Grognard, F. 2013 How optimal foragers should respond to habitat changes: a reanalysis of the Marginal Value Theorem. J. Math. Biol. 69, 1237–1265. doi: 10.1007/s00285-013-0734-y
[7] Galipaud, M., Bollache, L., Wattier, R., Dechaume-Moncharmont, F.-X. & Lagrue, C. 2015 Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson's paradox. Anim. Behav. 102, 217–221. doi: 10.1016/j.anbehav.2015.01.032
[8] Kievit, R. A., Frankenhuis, W. E., Waldorp, L. J. & Borsboom, D. 2013 Simpson's paradox in psychological science: a practical guide. Front. Psychol. 4, 513. doi: 10.3389/fpsyg.2013.00513
[9] Bolduc, J.-S. & Cézilly, F. 2012 Optimality modelling in the real world. Biol. Philos. 27, 851–869. doi: 10.1007/s10539-012-9333-3
[10] Pierce, G. J. & Ollason, J. G. 1987 Eight reasons why optimal foraging theory is a complete waste of time. Oikos 49, 111–118. doi: 10.2307/3565560
[11] Dechaume-Moncharmont, F.-X., Brom, T. & Cézilly, F. 2016 Opportunity costs resulting from scramble competition within the choosy sex severely impair mate choosiness. Anim. Behav. 114, 249–260. doi: 10.1016/j.anbehav.2016.02.019
[12] Snell-Rood, E. C. 2013 An overview of the evolutionary causes and consequences of behavioural plasticity. Anim. Behav. 85, 1004–1011. doi: 10.1016/j.anbehav.2012.12.031
[13] Fawcett, T. W., Fallenstein, B., Higginson, A. D., Houston, A. I., Mallpress, D. E. W., Trimmer, P. C. & McNamara, J. M. 2014 The evolution of decision rules in complex environments. Trends Cogn. Sci. 18, 153–161. doi: 10.1016/j.tics.2013.12.012
[14] Marshall, J. A. R., Trimmer, P. C., Houston, A. I. & McNamara, J. M. 2013 On evolutionary explanations of cognitive biases. Trends Ecol. Evol. 28, 469-473. doi: 10.1016/j.tree.2013.05.013

In their pre-registered paper [1], McCune and colleagues propose a field-based study of social versus individual learning mechanisms in an avian species (great-tailed grackles) that has been expanding its geographic range. The study forms part of a longer-term project that addresses various aspects of this species’ behaviour and biology, and the experience of the team is clear from the preprint. Assessing variation in learning mechanisms in different sections of the grackles’ distribution range, the researchers will investigate how individual learning and social transmission may impact learning about novel challenges in the environment. Considering that this is a social species, the authors expect both individual learning and social transmission to occur, when groups of grackles encounter new challenges/ opportunities in the wild. This in itself is not a very unusual idea to test [2, 3], but the authors are rigorously distinguishing between imitation, emulation, local enhancement, and social enhancement. Such rigour is certainly valuable in studies of cognition in the wild.
Further, the authors predict that the contribution of individual versus social learning could vary between populations, as the core may contain fewer unfamiliar/novel stimuli than the edge, where artificial sources of water (for example) may be more common. They make an argument that the core, middle, and edge populations would experience differing levels of environmental predictability. If true, their field experiments could yield very novel results on how changes in environmental predictability affect social/individual learning in a single study species. Their data would then give unusual insights into the ecological value of individual learning and distinct forms of social learning – something that is not easy to test in wild animals. The authors consider a variety of alternative hypotheses that may ultimately explain their findings, and clarify their methods and analyses in fine detail. The authors also set out limitations clearly, and give a thorough account of their approaches and thinking.
The reviewers and I have a still-unanswered question, which is central to the study: what is the predictability or unpredictability of the core versus edge environments? Although the authors have explained similarities and distinctions between the different sections of the grackles’ range, their description feels a bit vague -- it's not as rigorous or well-defined as the rest of the paper. Such a lack of definition may be inevitable in the limitations of a preprint, but ultimately it does suggest that there may be real uncertainty about the qualitative differences between the core, edge, and middle environments. The authors do explain that a lack of variation in individual responses to the field experiments would preclude the testing of further hypothesis, but do not mention how a salient lack of variation in novelty/ predictability between the environments could impact their hypotheses.
An assessment/quantification of the rate at which the different populations of grackles encounter novel stimuli would be a cornerstone of the success of this proposed study. Certainly, the authors cannot address this in much more detail during the preprint stage, but they need to consider how to best assess/describe differences before starting the full study. Such an assessment could take the form of either a GIS desktop study (comparing, for example, rates of dam/canal construction in core versus edge sections of the distribution range), or observational/ movement data contrasting how frequently members of core versus edge populations encounter artificial sources of water/food in a given month/year. Considering the long-term nature of the larger project, it is possible that these data are already available, but I am speculating. I would highly recommend that such an assessment be undertaken, beyond the mere mention of expected differences. This would solidify the central idea that there are concrete differences between the environments.
Despite this concern, the authors attended well to the comments and recommendations of the two reviewers – both experts in cognitive ecology. It is a preprint showing clear thinking and a consideration of most of the challenges that may be encountered during the course of the study. My own opinion and the estimations of the two reviewers all underscore the originality and value of this project – this should be a very valuable and potentially novel study. I look forward to seeing the outcomes of the research.

References

[1] McCune, K. B., McElreath, R., and Logan, C. J. (2019). Investigating the use of learning mechanisms in a species that is rapidly expanding its geographic range. In principle recommendation by Peer Community In Ecology. corinalogan.com/Preregistrations/g_sociallearning.html
[2] Benson-Amram, S. and Holekamp, K. E. (2012). Innovative problem solving by wild spotted hyenas. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 4087–4095. doi: 10.1098/rspb.2012.1450
[3] Federspiel, I. G., Boeckle, M., von Bayern, A. M. P. and Emery, N. J. (2019). Exploring individual and social learning in jackdaws (Corvus monedula). Learning & Behavior, 47(3), 258–270. doi: 10.3758/s13420-019-00383-8

In 2015, Brockmeyer et al. [1] suggested that mandrills (Mandrillus sphinx) may accept additional ranging costs to avoid heavily parasitized areas. Following this paper, Bicca-Marques and Calegaro-Marques [2] questioned this interpretation and presented other hypotheses. To summarize, whilst Brockmeyer et al. [1] proposed that elevated daily path length may be a consequence of elevated parasite richness, Bicca-Marques and Calegaro-Marques [2] viewed it as a cause. In this current paper, Charpentier and Kappeler [3] respond to some of the criticisms by Bicca-Marques and Calegaro-Marques and discuss the putative parsimony of the two competing scenarios. The manuscript is interesting and focuses on an important question concerning the discussion about the social organization and home range use in wild mandrills. This answer helps to move this debate forward and should stimulate more empirical studies of the role of environmentally-transmitted parasites in shaping ranging and movement patterns of wild vertebrates. Given the elements this paper brings to the topics, it should have been published in American Journal of Primatology, the journal that published the two previous articles.

References

[1] Brockmeyer, T., Kappeler, P. M., Willaume, E., Benoit, L., Mboumba, S., & Charpentier, M. J. E. (2015). Social organization and space use of a wild mandrill (Mandrillus sphinx) group. American Journal of Primatology, 77(10), 1036–1048. doi: 10.1002/ajp.22439
[2] Bicca-Marques, J. C., & Calegaro-Marques, C. (2016). Ranging behavior drives parasite richness: A more parsimonious hypothesis. American Journal of Primatology, 78(9), 923–927. doi: 10.1002/ajp.22561
[3] Charpentier, M. J., & Kappeler, P. M. (2018). A reply to “Ranging Behavior Drives Parasite Richness: A More Parsimonious Hypothesis.” ArXiv:1805.08151v2 [q-Bio]. Retrieved from http://arxiv.org/abs/1805.08151

Assessing the reliability of the methods we use in actually measuring the intended trait should be one of our first priorities when designing a study – especially when the trait in question is not directly observable and is measured through a proxy. 

This is the case for cognitive traits, which are often quantified through measures of behavioral performance. Behavioral flexibility is of particular interest in the context of great environmental changes that a lot of populations have to experiment. This type of behavioral performance is often measured through reversal learning experiments (Bond 2007). In these experiments, individuals first learn a preference, for example for an object of a certain type of form or color, associated with a reward such as food. The characteristics of the rewarded object then change, and the individuals hence have to learn these new characteristics (to get the reward). The time needed by the individual to make this change in preference has been considered a measure of behavioral flexibility.

Although reversal learning experiments have been widely used, their construct validity to assess behavioral flexibility has not been thoroughly tested. This was the aim of McCune and collaborators' (2023) study, through the test of the repeatability of individual performance within and across contexts of reversal learning, in the great-tailed grackle.

This manuscript presents a post-study of the preregistered study* (Logan et al. 2019) that was peer-reviewed and received an In Principle Recommendation for PCI Ecology (Coulon 2019; the initial preregistration was split into 3 post-studies).
Using 34 great-tailed grackles wild-caught in Tempe, Arizona (USA), the authors tested in aviaries 2 hypotheses:

• First, that the behavioral flexibility measured by reversal learning is repeatable within individuals across sessions of the same experiment;
• Second, that there is repeatability of the measured behavioral flexibility (within individuals) across different types of reversal learning experiments (context).

The first hypothesis was tested by measuring the repeatability of the time needed by individuals to switch color preference in a color reversal learning task (colored tubes), over serial sessions of this task. The second one was tested by measuring the time needed by individuals to switch solutions, within 3 different contexts: (1) colored tubes, (2) plastic and (3) wooden multi-access boxes involving several ways to access food.

Despite limited sample sizes, the results of these experiments suggest that there is both temporal and contextual repeatability of behavioral flexibility performance of great-tailed grackles, as measured by reversal learning experiments.

Those results are a first indication of the construct validity of reversal learning experiments to assess behavioral flexibility. As highlighted by McCune and collaborators, it is now necessary to assess the discriminant validity of these experiments, i.e. checking that a different performance is obtained with tasks (experiments) that are supposed to measure different cognitive abilities.
 
* A pre-registered study is a study in which context, aims, hypotheses and methodologies have been written down as an empirical paper, peer-reviewed and pre-accepted before research is undertaken. Pre-registrations are intended to reduce publication bias and reporting bias.
 
REFERENCES
 
Bond, A. B., Kamil, A. C., & Balda, R. P. (2007). Serial reversal learning and the evolution of behavioral
flexibility in three species of north american corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana,
Aphelocoma californica). Journal of Comparative Psychology, 121 (4), 372. https://doi.org/10.1037/0735-7036.121.4.372

Coulon, A. (2019) Can context changes improve behavioral flexibility? Towards a better understanding of species adaptability to environmental changes. Peer Community in Ecology, 100019. https://doi.org/10.24072/pci.ecology.100019

Logan, CJ, Lukas D, Bergeron L, Folsom M, & McCune, K. (2019).  Is behavioral flexibility related to foraging and social behavior in a rapidly expanding species? In Principle Acceptance by PCI Ecology of the Version on 6 Aug 2019. http://corinalogan.com/Preregistrations/g_flexmanip.html

McCune KB, Blaisdell AP, Johnson-Ulrich Z, Lukas D, MacPherson M, Seitz BM, Sevchik A, Logan CJ (2023) Using repeatability of performance within and across contexts to validate measures of behavioral flexibility. EcoEvoRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/X2R59K

Continuous observation of animal behaviour could be quite a challenge in the field, and the situation becomes even more complicated with aquatic species mostly active at night. In such cases, biologging techniques are real game changers in ecology, behavioural ecology or eco-physiology. An accelerating number of methodological applications of these tools in natural condition are thus published each year [1]. Biologging is not limited to movement ecology. For instance, fine grain information about energy expenditure can be inferred from body acceleration [2], and accelerometers has already proven useful in monitoring reproductive costs in some fish species [3,4]. The first part of the study by Tentelier et al. [5] is in line with this growing literature. It describes measurements of energy expenditure during reproduction in a fish species, Allis shad (Alosa Alosa), based on tail beat frequency and occurrence of spawning acts. The study has been convincingly conducted, and the results are important for fish biologists. But this is not the whole story: the authors added to this otherwise classical study a very original and insightful analysis which deserves closer interest.
Tentelier et al. propose to use static accelerometer to monitor change in body roundness through the reproductive season. These semelparous fish first mature and built up reserves in the Atlantic Ocean and migrate into fresh water to reproduce. Contrary to iteroparous species, female shads do not have to strategically preserve energy for future reproduction. The females die few days after spawning having exhausted their energetic reserves: they typically lose almost half of their body mass during the spawning season. The beautiful idea in this study was to track down information about this dramatic slimming in the accelerometer data. Indeed, the accelerometer was attached on the side of the fish (close to the dorsal fin). A change in its angle with the vertical plane could be correlated with the change in roundness, the angle declining with the female thinning. Accelerometers have already been used to record body posture [6] but, in the present study, the novelty was to monitor the change in body shape.
Unfortunately, the data by Tentelier et al. are inconclusive so far. Broadly speaking, the accelerometer angle recorded declined through the spawning season, indicating an average slimming of the females, but there was no correlation between the change in angle and the mass loss at the individual level. This was partly due to the fact that the dorsal position of the accelerometer was not optimized to measures egg laying whose effects are mostly observable on ventral side.
Yet, this nice idea deserves more scrutiny. The method seems to be sensitive enough to detect inflation of swim bladder, the gas-filled organ helping the fish to control their position in the water column, as the accelerometer angle increased when the fish stayed close to the water surface. Additional works and proper calibration are certainly needed to validate the use of accelerometer angle as a proxy for body roundness. The actual data were not strong enough to justify a standalone publication on the subject, but it would have been shame to lose traces of such analysis and keep it in the file drawer. This is why I strongly support its report as a side question in a broader study. Science progresses not only with neat conclusive studies but also when unexpected (apparently anecdotal) observations stimulate new researches.

References

[1] Börger L, Bijleveld AI, Fayet AL, Machovsky‐Capuska GE, Patrick SC, Street GM and Vander Wal E. (2020) Biologging special feature. J. Anim. Ecol. 89, 6–15. 10.1111/1365-2656.13163
[2] Wilson RP et al. (2020) Estimates for energy expenditure in free‐living animals using acceleration proxies: A reappraisal. J. Anim. Ecol. 89, 161–172. 10.1111/1365-2656.13040
[3] Tsuda Y, Kawabe R, Tanaka H, Mitsunaga Y, Hiraishi T, Yamamoto K and Nashimoto K. (2006) Monitoring the spawning behaviour of chum salmon with an acceleration data logger. Ecol. Freshw. Fish 15, 264–274. 10.1111/j.1600-0633.2006.00147.x
[4] Sakaji H, Hamada K, Naito Y. 2018 Identifying spawning events of greater amberjack using accelerometers. Mar. Biol. Res. 14, 637–641. 10.1080/17451000.2018.1492140
[5] Tentelier C, Bouchard C, Bernardin A, Tauzin A, Aymes J-C, Lange F, Récapet C, Rives J (2020) The dynamics of spawning acts by a semelparous fish and its associated energetic costs. bioRxiv, 436295. doi: 10.1101/436295 ver. 7 peer-reviewed and recommended by PCI Ecology. 10.1101/436295
[6] Brown DD, Kays R, Wikelski M, Wilson R, Klimley AP. 2013 Observing the unwatchable through acceleration logging of animal behavior. Anim. Biotelemetry 1, 20. 10.1186/2050-3385-1-20