Estimating population parameters is critical for analysis and management of wildlife populations. Drawing inference at the population level requires a robust sampling scheme and information about the representativeness of the studied population (Williams et al. 2002). In their textbook, Williams et al. (see chapter 5, 2002) listed several sampling issues, including both temporal and spatial heterogeneity and especially imperfect detection. Several methods, either sampling-based or model-based can be used to circumvent these issues.

In their paper, Kissling et al. (2024) addressed the case of the Kittlitz’s murrelet (Brachyramphus brevirostris), a cryptic ice-associated seabird, combining spatial variation in its distribution, temporal variation in breeding propensity, imperfect detection and logistical challenges to access the breeding area. The Kittlitz’s murrelet is thus the perfect species to illustrate common issues and logistical difficulties to implement a standard sampling scheme. 

The authors proposed a modelling framework unifying several datasets from different surveys to extract information on each step of the detection process: the spatial match between the targeted population and the sampled population, the probability of presence in the sample area, the probability of availability given presence in the sample area and finally, the probability of detection given presence and availability. All these components were part of the framework to estimate abundance and trend for this species. 

They took advantage of a radiotracking survey during several years to inform spatial match and probability of presence. They performed a behavioural experiment to assess the probability of availability of murrelets given it was present in sampling area, and they used a conventional distance-sampling boat survey to estimate detection of individuals. This is worth noting that the most variable components were the probability of presence in the sample area, with a global mean of 0.50, and the probability of detection given presence and availability ranging from 0.49 to 0.77. The estimated trend for Kittlitz’s murrelet was negative and all the information gathered in this study will be useful for future conservation plan. 

Coupling a decomposition of the detection process with different data sources was the key to solve problems raised by such “difficult” species, and the paper of Kissling et al. (2024) is a good way to follow for other species, allowing to inform the detection components for the targeted species - and also for our global understanding of detection process, and to infer about the temporal trend of species of conservation concern. 

References

Williams, B. K., Nichols, J. D., and Conroy, M. J. (2002). Analysis and management of animal populations. Academic Press.

Michelle L. Kissling, Paul M. Lukacs, Kelly Nesvacil, Scott M. Gende, Grey W. Pendleton (2024) Using multiple datasets to account for misalignment between statistical and biological populations for abundance estimation. EcoEvoRxiv, ver.3 peer-reviewed and recommended by PCI Ecology https://doi.org/10.32942/X2W03T

As seasonal cycles become increasingly disrupted, our understanding of the ecology and evolution of reproductive seasonality in tropical vertebrates remains limited (Bronson 2009). To predict how changes in seasonality might impact these animals, it is crucial to identify which elements of their varied reproductive patterns are connected to the equally varied patterns of rainfall seasonality (within-year fluctuations) or the significant climatic unpredictability (year-to-year variations) characteristic of the intertropical region. 

Dezeure et al. (2024) provide a comprehensive examination of reproductive seasonality in papionin monkeys across diverse African environments. By investigating the ecological and evolutionary determinants of reproductive timing, the authors offer novel insights into how climatic factors, particularly environmental unpredictability, shape reproductive strategies in these primates. This study stands out not only for its methodological rigour but also for its contribution to our understanding of how primates adapt their reproductive behaviours to varying environmental pressures. The findings have broad implications, particularly in the context of ongoing climate change, which is expected to increase environmental unpredictability globally. The innovative approach of this paper lies in its multifaceted examination of reproductive seasonality, which integrates data from 21 wild populations of 11 papionin species. The study employs a robust statistical framework, incorporating Bayesian phylogenetic generalised linear mixed models to control for phylogenetic relatedness among species. This methodological choice is crucial because it allows the authors to disentangle the effects of environmental variables from evolutionary history, providing a more accurate picture of how current ecological factors influence reproductive strategies.

The study’s focus on environmental unpredictability as a determinant of reproductive seasonality is particularly noteworthy. While previous research has established the importance of environmental seasonality (Janson and Verdolin 2005), this paper breaks new ground by showing that the magnitude of year-to-year variation in rainfall – rather than just the seasonal distribution of rainfall – plays a critical role in determining the intensity of reproductive seasonality. This finding is supported by the significant negative correlation between reproductive seasonality and environmental unpredictability, which the authors demonstrate across multiple populations and species. The results of this study are important for several reasons. First, they challenge the traditional view that reproductive seasonality is primarily driven by within-year environmental fluctuations. By showing that inter-annual variability in rainfall is a stronger predictor of reproductive timing than intra-annual variability, the authors suggest that primates, like papionins, have evolved flexible reproductive strategies to cope with the unpredictable availability of resources. This flexibility is likely an adaptive response to the highly variable environments that many African primates inhabit, where food availability can vary dramatically not just within a year but from year to year. Second, the study highlights the role of reproductive flexibility in the evolutionary success of papionins. The authors provide compelling evidence that species within the Papio genus, for example, exhibit significant variability in reproductive timing both within and between populations. This variability suggests that these species possess a remarkable ability to adjust their reproductive strategies in response to local environmental conditions, which may have contributed to their widespread distribution across diverse habitats in Africa. This finding aligns with the work of Brockman and Schaik (2005), who argued that reproductive flexibility is a key factor in the success of primates in unpredictable environments.

The study also contributes to our understanding of the evolutionary transition from seasonal to non-seasonal breeding in primates. The authors propose that the loss of strict reproductive seasonality in some papionin species may represent an adaptive shift toward greater reproductive flexibility. This shift could be driven by the need to maximise reproductive success in environments where the timing of resource peaks is difficult to predict. The authors’ findings support this hypothesis, as they show that populations living in more unpredictable environments tend to have lower reproductive seasonality. The broader implications of this study (Dezeure et al. 2024) extend beyond the specific case of papionin monkeys. The findings have relevance for the study of reproductive strategies in other long-lived, tropical mammals that face similar environmental challenges. As climate change is expected to increase the frequency and intensity of environmental unpredictability, understanding how species have historically adapted to such conditions can provide valuable insights into their potential resilience or vulnerability to future changes.

Many primate species are already facing significant threats from habitat loss, hunting, and climate change. By identifying the environmental factors that influence reproductive success, Dezeure et al. (2024) study can help inform conservation strategies aimed at protecting the most vulnerable populations. For example, conservation efforts could focus on maintaining or restoring habitat features that promote reproductive flexibility, such as access to a variety of food resources that peak at different times of the year (Chapman et al.).

References

Brockman D, Schaik C (2005) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press. https://doi.org/10.1017/CBO9780511542343

Bronson FH (2009) Climate change and seasonal reproduction in mammals. Philos Trans R Soc B Biol Sci 364:3331–3340. https://doi.org/10.1098/rstb.2009.0140

Chapman CA, Gogarten JF, Golooba M, et al Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers. Am J Primatol n/a:e23577. https://doi.org/10.1002/ajp.23577

Jules Dezeure, Julie Dagorrette, Lugdiwine Burtschell, Shahrina Chowdhury, Dieter Lukas, Larissa Swedell, Elise Huchard (2024) Flexible reproductive seasonality in Africa-dwelling papionins is associated with low environmental productivity and high climatic unpredictability. bioRxiv, ver.2 peer-reviewed and recommended by PCI Ecology https://doi.org/10.1101/2024.05.01.591991

Janson C, Verdolin J (2005) Seasonality of primate births in relation to climate. In: Schaik CP van, Brockman DK (eds) Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press, Cambridge, pp 307–350 https://doi.org/10.1017/CBO9780511542343.012

In the article, "Are the more flexible great-tailed grackles also better at behavioral inhibition?", Logan and colleagues (2021) are setting an excellent standard for cognitive research on wild-caught animals. Using a decent sample (N=18) of wild-caught birds, they set out to test the ambiguous link between behavioral flexibility and behavioral inhibition, which is supported by some studies but rejected by others. Where this study is more thorough and therefore also more revealing than most extant research, the authors ran a battery of tests, examining both flexibility (reversal learning and solution switching) and inhibition (go/no go task; detour task; delay of gratification) through multiple different test series. They also -- somewhat accidentally -- performed their experiments and analyses with and without different criteria for correctness (85%, 100%). Their mistakes, assumptions and amendments of plans made during preregistration are clearly stated and this demonstrates the thought-process of the researchers very clearly.

Logan et al. (2021) show that inhibition in great-tailed grackles is a multi-faceted construct, and demonstrate that the traditional go/no go task likely tests a very different aspect of inhibition than the detour task, which was never linked to any of their flexibility measures. Their comprehensive Bayesian analyses held up the results of some of the frequentist statistics, indicating a consistent relationship between flexibility and inhibition, with more flexible individuals also showing better inhibition (in the go/no go task). This same model, combined with inconsistencies in the GLM analyses (depending on the inclusion or exclusion of an outlier), led them to recommend caution in the creation of arbitrary thresholds for "success" in any cognitive tasks. Their accidental longer-term data collection also hinted at patterns of behaviour that shorter-term data collection did not. Of course, researchers have to decide on success criteria in order to conduct experiments, but in the same way that frequentist statistics are acknowledged to have flaws, the setting of success criteria must be acknowledged as inherently arbitrary. Where possible, researchers could reveal novel, biologically salient patterns by continuing beyond the point where a convenient success criterion has been reached. This research also underscores that tests may not be examining the features we expected them to measure, and are highly sensitive to biological and ecological variation between species as well as individual variation within populations.

To me, this study is an excellent argument for pre-registration of research (registered as Logan et al. 2019 and accepted by Vogel 2019), as the authors did not end up cherry-picking only those results or methods that worked. The fact that some of the tests did not "work", but was still examined, added much value to the study. The current paper is a bit densely written because of the comprehensiveness of the research. Some editorial polishing would likely make for more elegant writing. However, the arguments are clear, the results novel, and the questions thoroughly examined. The results are important not only for cognitive research on birds, but are potentially valuable to any cognitive scientist. I recommend this article as excellent food for thought.

References

Logan CJ, McCune K, Johnson-Ulrich Z, Bergeron L, Seitz B, Blaisdell AP, Wascher CAF. (2019) Are the more flexible individuals also better at inhibition? http://corinalogan.com/Preregistrations/g_inhibition.html  In principle acceptance by PCI Ecology of the version on 6 Mar 2019

Logan CJ, McCune KB, MacPherson M, Johnson-Ulrich Z, Rowney C, Seitz B, Blaisdell AP, Deffner D, Wascher CAF (2021) Are the more flexible great-tailed grackles also better at behavioral inhibition? PsyArXiv, ver. 7 peer-reviewed and recommended by Peer community in Ecology. https://doi.org/10.31234/osf.io/vpc39

Vogel E (2019) Adapting to a changing environment: advancing our understanding of the mechanisms that lead to behavioral flexibility. Peer Community in Ecology, 100016. https://doi.org/10.24072/pci.ecology.100016 

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 

Coastal lagoons are among the most productive natural ecosystems on Earth. These relatively closed basins are important habitats and nursery for endemic and endangered species and are extremely vulnerable to nutrient input from the surrounding catchment; therefore, they are highly susceptible to anthropogenic influence, pollution and invasion (Pérez-Ruzafa et al., 2019). In general, coastal lagoons exhibit great spatial and temporal variability in their physicochemical water characteristics due to the sporadic mixing of freshwater with marine influx. One of the alternatives for monitoring communities or target species in aquatic ecosystems is the environmental DNA (eDNA), since overcomes some limitations from traditional methods and enables the investigation of multiple species from a single sample (Thomsen and Willerslev, 2015). In coastal lagoons, where the water turbidity is highly variable, there is a major challenge for monitoring the eDNA because filtering turbid water to obtain the eDNA is problematic (filters get rapidly clogged, there is organic and inorganic matter accumulation, etc.). 

The study by Turba et al. (2023) analyzes different ways of dealing with eDNA sampling and processing in turbid waters and sediments of coastal lagoons, and offers guidelines to obtain unbiased results from the subsequent sequencing using 12S (fish) and 16S (Bacteria and Archaea) universal primers. They analyzed the effect on taxa detection of: i) freezing or not prior to filtering; ii) freezing prior to centrifugation to obtain a sample pellet; and iii) using frozen sediment samples as a proxy of what happens in the water. The authors propose these different alternatives (freeze, do not freeze, sediment sampling) because they consider that they are the easiest to carry out. They found that freezing before filtering using a 3 µm pore size filter had no effects on community composition for either primer, and therefore it is a worthwhile approach for comparison of fish, bacteria and archaea in this kind of system. However, significantly different bacterial community composition was found for sediment compared to water samples. Also, in sediment samples the replicates showed to be more heterogeneous, so the authors suggest increasing the number of replicates when using sediment samples. Something that could be a concern with the study is that the rarefaction curves based on sequencing effort for each protocol did not saturate in any case, this being especially evident in sediment samples. The authors were aware of this, used the slopes obtained from each curve as a measure of comparison between samples and considering that the sequencing depth did not meet their expectations, they managed to achieve their goal and to determine which protocol is the most promising for eDNA monitoring in coastal lagoons. Although there are details that could be adjusted in relation to this item, I consider that the approach is promising for this type of turbid system.

References

Pérez-Ruzafa A, Campillo S, Fernández-Palacios JM, García-Lacunza A, García-Oliva M, Ibañez H, Navarro-Martínez PC, Pérez-Marcos M, Pérez-Ruzafa IM, Quispe-Becerra JI, Sala-Mirete A, Sánchez O, Marcos C (2019) Long-Term Dynamic in Nutrients, Chlorophyll a, and Water Quality Parameters in a Coastal Lagoon During a Process of Eutrophication for Decades, a Sudden Break and a Relatively Rapid Recovery. Frontiers in Marine Science, 6. https://doi.org/10.3389/fmars.2019.00026

Thomsen PF, Willerslev E (2015) Environmental DNA – An emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation, 183, 4–18. https://doi.org/10.1016/j.biocon.2014.11.019

Turba R, Thai GH, Jacobs DK (2023) Different approaches to processing environmental DNA samples in turbid waters have distinct effects for fish, bacterial and archaea communities. bioRxiv, 2022.06.17.495388, ver. 2 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2022.06.17.495388