Environmental factors influencing red knot (Calidris canutus islandica) departure times of relocation flights within the non-breeding period.

Deciding when to depart on long-distance, sometimes global, movements can be especially important for flying species. Adverse weather conditions can affect energetic flight costs and navigational ability. While departure timings and conditions have been well-studied for migratory flights to and from the breeding range, few studies have focussed on flights within the non-breeding season. Yet in some cases, overwintering ranges can be large enough that ecological barriers, and a lack of resting sites en route, may resist movement, especially in unfavorable environmental conditions. Understanding the conditions that will enable or prohibit flights within an overwintering range is particularly relevant in light of climate change, whereby increases in extreme weather events may reduce the connectivity of sites. We tracked 495 (n = 251 in 2019; n = 244 in 2020) overwintering red knots (Calidris canutus islandica) in the Dutch Wadden Sea and investigated how many departed towards the UK (on westward relocation flights), which requires flying over the North Sea. For those that departed, we used a resource selection model to determine the effect of environmental conditions on the timing of relocation flights. Specifically, we investigated the effects of wind, rain, atmospheric pressure, cloud cover, and migratory timing relative to sunset and tidal cycle, which have all been shown to be crucial to migratory departure conditions. Approximately 37% (2019) and 36% (2020) of tagged red knots departed on westward relocation flights, indicating differences between individuals' space use within the overwintering range. Red knots selected for departures between 1 and 2.5 h after sunset, approximately 4 h before high tide, with tailwinds and little cloud cover. However, rainfall and changes in atmospheric pressure appear unimportant. Our study reveals environmental conditions that are important for relocation flights across an ecological barrier, indicating potential consequences of climate change on connectivity.

Individuals of a group-living shorebird show smaller home range overlap when food availability is low.

BACKGROUND: Group living animals, such as shorebirds foraging on intertidal mudflats, may use social information about where to find hidden food items. However, flocking also increases intraspecific competition for resources, which may be exacerbated by food scarcity. Therefore, although aggregation may bring benefits, it may also increase the intensity of intraspecific competition. METHODS: We examined this trade-off in adult great knots Calidris tenuirostris, a molluscivorous long-distance migrating shorebird species, using interannual variation based on 2 years with different levels of food availability during their northward migratory staging in the northern Yellow Sea, China. We estimated individual home ranges and the extent of spatial overlap of home ranges of individually tagged birds in 2012 and 2015, whilst discounting for possible differences in body size, body mass, sex and migration schedule between years. RESULTS: We found that home range size was not associated with body mass, arrival date, body size, or sex of the individual. Despite a significant difference in food availability between the two study years, there was no significant change in the 50% and 95% home range size of great knots in the contrasting situations. However, there was a significantly smaller spatial overlap between individuals in the year when food was less available, suggesting that great knots operated more independently when food was scarce than when it was abundant. CONCLUSIONS: These results suggest that minimizing intraspecific competition became more important when food was scarce. Where it is impossible to monitor all habitats en route, monitoring the local movements of shorebirds may offer a way to detect changes in habitat quality in real time.

Big-data approaches lead to an increased understanding of the ecology of animal movement.

Understanding animal movement is essential to elucidate how animals interact, survive, and thrive in a changing world. Recent technological advances in data collection and management have transformed our understanding of animal "movement ecology" (the integrated study of organismal movement), creating a big-data discipline that benefits from rapid, cost-effective generation of large amounts of data on movements of animals in the wild. These high-throughput wildlife tracking systems now allow more thorough investigation of variation among individuals and species across space and time, the nature of biological interactions, and behavioral responses to the environment. Movement ecology is rapidly expanding scientific frontiers through large interdisciplinary and collaborative frameworks, providing improved opportunities for conservation and insights into the movements of wild animals, and their causes and consequences.

A guide to pre-processing high-throughput animal tracking data.

Modern, high-throughput animal tracking increasingly yields 'big data' at very fine temporal scales. At these scales, location error can exceed the animal's step size, leading to mis-estimation of behaviours inferred from movement. 'Cleaning' the data to reduce location errors is one of the main ways to deal with position uncertainty. Although data cleaning is widely recommended, inclusive, uniform guidance on this crucial step, and on how to organise the cleaning of massive datasets, is relatively scarce. A pipeline for cleaning massive high-throughput datasets must balance ease of use and computationally efficiency, in which location errors are rejected while preserving valid animal movements. Another useful feature of a pre-processing pipeline is efficiently segmenting and clustering location data for statistical methods while also being scalable to large datasets and robust to imperfect sampling. Manual methods being prohibitively time-consuming, and to boost reproducibility, pre-processing pipelines must be automated. We provide guidance on building pipelines for pre-processing high-throughput animal tracking data to prepare it for subsequent analyses. We apply our proposed pipeline to simulated movement data with location errors, and also show how large volumes of cleaned data can be transformed into biologically meaningful 'residence patches', for exploratory inference on animal space use. We use tracking data from the Wadden Sea ATLAS system (WATLAS) to show how pre-processing improves its quality, and to verify the usefulness of the residence patch method. Finally, with tracks from Egyptian fruit bats Rousettus aegyptiacus, we demonstrate the pre-processing pipeline and residence patch method in a fully worked out example. To help with fast implementation of standardised methods, we developed the R package atlastools, which we also introduce here. Our pre-processing pipeline and atlastools can be used with any high-throughput animal movement data in which the high data-volume combined with knowledge of the tracked individuals' movement capacity can be used to reduce location errors. atlastools is easy to use for beginners while providing a template for further development. The common use of simple yet robust pre-processing steps promotes standardised methods in the field of movement ecology and leads to better inferences from data.

Exploration speed in captivity predicts foraging tactics and diet in free-living red knots.

Variation in foraging tactics and diet is usually attributed to differences in morphology, experience and prey availability. Recently, consistent individual differences in behaviour (personality) have been shown to be associated with foraging strategies. Bolder or more exploratory individuals are predicted to have a faster pace-of-life and offset the costs of moving more or in risky areas, with higher energetic gains by encountering profitable foraging opportunities and prey. However, the relationship between personality, foraging and diet is poorly understood. We investigated how exploratory behaviour in red knots Calidris canutus is associated with foraging tactics and diet by combining laboratory experiments, field observations and stable isotope analysis. First, we developed a mobile experimental arena to measure exploration speed in controlled settings. We validated the method by repeated testing of individuals over time and contexts. This setup allowed us to measure exploratory personality at the field site, eliminating the need to bring birds into captivity for long periods of time. After releasing birds within days of their capture, we asked whether exploration speed was associated with differences in foraging tactics and diet in the wild. We found that tactile foraging red knots mainly caught hard-shelled prey that are buried in the sediment, whereas visual foraging knots only captured soft preys located close to or on the surface. We also found that faster explorers showed a higher percentage of visual foraging than slower explorers. By contrast, morphology (bill length and gizzard size) had no significant effect on foraging tactics. Diet analysis based on δ15 N and δ13 C stable isotope values of plasma and red blood cells confirmed our field observations with slower explorers mainly consumed hard-shelled prey while faster explorers consumed more soft than hard-shelled prey. Our results show that foraging tactics and diet are associated with a personality trait, independent of morphological differences. We discuss how consistent behaviour might develop early in life through positive feedbacks between foraging tactics, prey type and foraging efficiency.

Quantification of marine benthic communities with metabarcoding.

DNA metabarcoding methods have been implemented in studies aimed at detecting and quantifying marine benthic biodiversity. In such surveys, universal barcodes are amplified and sequenced from environmental DNA. To quantify biodiversity with DNA metabarcoding, a relation between the number of DNA sequences of a species and its biomass and/or the abundance is required. However, this relationship is complicated by many factors, and it is often unknown. In this study, we validate estimates of biomass and abundance from molecular approaches with those from the traditional morphological approach. Abundance and biomass were quantified from 126 samples of benthic intertidal mudflat using traditional morphological approaches and compared with frequency of occurrence and relative read abundance estimates from a molecular approach. A relationship between biomass and relative read abundance was found for two widely dispersed annelid taxa (Pygospio and Scoloplos). None of the other taxons, however, showed such a relationship. We discuss how quantification of abundance and biomass using molecular approaches are hampered by the ecology of DNA i.e. all the processes that determine the amount of DNA in the environment, including the ecology of the benthic species as well as the compositional nature of sequencing data.

Optimizing the use of biologgers for movement ecology research.

The paradigm-changing opportunities of biologging sensors for ecological research, especially movement ecology, are vast, but the crucial questions of how best to match the most appropriate sensors and sensor combinations to specific biological questions and how to analyse complex biologging data, are mostly ignored. Here, we fill this gap by reviewing how to optimize the use of biologging techniques to answer questions in movement ecology and synthesize this into an Integrated Biologging Framework (IBF). We highlight that multisensor approaches are a new frontier in biologging, while identifying current limitations and avenues for future development in sensor technology. We focus on the importance of efficient data exploration, and more advanced multidimensional visualization methods, combined with appropriate archiving and sharing approaches, to tackle the big data issues presented by biologging. We also discuss the challenges and opportunities in matching the peculiarities of specific sensor data to the statistical models used, highlighting at the same time the large advances which will be required in the latter to properly analyse biologging data. Taking advantage of the biologging revolution will require a large improvement in the theoretical and mathematical foundations of movement ecology, to include the rich set of high-frequency multivariate data, which greatly expand the fundamentally limited and coarse data that could be collected using location-only technology such as GPS. Equally important will be the establishment of multidisciplinary collaborations to catalyse the opportunities offered by current and future biologging technology. If this is achieved, clear potential exists for developing a vastly improved mechanistic understanding of animal movements and their roles in ecological processes and for building realistic predictive models.

Erratum: Publisher Correction: Resource landscapes explain contrasting patterns of aggregation and site fidelity by red knots at two wintering sites.

[This corrects the article DOI: 10.1186/s40462-018-0142-4.].

Presence-absence of marine macrozoobenthos does not generally predict abundance and biomass.

Many monitoring programmes of species abundance and biomass increasingly face financial pressures. Occupancy is often easier and cheaper to measure than abundance or biomass. We, therefore, explored whether measuring occupancy is a viable alternative to measuring abundance and biomass. Abundance- or biomass-occupancy relationships were studied for sixteen macrozoobenthos species collected across the entire Dutch Wadden Sea in eight consecutive summers. Because the form and strength of these relationships are scale-dependent, the analysis was completed at different spatiotemporal scales. Large differences in intercept and slope of abundance- or biomass-occupancy relationships were found. Abundance, not biomass, was generally positively correlated with occupancy. Only at the largest scale, seven species showed reasonably strong abundance-occupancy relationships with large coefficients of determination and small differences in observed and predicted values (RMSE). Otherwise, and at all the other scales, intraspecific abundance and biomass relationships were poor. Our results showed that there is no generic relationship between a species' abundance or biomass and its occupancy. We discuss how ecological differences between species could cause such large variation in these relationships. Future technologies might allow estimating a species' abundance or biomass directly from eDNA sampling data, but for now, we need to rely on traditional sampling technology.

Resource landscapes explain contrasting patterns of aggregation and site fidelity by red knots at two wintering sites.

BACKGROUND: Space use strategies by foraging animals are often considered to be species-specific. However, similarity between conspecific strategies may also result from similar resource environments. Here, we revisit classic predictions of the relationships between the resource distribution and foragers' space use by tracking free-living foragers of a single species in two contrasting resource landscapes. At two main non-breeding areas along the East-Atlantic flyway (Wadden Sea, The Netherlands and Banc d'Arguin, Mauritania), we mapped prey distributions and derived resource landscapes in terms of the predicted intake rate of red knots (Calidris canutus), migratory molluscivore shorebirds. We tracked the foraging paths of 13 and 38 individual red knots at intervals of 1 s over two and five weeks in the Wadden Sea and at Banc d'Arguin, respectively. Mediated by competition for resources, we expected aggregation to be strong and site fidelity weak in an environment with large resource patches. The opposite was expected for small resource patches, but only if local resource abundances were high. RESULTS: Compared with Banc d'Arguin, resource patches in the Wadden Sea were larger and the maximum local resource abundance was higher. However, because of constraints set by digestive capacity, the average potential intake rates by red knots were similar at the two study sites. Space-use patterns differed as predicted from these differences in resource landscapes. Whereas foraging red knots in the Wadden Sea roamed the mudflats in high aggregation without site fidelity (i.e. grouping nomads), at Banc d'Arguin they showed less aggregation but were strongly site-faithful (i.e. solitary residents). CONCLUSION: The space use pattern of red knots in the two study areas showed diametrically opposite patterns. These differences could be explained from the distribution of resources in the two areas. Our findings imply that intraspecific similarities in space use patterns represent responses to similar resource environments rather than species-specificity. To predict how environmental change affects space use, we need to understand the degree to which space-use strategies result from developmental plasticity and behavioural flexibility. This requires not only tracking foragers throughout their development, but also tracking their environment in sufficient spatial and temporal detail.

Marine biorhythms: bridging chronobiology and ecology.

Marine organisms adapt to complex temporal environments that include daily, tidal, semi-lunar, lunar and seasonal cycles. However, our understanding of marine biological rhythms and their underlying molecular basis is mainly confined to a few model organisms in rather simplistic laboratory settings. Here, we use new empirical data and recent examples of marine biorhythms to highlight how field ecologists and laboratory chronobiologists can complement each other's efforts. First, with continuous tracking of intertidal shorebirds in the field, we reveal individual differences in tidal and circadian foraging rhythms. Second, we demonstrate that shorebird species that spend 8-10 months in tidal environments rarely maintain such tidal or circadian rhythms during breeding, likely because of other, more pertinent, temporally structured, local ecological pressures such as predation or social environment. Finally, we use examples of initial findings from invertebrates (arthropods and polychaete worms) that are being developed as model species to study the molecular bases of lunar-related rhythms. These examples indicate that canonical circadian clock genes (i.e. the homologous clock genes identified in many higher organisms) may not be involved in lunar/tidal phenotypes. Together, our results and the examples we describe emphasize that linking field and laboratory studies is likely to generate a better ecological appreciation of lunar-related rhythms in the wild.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Diet preferences as the cause of individual differences rather than the consequence.

Behavioural variation within a species is usually explained as the consequence of individual variation in physiology. However, new evidence suggests that the arrow of causality may well be in the reverse direction: behaviours such as diet preferences cause the differences in physiological and morphological traits. Recently, diet preferences were proposed to underlie consistent differences in digestive organ mass and movement patterns (patch residence times) in red knots (Calidris canutus islandica). Red knots are molluscivorous and migrant shorebirds for which the size of the muscular stomach (gizzard) is critical for the food processing rate. In this study, red knots (C. c. canutus, n = 46) were caught at Banc d'Arguin, an intertidal flat ecosystem in Mauritania, and released with radio-tags after the measurement of gizzard mass. Using a novel tracking system (time-of-arrival), patch residence times were measured over a period of three weeks. Whether or not gizzard mass determined patch residence times was tested experimentally by offering 12 of the 46 tagged red knots soft diets prior to release; this reduced an individual's gizzard mass by 20-60%. To validate whether the observed range of patch residence times would be expected from individual diet preferences, we simulated patch residence times as a function of diet preferences via a simple departure rule. Consistent with previous empirical studies, patch residence times in the field were positively correlated with gizzard mass. The slope of this correlation, as well as the observed range of patch residence times, was in accordance with the simulated values. The 12 birds with reduced gizzard masses did not decrease patch residence times in response to the reduction in gizzard mass. These findings suggest that diet preferences can indeed cause the observed among-individual variation in gizzard mass and patch residence times. We discuss how early diet experiences can have cascading effects on the individual expression of both behavioural and physiomorphic traits. This emphasizes that to understand the ecological consequences of individual differences, knowledge of the environment during development is required.

Understanding spatial distributions: negative density-dependence in prey causes predators to trade-off prey quantity with quality.

Negative density-dependence is generally studied within a single trophic level, thereby neglecting its effect on higher trophic levels. The 'functional response' couples a predator's intake rate to prey density. Most widespread is a type II functional response, where intake rate increases asymptotically with prey density; this predicts the highest predator densities at the highest prey densities. In one of the most stringent tests of this generality to date, we measured density and quality of bivalve prey (edible cockles Cerastoderma edule) across 50 km² of mudflat, and simultaneously, with a novel time-of-arrival methodology, tracked their avian predators (red knots Calidris canutus). Because of negative density-dependence in the individual quality of cockles, the predicted energy intake rates of red knots declined at high prey densities (a type IV, rather than a type II functional response). Resource-selection modelling revealed that red knots indeed selected areas of intermediate cockle densities where energy intake rates were maximized given their phenotype-specific digestive constraints (as indicated by gizzard mass). Because negative density-dependence is common, we question the current consensus and suggest that predators commonly maximize their energy intake rates at intermediate prey densities. Prey density alone may thus poorly predict intake rates, carrying capacity and spatial distributions of predators.

Benefits of foraging in small groups: An experimental study on public information use in red knots Calidris canutus.

Social foraging is common and may provide benefits of safety and public information. Public information permits faster and more accurate estimates of patch resource densities, thus allowing more effective foraging. In this paper we report on two experiments with red knots Calidris canutus, socially foraging shorebirds that eat bivalves on intertidal mudflats. The first experiment was designed to show that red knots are capable of using public information, and whether dominance status or sex affected its use. We showed that knots can detect the foraging success of conspecifics and choose a patch accordingly. Neither dominance status nor sex influenced public information use. In the second experiment, by manipulating group size, we investigated whether public information use affected food-patch discovery rates and patch residence times. We showed that the time needed before locating a food patch decreased in proportion to group size. Also, an individual's number of patch visits before locating the food declined with group size, and, to our surprise, their average patch residence time did as well. Moreover, knots differed in their search strategy in that some birds consistently exploited the searching efforts of others. We conclude that socially foraging knots have the potential to greatly increase their food-finding rate by using public information. This article is part of a Special Issue entitled: In Honor of Jerry Hogan.

Personality drives physiological adjustments and is not related to survival.

The evolutionary function and maintenance of variation in animal personality is still under debate. Variation in the size of metabolic organs has recently been suggested to cause and maintain variation in personality. Here, we examine two main underlying notions: (i) that organ sizes vary consistently between individuals and cause consistent behavioural patterns, and (ii) that a more exploratory personality is associated with reduced survival. Exploratory behaviour of captive red knots (Calidris canutus, a migrant shorebird) was negatively rather than positively correlated with digestive organ (gizzard) mass, as well as with body mass. In an experiment, we reciprocally reduced and increased individual gizzard masses and found that exploration scores were unaffected. Whether or not these birds were resighted locally over the 19 months after release was negatively correlated with their exploration scores. Moreover, a long-term mark-recapture effort on free-living red knots with known gizzard masses at capture confirmed that local resighting probability (an inverse measure of exploratory behaviour) was correlated with gizzard mass without detrimental effects on survival. We conclude that personality drives physiological adjustments, rather than the other way around, and suggest that physiological adjustments mitigate the survival costs of exploratory behaviour. Our results show that we need to reconsider hypotheses explaining personality variation based on organ sizes and differential survival.

Landscape-scale experiment demonstrates that Wadden Sea intertidal flats are used to capacity by molluscivore migrant shorebirds.

1. Whether intertidal areas are used to capacity by shorebirds can best be answered by large-scale manipulation of foraging areas. The recent overexploitation of benthic resources in the western Dutch Wadden Sea offers such an 'experimental' setting. 2. We review the effects of declining food abundances on red knot Calidris canutus islandica numbers, based on a yearly large-scale benthic mapping effort, long-term colour-ringing and regular bird-counts from 1996 to 2005. We focus on the three-way relationships between suitable foraging area, the spatial predictability of food and red knot survival. 3. For each benthic sampling position, red knot intake rate (mg AFDM s(-1)) was predicted by a multiple prey species functional response model, based on digestive rate maximization (this model explained diet and intake rate in earlier studies on red knots). This enabled us to derive the spatial distribution of the suitable foraging area, which in each of the 10 years was analysed with a measure of autocorrelation, i.e. Moran's I. 4. Over the 10 years, when accounting for a threshold value to meet energetic demands, red knots lost 55% of their suitable foraging area. This ran parallel to a decrease in red knot numbers by 42%. Although there was also a decrease in patchiness (i.e. less information about the location of the suitable feeding sites), this did not yet lead to additional loss of birds. 5. To cope with these landscape-scale declines in food stocks, an increase in the capacity for instantaneous food processing would be required. Although we show that red knots indeed enlarged their muscular gizzards, the increase in gizzard size was not enough to compensate for the decreased feeding area. 6. Survival of islandica knots in the western Dutch Wadden Sea, based on colour-ring resightings, declined from 89% in the first half of our study period to 82% in the second half of our study period and could account for almost half of the decline in red knot numbers; the rest must have moved elsewhere in winter. 7. Densities of red knots per unit suitable foraging area remained constant at 10 knots ha(-1) between 1996 and 2005, which suggests that red knots have been using the Dutch Wadden Sea to full capacity.