Explore and move: a key to success in a changing world?
Does space use behavior relate to exploration in a species that is rapidly expanding its geographic range?
Changes in the spatial range of many species are one of the major consequences of the profound alteration of environmental conditions due to human activities. Some species expand, sometimes spectacularly during invasions; others decline; some shift. Because these changes result in local biodiversity loss (whether local species go extinct or are replaced by colonizing ones), understanding the factors driving spatial range dynamics appears crucial to predict biodiversity dynamics. Identifying the factors that shape individual movement is a main step towards such understanding. The study described in this preregistration (McCune et al. 2020) falls within this context by testing possible links between individual exploration behaviour and movements related to daily space use in an avian study model currently rapidly expanding, the great-tailed grackle (Quiscalus mexicanus).
Movement and exploration: which direction(s) for the link between exploration and dispersal?
Individuals are known to differ in their tendency to explore the environment (Réale et al. 2007; Wolf and Weissing 2012) and therefore in their motivation to move. Accordingly, exploration has been shown to relate to dispersal behaviour, i.e. movements between breeding sites (Dingemanse et al. 2003, Le Galliard et al. 2011, Rasmussen and Belk 2012; reviews in Cote et al. 2010, Ronce et al. 2012). Yet, the mechanisms underlying this link often remain unclear, due to the correlative nature of the data. A classical assumption is that dispersers may benefit from a high capacity to explore, allowing them to familiarize quicker with their new environment once reached, thus alleviating dispersal costs (Bonte et al. 2012). The association between dispersal and exploration would in this case result from selection for this combination of traits (Ronce et al. 2012), even though dispersal event itself may be independent from (and precede the effect of) exploration behaviour. Alternatively (but not exclusively), dispersal may simply be the final outcome of longer movements by individuals exploring larger ranges (Badyaev et al. 1996, Schliehe-Diecks et al. 2012). In the absence of easy ways to manipulate dispersal behaviour, on the one hand, and exploration tendency, on the other hand, investigating detailed, small-scale individual movements in relation to exploration should thus shed light on which processes may yield the observed relations between exploration as an individual personality trait and large-scale, long-term movements, such as dispersal, underlying species range dynamics.
In this project, the exploration behaviour of grackles will be measured in controlled conditions using standardized tests in captivity (McCune et al. 2019) before individuals are released and their daily space use behaviour will then be measured using remote tracking over long time periods (McCune et al. 2020). Importantly, these coupled measures will be obtained for individuals captured in three different populations: within the historical range of the species, in the middle of its expanding range and at the edge of the range (McCune et al. 2020). Therefore, the project will test (i) whether daily space use of individuals is linked to their intrinsic exploration tendency and (ii) whether space use differs between individuals from different populations along the expanding range. The preregistration echoes a complementary project by the same team that will focus on exploration and test (iii) whether exploration tendency differs between individuals from these different populations. Taken together, these three analyses will therefore provide solid background information to assess the role of exploration in the individuals’ decisions leading to movement and range dynamics in this species.
As underlined in the preregistration, previous studies addressing the links between individual exploration behaviour and movements have mostly focused on dispersal. A first type of studies have (as will be done here) measured exploration behaviour of individuals, often in captivity (Dingemanse et al. 2003, Korsten et al. 2013) but also in the wild (Rasmussen and Belk 2012, Debeffe et al. 2013), and related these measures to subsequent dispersal behaviour. The (often implicit) underlying assumption is that more exploratory individuals will be more likely to move further, explore different habitats and thus end up breeding farther than less explorative ones. In other words, exploration tendency precedes and drives dispersal. Sometimes, exploratory behaviour is measured on individuals of known dispersal status, i.e. after the dispersal event (Hoset et al. 2011), in which case selection for certain exploration phenotypes among dispersers may already have occurred. Besides this first approach, another type of studies have measured ‘exploration’ behaviour under the form of prospecting movements of individuals and linked these movements to subsequent dispersal (often in the context of habitat selection). While these studies were in the past based on direct thus potentially biased observations (Reed et al. 1999), they now rely more and more on technological advances using (miniaturized) remote tracking devices (Ponchon et al. 2013) that provide far more complete and unbiased movement data, and sometimes also complementary measures of individuals’ internal state. In this case, the implicit assumption is that individuals prospecting farther and/or in more habitat patches will be more likely to settle in a site located farther away from their departure site, because of a more exhaustive sampling of possible sites allowing individuals to identify higher-quality sites (Badyaev et al. 1996). In other words, exploration tendency would not directly lead to higher movements or longer distances, but would allow individuals to optimize their habitat choice among more numerous options, thus leading to an increased dispersal probability or distance; the relation between exploration and dispersal would thus be indirect. Prospecting studies address more closely the underlying mechanisms of movement; however, they cannot easily separate intrinsic individual exploratory tendency from the prospecting movements themselves, with potential feedback effects of the information already gathered on future exploration of other sites or patches, thus on subsequent movements.
By focusing on individual daily space use movements as a mechanistic approach to understand large-scale movements potentially involved in colonization and range expansion, the grackle study described in this preregistration (McCune et al. 2020) will thus contribute to bridge the knowledge gaps between exploration and dispersal. By linking exploration measures obtained from a battery of standardized tests conducted in controlled conditions to individual daily space use and movements recorded in the wild, the grackle project is set in between previous studies addressing the links between exploration and dispersal: it will document exploration in a separate and independent context with respect to the movements themselves, and it will use a mechanistic view of detailed movements by the same individuals in the wild to explore potential implications for dispersal and range expansion. Testing differences between the three study populations over the species range will indeed inform about potential large-scale, population implications of among-individual variation in the link between exploration and movements. Because this study will only measure already settled adult individuals whose previous history is unknown, there will nevertheless be no direct possible exploration of the link with either previous or subsequent dispersal behaviour. Thus, the potential links studied here relate more directly to post-dispersal benefits of exploration for an optimal exploitation of the new environment. Yet, if exploration is a life-long personality trait linked to daily movement patterns, it may also relate to natal dispersal movements in young individuals.
Evolutionary and conservation perspectives
If the results of the project reveal that exploration tendency and daily space use movements are indeed linked, and that individuals from populations across the species range differ in these traits, new questions will emerge. A first question would be whether such among-individual differences are at the origin of range expansion or rather one of its consequences since, again, we deal with correlative data here. In other words, individuals may differ in exploration tendency, and this may confer them different ability to move around, find and colonize new habitats; or individuals may show differences in exploration following arrival in a new habitat, either because more explorative individuals gain fitness benefits and are thus selected, or because of behavioural plasticity and post-colonization adjustment of exploration behaviour when facing new ecological and social conditions in the new environment. Another open question relates to the link between daily space use and dispersal: is dispersal a by-product of higher daily movements that allow individuals to discover new favorable places where to settle? Exploring this link could involve measuring just fledged individuals before natal dispersal occurs and/or individuals chosen according to their own dispersal history, and this would then imply long-term population monitoring as an efficient (but constraining) tool to address such questions. Finally, assessing the fitness consequences of the link between exploration and space use behaviour, and whether these consequences differ between populations along the range expansion, would also be needed to understand the contribution of this link to the invasion success of this species.
The study model chosen for this project is a rapidly expanding species. Importantly, however, and as emphasized in the preregistration, documenting links between exploration and daily space use patterns as well as differences between populations with different trajectories can provide crucial information in general to understand population persistence in response to global climate and landscape changes, both regarding invasion ability or extinction risk. The information should be key to assess the probability that a species may decline, persist or expand in studies addressing biodiversity and community dynamics in a changing world.
Badayev, A. V., Martin, T. E and Etges, W. J. 1996. Habitat sampling and habitat selection by female wild turkeys: ecological correlates and reproductive consequences. Auk 113: 636-646. doi: https://doi.org/10.2307/4088984
Bonte, D. et al. 2012. Costs of dispersal. Biological Reviews 87: 290-312. doi: https://doi.org/10.1111/j.1469-185X.2011.00201.x
Cote, J., Clobert, J., Brodin, T., Fogarty, S. and Sih, A. 2010. Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philosophical Transactions of the Royal Society B 365: 4065-4576. doi: https://doi.org/10.1098/rstb.2010.0176
Debeffe, L., Morellet, N., Cargnelutti, B., Lourtet, B., Coulon, A., Gaillard, J.-M., Bon, R. and Hewison A. J. M. 2013. Exploration as a key component of natal dispersal: dispersers explore more than philopatric individuals in roe deer. Animal Behaviour 86: 143-151. doi: https://doi.org/10.1016/j.anbehav.2013.05.005
Dingemanse, N. J., Both, C., van Noordwijk, A. J., Rutten, A. L. and Drent, P. J. 2003. Natal dispersal and personalities in great tits (Parus major). Proceedings of the Royal Society B 270: 741-747. doi: https://doi.org/10.1098/rspb.2002.2300
Hoset, K. S., Ferchaud, A.-L., Dufour, F., Mersch, D., Cote, J. and Le Galliard, J.-F. 2011. Natal dispersal correlates with behavioral traits that are not consistent across early life stages. Behavioral Ecology 22: 176–183. doi: https://doi.org/10.1093/beheco/arq188
Korsten, P., van Overveld, T., Adriaensen, F. and Matthysen, E. 2013. Genetic integration of local dispersal and exploratory behaviour in a wild bird. Nature Communications 4: 2362. doi: https://doi.org/10.1038/ncomms3362
Le Galliard, J.-F., Rémy, A., Ims, R. A. and Lambin, X. 2011. Patterns and processes of dispersal behaviour in arvicoline rodents. Molecular Ecology 21: 505-523. doi: https://doi.org/10.1111/j.1365-294X.2011.05410.x
McCune K, Ross C, Folsom M, Bergeron L, Logan CJ. 2020. Does space use behavior relate to exploration in a species that is rapidly expanding its geographic range? http://corinalogan.com/Preregistrations/gspaceuse.html In principle acceptance by PCI Ecology of the version on 23 Sep 2020 https://github.com/corinalogan/grackles/blob/master/Files/Preregistrations/gspaceuse.Rmd.
McCune K, MacPherson M, Rowney C, Bergeron L, Folsom M, Logan CJ. 2019. Is behavioral flexibility linked with exploration, but not boldness, persistence, or motor diversity? (http://corinalogan.com/Preregistrations/gexploration.html) In principle acceptance by PCI Ecology of the version on 27 Mar 2019 https://github.com/corinalogan/grackles/blob/master/Files/Preregistrations/gexploration.Rmd
Ponchon, A., Grémillet, D., Doligez, B., Chambert, T., Tveraa, T., González-Solís, J. and Boulinier, T. 2013. Tracking prospecting movements involved in breeding habitat selection: insights, pitfalls and perspectives. Methods in Ecology and Evolution 4: 143-150. doi: https://doi.org/10.1111/j.2041-210x.2012.00259.x
Rasmussen, J. E. and Belk, M. C. 2012. Dispersal behavior correlates with personality of a North American fish. Current Zoology 58: 260–270. doi: https://doi.org/10.1093/CZOOLO%2F58.2.260
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. 2007. Integrating animal temperament within ecology and evolution. Biological Reviews 82: 291-318. doi: https://doi.org/10.1111/j.1469-185x.2007.00010.x
Reed, J. M., Boulinier, T., Danchin, E. and Oring, L. W. 1999. Informed dispersal: prospecting by birds for breeding sites. Current Ornithology 15: 189-259. doi: https://doi.org/10.1007/978-1-4757-4901-4_5
Ronce, O. and Clobert, J. 2012. Dispersal syndromes. pp. 119-138 In Dispersal Ecology and Evolution (eds. Clobert, J., Baguette, M., Benton, T. G. and Bullock, J. M.), pp. 119-138. Oxford University Press.
Schliehe-Diecks, S., Eberle, M. and Kappeler, P. M. 2012. Walk the line - dispersal movements of gray mouse lemurs (Microcebus murinus). Behavioral Ecology and Sociobiology 66: 1175-1185. doi: https://dx.doi.org/10.1007%2Fs00265-012-1371-y
Wolf, M. and Weissing, F. J. 2012. Animal personalities: consequences for ecology and evolution. Trends in Ecology and Evolution 27: 452-461. doi: https://doi.org/10.1016/j.tree.2012.05.001
Blandine Doligez (2020) Explore and move: a key to success in a changing world?. Peer Community in Ecology, 100058. 10.24072/pci.ecology.100058
Revision round #417 Sep 2020
Decision round #4
Thank you very much for the changes made in the manuscript, especially in the introduction section to put the focus on the biological context of the study rather than on the methods. To me, it is now as close as possible to the introduction of a “standard” paper. I understand the authors’ willingness for not changing this introduction a posteriori in the future resulting publication, and to me this introduction now presents the rationale of the study very well (including the presentation of the study model in view of reporting results before detailing methods as planned). Well done!
I am of course ready to recommend the preregistration, but as I understood that all changes need to be done at this stage, there is still one point that requires checking in the current version of the text: I spotted in the introduction three occurrences of “???” where there should be references (in the first, second and last paragraphs). Can you please check these out to make sure that the corresponding references appear correctly?
In addition, because you intend to keep the introduction as it currently is for later reporting of the full study, I have a few other small suggestions to still improve the clarity of this section (I hope you will not find those remarks too picky!):
“Range expansions leading to problematic invasive species are occurring across the globe”: maybe reformulate here to “Problematic range expansions of invasive species are occurring across the globe” or “Range expansions leading to problematic invasions are occurring across the globe”
“Within-species variation in the ability (movement) and motivation (exploratory tendency) to encounter conspecifics, novel foods, and novel food sources could be a limiting factor in successful species range expansions”: is it really within-species variation that is a limiting factor? Or rather limited ability and motivation to move themselves? Within-species variation should on the contrary favor such expansion (the higher the within-species variation, the higher the chances that some individuals with extreme phenotypes may successfully settle in new places)
“the occurrence of conspecifics, food, and predators”: but also heterospecific competitors, parasites… maybe the list should remain open for the many environmental factors concerned a priori
“Additionally, common mynas were faster to approach a novel object for food in urban areas where novelty is frequently encountered compared with mynas in areas with low exposure to novelty”: sorry I do not clearly see the link with the preceding idea here about differences between core and edge habitats as the focus is here mostly on between-individual differences rather than between habitat differences. Can you please rephrase here? (e.g. start with urban areas imposing high level of novelty, thus favoring more explorative individuals (here mynas) compared to rural areas, as a second example here?)
“while dispersal has been shown to vary based on exploratory tendency”: consider replacing by “while dispersal and exploratory tendencies have been shown to be associated” because these are only correlations, not causal relations (in most cases at least – I can recall only one selection experiment on exploration in great tits that drove longer dispersal distances, if I remember well – but I could not find again the reference!)
“Space use behavior is influenced by internal states like exploratory tendency and hunger”: maybe replace by “Space use behavior is expected to be influenced by internal states like exploratory tendency and hunger” otherwise you would already state as certain what you plan to investigate here?
Maybe consider being more general in the following sentence by adding this suggested part: “Instead, spatial and temporal autocorrelation, where the position of an individual at a given time will be tightly linked to its position both before and after, including cases where individuals are repeatedly found in the same locations across time”
Consider a slight change: “The nature and level of ecological and social factors grackles experience may vary in importance between populations…”
Typo: “TGenerally, this species is strongly…” (remove T)
Consider slight changes: “First, we will test whether grackles’ performance on exploration tasks in captivity is related to the space use metrics of the same individuals …”
Revision round #301 Sep 2020
Decision round #3
Thank you for your very detailed answers to our questions and comments in the last round, and in particular for adding a clear introductory section presenting the context of the study, the objectives, the general methods and potential implications. This section is currently a sort of a mix between introduction, methods and discussion as would be in a standard paper, and I think it will need to be reorganized in the manuscripts resulting from the study, but for now I am fully satisfied with this section that perfectly addresses my previous demand for a more dedicated section on presenting the study. In particular, I find the link between the individual processes and the population-level expansion question and the rationale for grouping the two main questions of interest here now much clearer; both aspects are now much better integrated (including in the title).
I am therefore happy to recommend the pre-registration for PCI Ecology, and of course wish you good luck for the continuation of the project. I list below a few more details (and a few comments) that you could consider to still improving the text before publication.
Abstract : - “Range expansion could be facilitated by individuals on the range edge that consistently differ in behavior compared to individuals in other parts of the range”: consider replacing by: “by consistent behavioural differences between individuals on the range edge and those in other parts of the range”? - “We will compare performance on an exploration task in captivity to subsequent space use behavior in the wild”: consider replacing by “we will test whether performance on an exploration task in captivity relates to subsequent space use behavior in the wild”? - add identify in “e.g. identify which individuals are likely to remain…”
Introduction: - “Duckworth and Badyaev (2007) found that the more aggressive male western bluebirds dispersed the furthest”: strictly speaking, I do not think that these authors explored dispersal distance, but they found that new individuals in a population (defined as dispersers) were more aggressive. Consider rewording here accordingly? - “thus facilitating the range expansion and displacing the less aggressive mountain bluebirds”: not sure that this is easily understandable for readers not familiar with this earlier paper, consider replacing by “thus facilitating the displacement of competing but less aggressive mountain bluebirds and favoring range expansion” or something like this? - citation for the definition of dispersal: instead of Cote et al. 2010, it would be more appropriate to cite Greenwood 1980 or 1982 - “novel foods, and food sources”: what do you mean here by distinguishing both? - consider adding the bold parts in the following sentence: “Traditional studies of animal space use required spatial and temporal independence of data points for statistical analysis (Swihart and Slade 1985). Yet, movement behavior is influenced by internal state, as well as the availability of habitat and resources, which can be distributed non-randomly across the landscape (Nathan et al. 2008), and movement data points are therefore and by construction unlikely to meet such spatio-temporal independence criteria.” (otherwise, which link do you make between these two sentences?) - the 3rd paragraph is entirely methodological and comes a bit early in the manuscript, but this will certainly be re-adjusted in the resulting publication after the study is completed. - 4th paragraph: I personally prefer to remain general as long as possible in the introduction and detail the study species specificities only in the methods, while keeping only general aims and objectives in the introduction. But again, you will see later on whether you wish to adjust the text accordingly in the resulting manuscripts. - internal state (singular)? - “with these ecological and social factors which may vary”: add a coma after factors - first sentence of 5th paragraph: maybe make a transition here to start with (To better understand…), and I think it could be good to separate (i) the general objectives (testing the relation between exploratory tendency and space use behaviour) and (ii) the contexts for measuring these two behaviours (in captivity for exploration, in the wild for space use). This could simply be done by a slight change such as “We aim to understand whether measures of exploration, measured in captivity, are associated with space use behavior, measured in the wild, in grackles from three populations…” but importantly would place the focus back to the general objective. - consider adding the bold part in the following sentence: “measured here following the protocol described in McCune et al. 2019 » - “To validate that our methods are producing behavioral responses due to an inherent behavioral type”: consider replacing by “to test whether our methods are producing behavioral responses due to an inherent behavioral type”? (you do not have the answer already?) - consider adding the bold part in the following sentence: “whether performance on each task is correlated with performance on other tasks”? (or indicate to what it would be correlated here) - “on the two exploration tasks”: I am not sure readers will understand what the two tasks are here, so it may be better to mention them in full here by adding “(response to novel environment and to novel object)” – if I am right - Overall, the current version of the introductory section is very methodological oriented, but I think the writing of a standard manuscript following the analyses of resulting data will separate the objectives from methods in a more classical way (adding more info about previous literature to identify the biological questions to be explored). For now, I find this general presentation highly helpful and I am fully satisfied with it. - consider changing the bold parts in the following sentence: “we will attach a radio tag to each grackle and release them back” - “Furthermore, if space use behavior correlates with measures of exploration, then space use data could be used to inform conservation management strategies”: indeed, but this is not an objective of the present study since the study species in invasive! Probably something to highlight in the future discussion sections of the publications to follow. - I’m also fine regarding the “make more touches”; I did not have time to read the pre-registration describing the exploration tests in detail, but in any case, you will describe (even briefly) the tests in the manuscripts to follow, so the readers will not be disturbed by this point.
Revision round #201 Jul 2020
Decision round #2
Does great-tailed grackle space use behavior reflect individual differences in exploration? Preregistration by Dr. Kelsey B. McCune, Dr. Cody Ross, Melissa Folsom, Luisa Bergeron, Dr. Corina Logan Review round 2
First of all, my deepest apologies for the long delay in processing the revision of your pre-registration. I believe that these past months have been difficult for all of us and the timing was particularly bad on my side…
Thank you for a thorough revision providing many details and adjustments to make the context and methods of the study clearer and take caution on the inferences that can be made from the results. The two reviewers (out of the three original ones) that could read your revised text and answers to their comments were happy with your changes, and my own reading also confirms that you have been able to satisfactorily take into account the comments of the last reviewer. We all agree that this work currently in progress will bring much information to relate individual behavioural traits to population-level processes, and as such, constitutes a highly valuable contribution to our understanding of movement (and expansion) processes.
When reading the revised version, two additional main comments / questions came to my mind, and I think it may be good to consider them before I recommend the preregistration.
First, the format of the preregistration still makes me feel a bit uncomfortable; I acknowledge that this is not a standard manuscript, yet the absence of a dedicated introduction clearly setting the context of the study makes it difficult to really understand some of the choices made in the methods. Currently, this context appears in part in the “abstract” (a longer version that lies in between a standard abstract and an introduction) and in part in the methods themselves to justify the variables, models used etc. Would it be possible to write a clear introduction section in a more standard way, that would provide more details about previous studies, what they have done and what remains to explore, and the implications of the work? The current abstract section does not provide enough details about the context and rationale of the study (in particular, the transition to the second main prediction is inexistent, see also below). I think the preregistration would gain in clarity by adding a clear introduction and this would anyway be used in the future manuscripts resulting from the work. I would therefore consider adding this section, if it falls in the scope of preregistrations (not sure what format is required?)
Second (and this is also linked to the previous comment), I still think that the current presentation of the study and analyses leaves a gap between the individual and population processes that it aims to link. The ultimate aim of the work here is to relate (i) individual exploratory behaviour (measured in captivity), (ii) individual space use behaviour (measured in the field) and (iii) population-level expansion processes (through the among-population comparison across the species range). Yet, the two main hypotheses appear to only partly address this aim because one part is missing in this tryptic: we will have no information about the differences in exploratory behaviour between the study populations, which would close the circle here and help understand whether individual differences in exploratory behaviour can at least partly explain species range expansion through individual space use. Thus I would suggest to (i) either add the among-population comparison of individual exploratory behaviour as a third axis of this work, or (ii) link more closely the two currently independent axes. As I suspect that the among-comparison in exploratory behaviour is planned to be part of another piece of work (?), maybe the second option would be best. In this case, why not simply consider a single model including the study population among the main effects of the model exploring the link between space use and exploratory behaviour (conspecific density can be considered at a small scale only, which seems to me more relevant to explain individual space use behaviour)? I understand that the data is limited and this would add one more explanatory variable to the models, but on the other hand it would avoid implementing separate models and allow testing more directly for a link to population processes that is currently missing to my opinion. Globally, both when presenting the study and in the statistical analyses planned, I would say that more effort seems to be needed to complete the exploration of the links between the three main variables of interest here (this is also apparent in the title, which does not mention the population and range expansion processes at all). I still think that making a clearer link between both predictions is needed for the coherence of the whole project. This would easily be done in a “real” introduction section here. Again, while this does not decrease the merits of the study, I believe that this point is likely to be raised by reviewers who will later on assess the manuscript out of the study. Thus maybe it could be good to better integrate the currently two axes of the work already here.
I also detail below a number of additional comments and questions (sorry there are no line numbers so it is not always easy to spot the location in the text), and attach a version of the text in which I have made suggestions and comments directly in the text.
- Abstract: “which could be subject to selection”: are you planning to investigate the genetic basis of exploration behaviour later on? Maybe a word on it as a perspective would be good…
- Prediction 1 alternative 1: it does not seem straightforward to me to link the use of a smaller area to higher efficiency; showing this may require an additional measure of this efficiency (e.g. foraging efficiency?).
- Prediction 1 alternative 2 and 3: but again, I think that the correlation between the different measures of exploration should be investigated first (before being related to space use). The authors mention it but it appears later on only, and it is not clear how this will be done overall (only correlations? what kind of models will be used? etc.)
- Table 1: please explain the number of years and generation presented for the first site
- I am wondering why the testing of 57 birds is anticipated rather than e.g. 60? Maybe there is no need to raise questions about an approximate number, and 60 (20 per site x 3 sites, half of each sex, thus 10 birds of each sex per site) reads more naturally than 57? I’d suggest replacing by 60, this remains the expected approximate sample size.
- “we are able to understand what this species is capable of, rather than testing juveniles who might still be developing their cognitive skills”: given that, as also noted in the text, adults may converge to a common phenotype, what the species is capable of might however be expressed during the juvenile stage. Thus this justification is a bit strange to me?
- “so they fall off after one to four months”: this means that the comparison between space use behaviour during the breeding and non-breeding seasons is made across-individuals and not within-individuals: I think that this should be made clear in the text.
- “an experimenter tracks each tagged grackle for approximately 1.5 hours on a given day”: this is not totally clear as it gives the feeling that all birds are tracked every day, which appears not to be the case in the next sentence. This may need to be reformulated.
- “we aim to track all grackles equally during morning and afternoon time periods”: replace by “we aim to balance tracking data equally during morning and afternoon time periods for all grackles” (I if understand well)?
- “To account for alternative variables that may relate to space use behavior in wild grackles, we will also include covariates in our models that measure energetic condition (described in Berens et al. 2019), and habitat characteristics such as human food sources and available breeding habitat (described in Logan et al. 2019).”: this mention is fine overall, but more explanation (even brief) about why including these variables may be needed here (just as done for about conspecific density).
- “Each point will be visited once during the non-breeding season (Sep-Mar)”: a single count does not appear sufficient to provide a reliable estimate of density; the use of classical CMR methods requiring at least three counts may be needed. Or the reason why only one count will be performed needs to be explained here, along with the way to account for potential biases (e.g. if grackles show behavioural differences that affect detection probability between populations).
- “We catch grackles with a variety of methods”: at least describe all these methods used here (even briefly, with just their name)? or include a reference to another preregistration that describes them?
- “we attach radio tags to birds that do not participate in aviary tests”: explain here that this non-participation is due to the bird behaviour and not to other reasons (e.g. technical difficulties, choice of the experimenter or other).
- “times 1 and 2”: explain what these time periods are.
- “If there is a significant effect of season, we will run models separately for each dependent variable and each season”: why not simply including a season effect in the model and keep all data together? Unless behaviours are very different between both periods, this would be more powerful and also allow testing formal differences between seasons (through testing interactions between season and other variables).
- The sections “Methods” and “Analysis plan” show quite some repetitions, in particular in the descriptions of parameters / variables considered. Here again, the format used for this preregistration that differs from a standard manuscript may not appear optimal?
- “We will then model the relationship between bird-specific data on performance in the exploration tasks (and other covariates), and bird-specific movement parameters (e.g. step-size, turning angle, autocorrelation in space use).”: this is very brief and I think not sufficient to assess what statistical models will be used. Please provide details here.
- In particular: “The number of predictor variables was restricted to only the fixed effects because this test was not designed for mixed models.” but unless I missed it, the fixed vs. random effects are not described earlier?
- Check out the double parentheses issue with references.
Regarding your answers to the reviewers’ comments:
- Response 1: it may not be related to dispersal (but see comment below) but still, why do you not define your links as behavioural syndromes?
- Response 3: authors mention “…at both the individual and population level we have incorporated additional measures for data collection and analyses” but only one measure of density (group size, thus local density) seems to be considered later on, so this needs clarification (what variable refers to each of the two scales mentioned here?)
- Response 6: make clear that several females can breed on the territory defended by one (or more?) males, thus there is polygyny here (I found that this was not totally clear here).
- “we would have a biased sample”: I don’t understand this comment, especially as the proportion of non-participating birds caught with each of the two methods is compared later on to the proportion caught overall with each method, thus it is indeed possible to check for such biases (in participating to the tests and then for those participating, in the measures of exploration).
- By successive home ranges, I did not mean here between the breeding and non-breeding seasons, but during the same period, i. e. wandering birds that prospect from one place to another (or possibly use different home ranges successively over short periods of time). But then this does not seem to happen in this species, right? All adults (at least those caught) are in fact established over given determined territories? I think it may be a good idea to mention this clearly, as this is not true for all species. And this raises another thought: what if the processes of interest here, i. e. exploration, space use and ultimately colonization of new places, are in fact mostly occurring in juveniles during natal dispersal, while variation in these behaviours disappears in settled adults? An absence of differences between individuals / populations may be due to the age class considered here not being the most relevant here. I am not sure that this needs to be discussed in this pre-registration at this stage, but it might be something to keep in mind when results come in.
- Paragraph on power analyses: I’d suggest some rewriting, e.g. “To assess the effects that we will be able to detect given the expected sample size, we used GPower (v.3.1, @faul2007g, @faul2009statistical) to conduct power analyses based on confidence intervals. GPower uses pre-set drop down menus and we chose the options that were as close to our analysis methods as possible (listed in each analysis below). […] These power analyses are not fully aligned with our study design, and the expected effect sizes are difficult to estimate due to the lack of prior data on this species; yet we are unaware of current better options.”
- “our interest in decreasing noise by attempting to measure it, which increases the number of explanatory variables”: I do not understand this section, and thus suggest to either delete or explain it in more detail? How do you measure noise by increasing explanatory variables? Please rephrase here.
- Response 25: I am not sure to understand the link between fitness / adaptation and sex biases in dispersal. I concur with the reviewer here that the evolutionary aspect is not part of the present project and thus that it would be better not to mention it here to start with (but could be done in the discussion section) and possibly leave it to other parts of the study (other pre-registrations, as mentioned here).
- “Regarding dispersal syndromes, to us dispersal would refer to grackles moving out of the natal area when they are young and/or as adults searching for new territories. However, this type of longer-distance movement (and tracking of young birds) is beyond the scope of this investigation. Therefore, we are not investigating the effect of consistent behavioral differences in population dynamics.” While I agree with this answer at a detailed scale, the link is nevertheless made with evolutionary population dynamics through the study of three different populations at different stages of range expansion. Thus I still agree with the reviewer that dispersal / colonization syndromes are at play here, even if the variables investigated here are not directly dispersal – it seems implicit in the study design (otherwise, why compare these populations?)
- “but it is still unknown whether individual differences in exploration relate to daily movement patterns”: I’d replace this by “but it is still unknown whether such relationships rely on links between individual differences in exploration and daily movement patterns”.
- Response 30: even if there is no connectivity between the three study populations (which indeed does not seem plausible given the between-population distances!) I believe that the reviewer was thinking more in terms of connectivity between adjacent populations: if there are a network of highly connected populations, differences may disappear quickly. Maybe a word could be added here about whether many connected populations can be found around the study populations chosen here, or in other words whether the grackle populations form a continuous network of connected populations (even if dispersal occurs at a limited spatial scale). Also, was the discussion about turnover speed somehow evoked in the text?
- Be careful not to use interchangeably neophobia and boldness, both traits have different definitions, as noted in the text: boldness includes a notion of risk to the individual while neophobia does not. They are usually considered two different personality traits for this reason. Boldness involves that individuals identify a specific risk before displaying a reaction, e.g. when a dummy predator is present.
- “Many studies that measure animal personality using novel objects have similarly used the same objects in two (or more) repeated exposures and found that responses are repeatable (e.g. @mccune2018personality). If there is habituation to the object because it has become familiar after Time 1, this will likely affect all individuals similarly and we will still be able to detect overall repeatability in behavior”. While I agree with the first part of the statement (the use of the same object repeatedly on the same individuals in different tests, in most cases to make sure indeed the same level of stimulation / motivation is reached, as mentioned here), I am not sure that I agree with the end part: habituation to an object may differ between individuals – I would even say that it can be expected to differ between individuals! Yet, no ideal design for such tests exists (using the same object repeatedly vs. changing objects both have their drawbacks), thus I have no problem with using the same object in several tests, but I think it is necessary to acknowledge the limitation that this repeated use imposes.
- “Based on these findings, it is unlikely that the aviary grackles that are released back to the wild change social groups or home ranges.” Even if this sounds highly plausible, it remains necessary to formally show it by tracking individuals not held in captivity as mentioned just after.
- “It is possible that grackles that participate in aviary tests are more bold and exploratory than conspecifics that were never in the aviaries.” Why would it be so? Do you suggest that spending time in the aviaries may change the behavioural responses of the birds post-release? Or do you suggest that the birds initially placed in aviaries are not representative of the whole population, and if yes, why? Please can you explain?
- “so that our question solely refers to adult behavior”: fine but large differences are usually reported (especially with regards to behaviour) between one-year-old and older adults, as mentioned by the reviewer. Because it is not possible to distinguish these two age categories here, as detailed by the authors, it could be good to mention this point clearly (to avoid further questions by future referees).
Reviewed by Joe Nocera, 05 May 2020 19:46
Reviewed by Laure Cauchard, 05 May 2020 22:37
Revision round #123 Dec 2019
Decision round #1
My apologies for the delay in handling the reviewing process of your pre-print ‘Does great-tailed grackle space use behavior reflect individual differences in exploration?’. Three reviewers have now read your pre-print, along with myself, and all of us found your planed study of high interest, as it should bring very important and relevant insights into the links between behavioural traits and space use in the wild, and ultimately help bridging gaps between individual behaviour and population dynamics in the context of range expansion and invasions. But as you will also see, we all have comments and suggestions on different aspects of your work, ranging from the conceptual part (do you really measure behavioural flexibility?) to the practical part (design of the measures of exploration and tracking in the field, including replicates of the three populations, explaining planned sample sizes, and statistical issues regarding measuring home ranges and including variables in your models). I think that all the comments and suggestions are highly relevant and I really recommend that you follow them as much as possible, since (as mentioned by reviewers) you are likely to face these comments for the manuscripts issued from the study once performed (and some may require adjusting your protocol / sampling from the start). Thus I think that these comments require such work on your preprint and thus would be happy to read a revised version of it.
My own comments below:
I concur with the reviewers in that the question investigated here as it is stated currently relates to dispersal syndromes (i.e. consistent suite of behavioural differences between individuals) rather than behavioural flexibility (i.e. within-individual variation). Yet, as we understand, the authors plan to measure exploratory behaviour over a possibly large long of time (it is mentioned that individuals may be held in captivity up to 6 months – see below regarding this point), and this may imply a series of measures on the same individuals over time, which should allow estimating within-individual repeatability in this behaviour and thus, by contrast, flexibility (i.e. the variable part). Similarly, the movements of tagged individuals can be followed in the field over large periods of time, which should allow estimating again repeatability and by contrast flexibility. However, we currently have no information about such estimates (how many series of measurements in captivity? how to estimate within-individual variability of movement in the field, over space and time?); instead, the feeling here is that basically only one measure will be used for each behavioural compartment (exploration in captivity and space use in the field, in particular with the use of a single measure of home range). I believe that, as presented here, the authors aim to address behavioural syndromes, but they nevertheless have the potential to explore flexibility, thus they should possibly re-consider their behavioural measures so as to make sure they estimate both the consistent and flexible part, and rewrite this estimate description and analyses parts with this in mind. I believe that assessing flexibility as stated from the start would certainly be of great interest here.
In line with this, the authors should be careful about how they characterize exploration as measured by the tests in captivity and exploration as can be measured by space use behaviour in the wild. It is often assumed that prospecting movements represent exploration in the wild, but using the same term in both contexts here can be misleading about the hypotheses tested, as this gives the feeling that it is already assumed that space use is linked to exploratory – one of the very question investigated.
Indeed, space use will be largely influenced by habitat use, thus I concur with reviewers that a clear description of the habitat available for different activities (foraging, breeding, mating…) is needed here for each individual monitored. If such information is not accounted for, it will be very difficult to address the questions of interest, especially if habitat varies globally between the three populations investigated.
I also agree with reviewers that replicates for each zone would be needed to allow separating an individual population effect from the location within the expansion range. Alternatively, a more complete gradient of populations over the expansion range could also be used (e.g. either 2-3 replicates per population at the centre, middle and edge of the expansion range, or a gradient of 6-8 populations over the range, controlling if possible for longitude and/or latitude). I acknowledge that this may be practically difficult, but three points will likely be insufficient to fully answer the question of the link with population dynamics and expansion here.
I do not know what the authors plan to do with the different measures of exploration in captivity, but rather than using different measures and link them one by one to the space use measures (which will automatically increase the total number of models and thus the risk of false positive), it may be better to first check whether and how these different measures relate to each other and whether they may define an overall exploration score for a given individual. I also concur with the reviewers’ comments about (1) making sure about what is measured (as mentioned, the novel environment test could also be considered as a novel object test instead) and (2) it seems a bit far-fletched to assume that space use in the wild may be related to one or the other of the exploration measures in captivity only, as presented here (as mentioned, clear predictions about why it should be so seems rather difficult to do, especially without testing directly behaviour towards novel food sources) – assessing the relations between these different measures in captivity as a first step should allow addressing this point, and I would encourage the author to include such a phase in their approach, possibly simplifying prediction 1 alternatives 2 and 3 then here.
Prediction 1 alternative 4 includes the first mention that only adult individuals will be tested: why is it so? This should be specified. I also concur here with reviewers in that even among adults, there may be large differences between yearlings (and possibly 2-years old, depending on the longevity of the species) and older adults in behaviour linked to dominance, experience etc. More information should be given on this point, and also generally about the life-cycle and ecology of the species, as it is currently described nowhere in the pre-print. Yet, some of the assertions and hypotheses depend on such information. For instance Prediction 1 alternative 2 mentions different ecological constraints (habitats availability, predation, etc.) but it is currently very difficult to get an idea of the influence of these constraints. Similarly, whether grackles are territorial or live in social groups and to what extent (e.g. they may be flocking over the wintering season to find food but breed in individual territories) seems fundamental information to understand the space use patterns – and also the possible influence of captivity duration on subsequent behaviour after release (as clearly mentioned by reviewers, 6 months of captivity are likely to affect access to territory / social groups…)
The reference to Duckworth and Badyaev (2007) study in Prediction 2 is misleading here as they worked on aggressiveness and not on exploration.
Prediction 2 alternative 1: there could also be selection for certain phenotypes for other reasons than space use, e.g. on energy allocation trade-offs, that would in a second step, i.e. indirectly, impose constraints on space use. Maybe the authors should consider this possibility, at least theoretically (as it may be difficult to test it directly)?
Overall, the link between the two main predictions is not sufficiently clearly explained, and more specifically, I do not really understand in what prediction 2 is addressing the main question, namely the link between exploration and space use. Of course, we understand that individuals will be sampled from the different populations over the expansion range, so that ultimately, the hypothesis tested is whether individuals from different populations differ in their exploration behaviour, which influences the expansion of the species. But to me, this should be more directly and clearly stated, to make the link between the two predictions clear; in particular the sampling scheme for capturing and testing individuals in captivity should be described. We only currently know that a total of approx. 60 individuals will be tested, but we do not know the composition of this sample in terms of population of origin, as well as age, sex, etc. See also the important comments by reviewers about sample size and how it is possible to make sure that this sample will be large enough (i.e. power analysis), especially if sex, age, population of origin etc. need to be accounted for.
Again, more information is needed about the duration of captivity with regards to the experimental tests: why would 6 months be needed, and why should this vary between individuals? How many tests are performed per individual?
Regarding the tracking protocol in the field: it is not clear to me how the authors will ensure that they can detect exploratory trips. How to make sure that there will be no bias towards already known locations, where birds may be searched for in the first place? Are there previous data about movement in this species that may help with designing search protocols? Or will experimenters search for birds until they are found (but in any case there will be a giving-up time point, and how will it be set up)? Also what is the distance of detection in this system with the tags used? This will influence the distance of approach needed for the experimenter, and thus its potential consequences on subsequent bird behaviour (e.g. will it flee if it detects the experimenter’s presence?). The protocol mentions that the experimenters will not get too close, but I believe more precise information are needed on this point here (see also comments by reviewers on the comparison between tagged and color-ringed individuals, the latter requiring a relatively close approach for identification that may modify their behaviour differently compared to tagged individuals if detected from farther away; this comparison may also be influenced by the likely different resighting effort for the two categories). Also, information about tag mass with respect to bird mass should be given and justified. Overall, it will be necessary to describe the tagging and remote tracking procedure more precisely here.
What is the maximum number of birds that can be expected to be monitored? The authors only mention ‘as many as possible’, but this will depend on the search effort in the field, and an estimate would be useful here. Also, what will be the relative effort of catching with each planned capture method? Importantly, a potential bias in individuals’ exploration behaviour depending on the catching method should be a posteriori checked using the behavioural estimates in captivity.
Besides the comment by reviewers about the planned estimate of space use, I was wondering whether grackles could exploit successive home ranges, and if yes how this may be detected here? More generally, how will the end of the sampling period for remote tracking in the field be determined? Will it depend on each individual, based on his previous behaviour, or will it be a fixed period for all individuals? If the former, how to ensure that the same biological processes will be captured for all individuals (e.g. if some individuals may regularly move over a given range while others may exploit different home ranges successively)?
Regarding independent variables: is a sex effect expected (and in this case why) or will sex be included only as a controlling factor here? The measure proposed for condition first surprised me, as I was expecting a measure of body condition such as the classical ratio mass / size (tarsus or wing length); then I understood that this is not really condition, but rather captivity experience, and I would suggest changing the term here so that there is no confusion. What about including a ‘real’ measure of body condition? and age? (see above and reviewer’s comments). It would also be important here to first know which variables affect exploratory measures in captivity, so I believe that this should be a first step (probably included in the other protocol focused on these measures, but it would be important to mention it here as not all readers will also read the other protocols).
Regarding the presentation: the list of variables in P1 alternative 1 could simply include the additional variables to avoid repetition. Among these new variables, the problem-solving performance is mentioned here but nowhere else! It would be important to explain why this variable is included here, what will be tested, etc.
In the analysis plan section: how do you know that no data will be missing? How do you also know that GPS locations will be recorded during ‘normal activities’? (besides, what is a ‘normal’ activity?)
This is a long list of questions and remarks, but I hope that the authors will find it useful to improve the presentation and justification of their study, and want to stress again that this is a very nice study plan that should provide many very useful insights about important questions, both on fundamental and applied points of views.