While many species' populations are declining, primarily due to human-related impacts (McKnee et al., 2014), certain species have thrived by utilizing human-influenced environments, leading to their population expansion (Muñoz & Real, 2006). In this context, the capacity to adapt and modify behaviors in response to new surroundings is believed to play a crucial role in facilitating species' spread to novel areas (Duckworth & Badyaev, 2007). For example, an increase in innovative behaviors within recently established communities could aid in discovering previously untapped food resources, while a decrease in exploration might reduce the likelihood of encountering dangers in unfamiliar territories (e.g., Griffin et al., 2016). To investigate the contribution of these behaviors to rapid range expansions, it is essential to directly measure and compare behaviors in various populations of the species.

The study conducted by Logan et al. (2023) aims to comprehend the role of behavioral changes in the range expansion of great-tailed grackles (Quiscalus mexicanus). To achieve this, the researchers compared the prevalence of specific behaviors at both the expansion's edge and its middle. Great-tailed grackles were chosen as an excellent model due to their behavioral adaptability, rapid geographic expansion, and their association with human-modified environments. The authors carried out a series of experiments in captivity using wild-caught individuals, following a detailed protocol. The study successfully identified differences in two of the studied behavioral traits: persistence (individuals participated in a larger proportion of trials) and flexibility variance (a component of the species' behavioral flexibility, indicating a higher chance that at least some individuals in the population could be more flexible). Notably, individuals at the edge of the population exhibited higher values of persistence and flexibility, suggesting that these behavioral traits might be contributing factors to the species' expansion. Overall, the study by Logan et al. (2023) is an excellent example of the importance of behavioral flexibility and other related behaviors in the process of species' range expansion and the significance of studying these behaviors across different populations to gain a better understanding of their role in the expansion process.

Finally, it is important to underline that this study is part of a pre-registration that received an In Principle Recommendation in PCI Ecology (Sebastián-González 2020) where objectives, methodology, and expected results were described in detail. The authors have identified any deviation from the original pre-registration and thoroughly explained the reasons for their deviations, which were very clear. 

References

Duckworth, R. A., & Badyaev, A. V. (2007). Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proceedings of the National Academy of Sciences, 104(38), 15017-15022. https://doi.org/10.1073/pnas.0706174104

Griffin, A.S., Guez, D., Federspiel, I., Diquelou, M., Lermite, F. (2016). Invading new environments: A mechanistic framework linking motor diversity and cognition to establishment success. Biological Invasions and Animal Behaviour, 26e46. https://doi.org/10.1017/CBO9781139939492.004

Logan, C. J., McCune, K., LeGrande-Rolls, C., Marfori, Z., Hubbard, J., Lukas, D. 2023. Implementing a rapid geographic range expansion - the role of behavior changes. EcoEvoRxiv, ver. 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.32942/X2N30J

McKee, J. K., Sciulli, P. W., Fooce, C. D., & Waite, T. A. (2004). Forecasting global biodiversity threats associated with human population growth. Biological Conservation, 115(1), 161-164. https://doi.org/10.1016/S0006-3207(03)00099-5

Muñoz, A. R., & Real, R. (2006). Assessing the potential range expansion of the exotic monk parakeet in Spain. Diversity and Distributions, 12(6), 656-665. https://doi.org/10.1111/j.1472-4642.2006.00272.x

Sebastián González, E. (2020) The role of behavior and habitat availability on species geographic expansion. Peer Community in Ecology, 100062. https://doi.org/10.24072/pci.ecology.100062. Reviewers: Caroline Nieberding, Tim Parker, and Pizza Ka Yee Chow.

The output of a community model depends on how you set its parameters. Thus, analyses of specific parameter settings hardwire the results to specific ecological scenarios. Because more general answers are often of interest, one tradition is to give models a statistical treatment: one summarizes how model parameters vary across species, and then predicts how changing the summary, instead of the individual parameters themselves, would change model output. Arguably the best-known example is the work initiated by May, showing that the properties of a community matrix, encoding effects species have on each other near their equilibrium, determine stability (1,2). More recently, this statistical treatment has also been applied to one of community ecology’s more prickly and slippery subjects: community assembly, which deals with the question “Given some regional species pool, which species will be able to persist together at some local ecosystem?”. Summaries of how species grow and interact in this regional pool predict the fraction of survivors and their relative abundances, the kind of dynamics, and various kinds of stability (3,4). One common characteristic of such statistical treatments is the assumption of disorder: if species do not interact in too structured ways, simple and therefore powerful predictions ensue that often stand up to scrutiny in relatively ordered systems. 
 
In their recent preprint, Miller, Clenet, et al. (5) subscribe to this tradition and consider tractable assembly scenarios (6) to study the outcome of assembly in a metacommunity. They recover a result of remarkable simplicity: roughly half of the species pool makes it into the final assemblage. Their vehicle is Tilman’s classic metacommunity model (7), where colonization rates are traded off with competitive ability. More precisely, in this model, one ranks species according to their colonization rate and attributes a greater competitive strength to lower-ranked species, which makes competition strictly hierarchical and thus departs from the disorder usually imposed by statistical approaches. The authors then leverage the simplicity of the species interaction network implied by this recursive setting to analytically probe how many species survive assembly. This turns out to be a fixed fraction that is distributed according to a Binomial with a mean of 0.5. While these results should not be extrapolated beyond the system at hand (4), they are important for two reasons. First, they imply that, within the framework of metacommunities driven by competition-colonization tradeoffs, richer species pools will produce richer communities: there is no upper bound on species richness, other than the one set by the raw material available for assembly. Second, this conclusion does not rely on simulation or equation solving and is, therefore, a hopeful sign of the palatability of the problem, if formalized in the right way. Their paper then shows that varying some of the settings does not change the main conclusion: changing how colonization rates distribute across species, and therefore the nature of the tradeoff, or the order with which species invade seems not to disrupt the big picture. Only when invaders are created “de novo” during assembly, a scenario akin to “de novo” mutation, a smaller fraction of species will survive assembly. 
 
As always, logical extensions of this study involve complicating the model and then looking if the results stay on par. The manuscript cites switching to other kinds of competition-colonization tradeoffs, and the addition of spatial heterogeneity as two potential avenues for further research. While certainly of merit, alternative albeit more bumpy roads would encompass models with radically different behavior. Most notably, one wonders how priority effects would play out. The current analysis shows that different invasion orders always lead to the same final composition, and therefore the same final species richness, confirming earlier results from models with similar structures (6). In models with priority effects, different invasion orders will surely lead to different compositions at the end. However, if one only cares about how many (and not which) species survive, it is unsure how much priority effects will qualitatively affect assembly. Because priority effects are varied in their topological manifestation (8), an important first step will be to evaluate which kinds of priority effects are compliant with formal analysis. 
 
References
 
1. May, R. M. (1972). Will a Large Complex System be Stable? Nature 238, 413–414. https://doi.org/10.1038/238413a0

2. Allesina, S. & Tang, S. (2015). The stability–complexity relationship at age 40: a random matrix perspective. Population Ecology, 57, 63–75. https://doi.org/10.1007/s10144-014-0471-0

3. Bunin, G. (2016). Interaction patterns and diversity in assembled ecological communities. Preprint at http://arxiv.org/abs/1607.04734.

4. Barbier, M., Arnoldi, J.-F., Bunin, G. & Loreau, M. (2018). Generic assembly patterns in complex ecological communities. Proceeding of the National Academy of Sciences, 115, 2156–2161. https://doi.org/10.1073/pnas.1710352115

5. Miller, Z. R., Clenet, M., Libera, K. D., Massol, F. & Allesina, S. (2023). Coexistence of many species under a random competition-colonization trade-off. bioRxiv 2023.03.23.533867, ver 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.1101/2023.03.23.533867

6. Serván, C. A. & Allesina, S. (2021). Tractable models of ecological assembly. Ecology Letters, 24, 1029–1037. https://doi.org/10.1111/ele.13702

7. Tilman, D. (1994). Competition and Biodiversity in Spatially Structured Habitats. Ecology, 75, 2–16. https://doi.org/10.2307/1939377

8. Song, C., Fukami, T. & Saavedra, S. (2021). Untangling the complexity of priority effects in multispecies communities. Ecolygy Letters, 24, 2301–2313. https://doi.org/10.1111/ele.13870

​​Contrasting with the great alarm on bee declines, it is astonishing how little basic biology we know about bees, including on abundant and widespread species that are becoming model species. Plant-pollinator relationships are one of the cornerstones of bee ecology, and researchers are increasingly documenting bees' diets. However, we rarely know which effects feeding on different flowers has on bees' health. This paper (Tourbez et al. 2023) uses an elegant experimental setting to test the effect of heather pollen on bumblebees' (Bombus terrestris) reproductive success. This is a timely question as heather is frequently used by bumblebees, and its nectar has been reported to reduce parasite infections. In fact, it has been suggested that bumblebees can medicate themselves when infected (Richardson et al. 2014), and the pollen of some Asteraceae has been shown to help them fight parasites (Gekière​ et al. 2022). The starting hypothesis is that heather pollen contains flavonoids that might have a similar effect. Unfortunately, Tourbez​ and collaborators do not support this hypothesis, showing a negative effect of heather pollen, in particular its flavonoids, in bumblebees offspring, and an increase in parasite loads when fed on flavonoids. This is important because it challenges the idea that many pollen and nectar chemical compounds might have a medicinal use, and force us to critically analyze the effect of chemical compounds in each particular case. The results open several questions, such as why bumblebees collect heather pollen, or in which concentrations or pollen mixes it is deleterious. A limitation of the study is that it uses micro-colonies, and extrapolating this to real-world conditions is always complex. Understanding bee declines require a holistic approach starting with bee physiology and scaling up to multispecies population dynamics.  

References

Gekière, A., Semay, I., Gérard, M., Michez, D., Gerbaux, P., & Vanderplanck, M. 2022. Poison or Potion: Effects of Sunflower Phenolamides on Bumble Bees and Their Gut Parasite. Biology, 11(4), 545.​ https://doi.org/10.3390/biology11040545

Richardson, L.L., Adler, L.S., Leonard, A.S., Andicoechea, J., Regan, K.H., Anthony, W.E., Manson, J.S., &​ Irwin, R.E. 2015. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society of London B: Biological Sciences 282 (1803), 20142471. https://doi.org/10.1098/rspb.2014.2471

Tourbez, C., Semay, I., Michel, A., Michez, D., Gerbaux, P., Gekière A. & Vanderplanck, M. 2023. Heather pollen is not necessarily a healthy diet for bumble bees. Zenodo, ver 3, reviewed and recommended by PCI Ecology. https://doi.org/10.5281/zenodo.8192036​​

In a progressively human-dominated planet (Venter et al., 2016), the fate of many species will depend on the extent to which they can persist in anthropogenic landscapes. In Western Europe, where only small areas of primary habitat remain (e.g. Sabatini et al., 2018), semi-natural areas are crucial habitats to many native species, yet they are threatened by the expansion of human activities, including agricultural expansion and intensification (Rigal et al., 2023). 

A new study by Mallet and colleagues (Mallet et al., 2023) investigates the extent to which bird species in the Camargue region are able to use the margins of agricultural fields as substitutes for their preferred semi-natural habitats. Located in the delta of the Rhône River in Southern France, the Camargue is internationally recognized for its biodiversity value, classified as a Biosphere Reserve by UNESCO and as a Wetland of International Importance under the Ramsar Convention (IUCN & UN-WCMC, 2023). Mallet and colleagues tested three specific hypotheses: that grass strips (grassy field boundaries, including grassy tracks or dirt roads used for moving agricultural machinery) can function as substitute habitats for grassland species; that reed strips along drainage ditches (common in the rice paddy landscapes of the Camargue) can function as substitute habitats to wetland species; and that hedgerows can function as substitute habitats to species that favour woodland edges. They did so by measuring how the local abundances of 14 bird species (nine typical of forest edges, 3 of grasslands, and two of reedbeds) respond to increasing coverage of either the three types of field margins or of the three types of semi-natural habitat. 

This is an elegant study design, yet – as is often the case with real field data – results are not as simple as expected. Indeed, for most species (11 out of 14) local abundances did not increase significantly with the area of their supposed primary habitat, undermining the assumption that they are strongly associated with (or dependent on) those habitats. Among the three species that did respond positively to the area of their primary habitat, one (a forest edge species) responded positively but not significantly to the area of field margins (hedgerows), providing weak evidence to the habitat compensation hypothesis. For the other two (grassland and a wetland species), abundance responded even more strongly to the area of field margins (grass and reed strips, respectively) than to the primary habitat, suggesting that the field margins are not so much a substitute but valuable habitats in their own right. 

It would have been good conservation news if field margins were found to be suitable habitat substitutes to semi-natural habitats, or at least reasonable approximations, to most species. Given that these margins have functional roles in agricultural landscapes (marking boundaries, access areas, water drainage), they could constitute good win-win solutions for reconciling biodiversity conservation with agricultural production. Alas, the results are more complicated than that, with wide variation in species responses that could not have been predicted from presumed habitat affinities. These results illustrate the challenges of conservation practice in complex landscapes formed by mosaics of variable land use types. With species not necessarily falling neatly into habitat guilds, it becomes even more challenging to plan strategically how to manage landscapes to optimize their conservation. The results presented here suggest that species’ abundances may be responding to landscape variables not taken into account in the analyses, such as connectivity between habitat patches, or maybe positive and negative edge effects between land use types. That such uncertainties remain even in a well-studied region as the Camargue, and for such a well-studied taxon such as birds, only demonstrates the continued importance of rigorous field studies testing explicit hypotheses such as this one by Mallet and colleagues. 

References

IUCN, & UN-WCMC (2023). Protected Planet. Protected Planet. https://www.protectedplanet.net/en 

Mallet, P., Béchet, A., Sirami, C., Mesléard, F., Blanchon, T., Calatayud, F., Dagonet, T., Gaget, E., Leray, C., & Galewski, T. (2023). Field margins as substitute habitat for the conservation of birds in agricultural wetlands. bioRxiv, 2022.05.05.490780, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.05.05.490780 

Rigal, S., Dakos, V., Alonso, H., Auniņš, A., Benkő, Z., Brotons, L., Chodkiewicz, T., Chylarecki, P., de Carli, E., del Moral, J. C. et al. (2023). Farmland practices are driving bird population decline across Europe. Proceedings of the National Academy of Sciences, 120, e2216573120. https://doi.org/10.1073/pnas.2216573120 

Sabatini, F. M., Burrascano, S., Keeton, W. S., Levers, C., Lindner, M., Pötzschner, F., Verkerk, P. J., Bauhus, J., Buchwald, E., Chaskovsky, O., Debaive, N. et al. (2018). Where are Europe’s last primary forests? Diversity and Distributions, 24, 1426–1439. https://doi.org/10.1111/ddi.12778 

Venter, O., Sanderson, E. W., Magrach, A., Allan, J. R., Beher, J., Jones, K. R., Possingham, H. P., Laurance, W. F., Wood, P., Fekete, B. M., Levy, M. A., & Watson, J. E. M. (2016). Sixteen years of change in the global terrestrial human footprint and implications for biodiversity conservation. Nature Communications, 7, 12558. https://doi.org/10.1038/ncomms12558 

Dispersal is a key element of the natural dynamics of meta-communities, and plays a central role in the success of populations colonizing new landscapes. Understanding how demographic processes may affect the speed at which alien species spread through environmentally-heterogeneous habitat fragments is therefore of key importance to manage biological invasions. This requires studying together the complex interplay of dispersal and population processes, two inextricably related phenomena that can produce many possible outcomes. Stochastic models offer an opportunity to describe this kind of process in a meaningful way, but to ensure that they are realistic (sensu Levins 1966) it is also necessary to combine model simulations with empirical data (Snäll et al. 2007).

Morel-Journel et al. (2023) put together stochastic models and experimental data to study how population density may affect the speed at which alien species spread through a heterogeneous landscape. They do it by focusing on what they call ‘colonisation debt’, which is merely the impact that population density at the invasion front may have on the speed at which the species colonizes patches of different carrying capacities. They investigate this issue through two largely independent approaches. First, a stochastic model of dispersal throughout the patches of a linear, 1-dimensional landscape, which accounts for different degrees of density-dependent growth. And second, a microcosm experiment of a parasitoid wasp colonizing patches with different numbers of host eggs. In both cases, they compare the velocity of colonization of patches with lower or higher carrying capacity than the previous one (i.e. what they call upward or downward gradients).

Their results show that density-dependent processes influence the speed at which new fragments are colonized is significantly reduced by positive density dependence. When either population growth or dispersal rate depend on density, colonisation debt limits the speed of invasion, which turns out to be dependent on the strength and direction of the gradient between the conditions of the invasion front, and the newly colonized patches. Although this result may be quite important to understand the meta-population dynamics of dispersing species, it is important to note that in their study the environmental differences between patches do not take into account eventual shifts in the scenopoetic conditions (i.e. the values of the environmental parameters to which species niches’ respond to; Hutchinson 1978, see also Soberón 2007). Rather, differences arise from variations in the carrying capacity of the patches that are consecutively invaded, both in the in silico and microcosm experiments. That is, they account for potential differences in the size or quality of the invaded fragments, but not on the costs of colonizing fragments with different environmental conditions, which may also determine invasion speed through niche-driven processes. This aspect can be of particular importance in biological invasions or under climate change-driven range shifts, when adaptation to new environments is often required (Sakai et al. 2001; Whitney & Gabler 2008; Hill et al. 2011).

The expansion of geographical distribution ranges is the result of complex eco-evolutionary processes where meta-community dynamics and niche shifts interact in a novel physical space and/or environment (see, e.g., Mestre et al. 2020). Here, the invasibility of native communities is determined by niche variations and how similar are the traits of alien and native species (Hui et al. 2023). Within this context, density-dependent processes will build upon and heterogeneous matrix of native communities and environments (Tischendorf et al. 2005), to eventually determine invasion success. What the results of Morel-Journel et al. (2023) show is that, when the invader shows density dependence, the invasion process can be slowed down by variations in the carrying capacity of patches along the dispersal front. This can be particularly useful to manage biological invasions; ongoing invasions can be at least partially controlled by manipulating the size or quality of the patches that are most adequate to the invader, controlling host populations to reduce carrying capacity. But further, landscape manipulation of such kind could be used in a preventive way, to account in advance for the effects of the introduction of alien species for agricultural exploitation or biological control, thereby providing an additional safeguard to practices such as the introduction of parasitoids to control plagues. These practical aspects are certainly worth exploring further, together with a more explicit account of the influence of the abiotic conditions and the characteristics of the invaded communities on the success and speed of biological invasions.

REFERENCES

Hill, J.K., Griffiths, H.M. & Thomas, C.D. (2011) Climate change and evolutionary adaptations at species' range margins. Annual Review of Entomology, 56, 143-159. https://doi.org/10.1146/annurev-ento-120709-144746

Hui, C., Pyšek, P. & Richardson, D.M. (2023) Disentangling the relationships among abundance, invasiveness and invasibility in trait space. npj Biodiversity, 2, 13. https://doi.org/10.1038/s44185-023-00019-1

Hutchinson, G.E. (1978) An introduction to population biology. Yale University Press, New Haven, CT.

Levins, R. (1966) The strategy of model building in population biology. American Scientist, 54, 421-431. 

Mestre, A., Poulin, R. & Hortal, J. (2020) A niche perspective on the range expansion of symbionts. Biological Reviews, 95, 491-516. https://doi.org/10.1111/brv.12574

Morel-Journel, T., Haond, M., Duan, L., Mailleret, L. & Vercken, E. (2023) Colonisation debt: when invasion history impacts current range expansion. bioRxiv, 2022.11.13.516255, ver. 3 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.11.13.516255

Snäll, T., B. O'Hara, R. & Arjas, E. (2007) A mathematical and statistical framework for modelling dispersal. Oikos, 116, 1037-1050. https://doi.org/10.1111/j.0030-1299.2007.15604.x

Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. & Weller, S.G. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics, 32, 305-332. https://doi.org/10.1146/annurev.ecolsys.32.081501.114037

Soberón, J. (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecology Letters, 10, 1115-1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x

Tischendorf, L., Grez, A., Zaviezo, T. & Fahrig, L. (2005) Mechanisms affecting population density in fragmented habitat. Ecology and Society, 10, 7. https://doi.org/10.5751/ES-01265-100107

Whitney, K.D. & Gabler, C.A. (2008) Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14, 569-580. https://doi.org/10.1111/j.1472-4642.2008.00473.x