Towards a toolkit for global insect biodiversity monitoring.

Insects are the most diverse group of animals on Earth, yet our knowledge of their diversity, ecology and population trends remains abysmally poor. Four major technological approaches are coming to fruition for use in insect monitoring and ecological research-molecular methods, computer vision, autonomous acoustic monitoring and radar-based remote sensing-each of which has seen major advances over the past years. Together, they have the potential to revolutionize insect ecology, and to make all-taxa, fine-grained insect monitoring feasible across the globe. So far, advances within and among technologies have largely taken place in isolation, and parallel efforts among projects have led to redundancy and a methodological sprawl; yet, given the commonalities in their goals and approaches, increased collaboration among projects and integration across technologies could provide unprecedented improvements in taxonomic and spatio-temporal resolution and coverage. This theme issue showcases recent developments and state-of-the-art applications of these technologies, and outlines the way forward regarding data processing, cost-effectiveness, meaningful trend analysis, technological integration and open data requirements. Together, these papers set the stage for the future of automated insect monitoring. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Monitoring aerial insect biodiversity: a radar perspective.

In the current biodiversity crisis, populations of many species have alarmingly declined, and insects are no exception to this general trend. Biodiversity monitoring has become an essential asset to detect biodiversity change but remains patchy and challenging for organisms that are small, inconspicuous or make (nocturnal) long-distance movements. Radars are powerful remote-sensing tools that can provide detailed information on intensity, timing, altitude and spatial scale of aerial movements and might therefore be particularly suited for monitoring aerial insects and their movements. Importantly, they can contribute to several essential biodiversity variables (EBVs) within a harmonized observation system. We review existing research using small-scale biological and weather surveillance radars for insect monitoring and outline how the derived measures and quantities can contribute to the EBVs 'species population', 'species traits', 'community composition' and 'ecosystem function'. Furthermore, we synthesize how ongoing and future methodological, analytical and technological advancements will greatly expand the use of radar for insect biodiversity monitoring and beyond. Owing to their long-term and regional-to-large-scale deployment, radar-based approaches can be a powerful asset in the biodiversity monitoring toolbox whose potential has yet to be fully tapped. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Continental-scale patterns in diel flight timing of high-altitude migratory insects.

Many insects depend on high-altitude, migratory movements during part of their life cycle. The daily timing of these migratory movements is not random, e.g. many insect species show peak migratory flight activity at dawn, noon or dusk. These insects provide essential ecosystem services such as pollination but also contribute to crop damage. Quantifying the diel timing of their migratory flight and its geographical and seasonal variation, are hence key towards effective conservation and pest management. Vertical-looking radars provide continuous and automated measurements of insect migration, but large-scale application has not been possible because of limited availability of suitable devices. Here, we quantify patterns in diel flight periodicity of migratory insects between 50 and 500 m above ground level during March-October 2021 using a network of 17 vertical-looking radars across Europe. Independent of the overall daily migratory movements and location, peak migratory movements occur around noon, during crepuscular evening and occasionally the morning. Relative daily proportions of insect migration intensity and traffic during the diel phases of crepuscular-morning, day, crepuscular-evening and night remain largely equal throughout May-September and across Europe. These findings highlight, extend, and generalize previous regional-scale findings on diel migratory insect movement patterns to the whole of temperate Europe. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Predicting resilience of migratory birds to environmental change.

The pace and scale of environmental change represent major challenges to many organisms. Animals that move long distances, such as migratory birds, are especially vulnerable to change since they need chains of intact habitat along their migratory routes. Estimating the resilience of such species to environmental changes assists in targeting conservation efforts. We developed a migration modeling framework to predict past (1960s), present (2010s), and future (2060s) optimal migration strategies across five shorebird species (Scolopacidae) within the East Asian-Australasian Flyway, which has seen major habitat deterioration and loss over the last century, and compared these predictions to empirical tracks from the present. Our model captured the migration strategies of the five species and identified the changes in migrations needed to respond to habitat deterioration and climate change. Notably, the larger species, with single or few major stopover sites, need to establish new migration routes and strategies, while smaller species can buffer habitat loss by redistributing their stopover areas to novel or less-used sites. Comparing model predictions with empirical tracks also indicates that larger species with the stronger need for adaptations continue to migrate closer to the optimal routes of the past, before habitat deterioration accelerated. Our study not only quantifies the vulnerability of species in the face of global change but also explicitly reveals the extent of adaptations required to sustain their migrations. This modeling framework provides a tool for conservation planning that can accommodate the future needs of migratory species.

Duration and variability of spring green-up mediate population consequences of climate change.

Single phenological measures, like the average rate of phenological advancement, may be insufficient to explain how climate change is driving trends in animal populations. Here, we develop a multifactorial concept of spring phenology-including the onset of spring, spring duration, interannual variability, and their temporal changes-as a driver for population dynamics of migratory terrestrial species in seasonal environments. Using this conceptual model, we found that effects of advancing spring phenology on animal populations may be buffered or amplified depending on the duration and interannual variability of spring green-up, and those effects are modified by evolutionary and plastic adaptations of species. Furthermore, we compared our modelling results with empirical data on normalized difference vegetation index-based spring green-up phenology and population trends of 106 European landbird finding similar associations. We conclude how phenological changes are expected to affect migratory bird populations across Europe and identify regions that are particularly prone to suffer population declines.

The association between haemosporidian infection and non-breeding moult location in great reed warblers revisited by combining feather stable isotope profiles and geolocator data.

Stable isotope analysis provides valuable insights into the ecology of long-distance migratory birds during periods spent away from a specific study site. In a previous study, Swedish great reed warblers (Acrocephalus arundinaceus) infected with haemosporidian parasites differed in feather isotope ratios compared to non-infected birds, suggesting that infected and non-infected birds spent the non-breeding season in different locations or habitats. Here, we use a novel dataset comprising geolocator data, isotopes, and haemosporidian infection status of 92 individuals from four Eurasian populations to investigate whether parasite transmission varies with geography or habitats. We found that the probability of harbouring Plasmodium and Leucocytozoon parasites was higher in birds moulting in the eastern region of the non-breeding grounds. However, no geographic pattern occurred for Haemoproteus infections or overall infection status. In contrast to the previous study, we did not find any relationship between feather isotope ratios and overall haemosporidian infection for the entire current dataset. Plasmodium-infected birds had lower feather δ15N values indicating that they occupied more mesic habitats. Leucocytozoon-infected birds had higher feather δ34S values suggesting more coastal sites or wetlands with anoxic sulphate reduction. As the composition and prevalence of haemosporidian parasites differed between the old and the current dataset, we suggest that the differences might be a consequence of temporal dynamics of haemosporidian parasites. Our results emphasize the importance of replicating studies conducted on a single population over a restricted time period, as the patterns can become more complex for data from wider geographical areas and different time periods.

Favorable winds speed up bird migration in spring but not in autumn.

Wind has a significant yet complex effect on bird migration speed. With prevailing south wind, overall migration is generally faster in spring than in autumn. However, studies on the difference in airspeed between seasons have shown contrasting results so far, in part due to their limited geographical or temporal coverage. Using the first full-year weather radar data set of nocturnal bird migration across western Europe together with wind speed from reanalysis data, we investigate variation of airspeed across season. We additionally expand our analysis of ground speed, airspeed, wind speed, and wind profit variation across time (seasonal and daily) and space (geographical and altitudinal). Our result confirms that wind plays a major role in explaining both temporal and spatial variabilities in ground speed. The resulting airspeed remains relatively constant at all scales (daily, seasonal, geographically and altitudinally). We found that spring airspeed is overall 5% faster in Spring than autumn, but we argue that this number is not significant compared to the biases and limitation of weather radar data. The results of the analysis can be used to further investigate birds' migratory strategies across space and time, as well as their energy use.

Short- and long-distance avian migrants differ in exercise endurance but not aerobic capacity.

BACKGROUND: Migratory birds differ markedly in their migration strategies, particularly those performing short- versus long-distance migrations. In preparation for migration, all birds undergo physiological and morphological modifications including enlargement of fat stores and pectoral muscles to fuel and power their flights, as well as cardiovascular and biochemical adjustments that improve lipid and oxygen delivery and uptake by flight muscles. While the magnitude of these changes varies in relation to migration strategy, the consequence of these variations on aerobic performance is unknown. We tested whether the aerobic performance of four Old-world flycatcher species (Muscicapidae) varied according to migration strategy by comparing minimum resting metabolic rates (RMRmin), exercise-induced maximum metabolic rates (MMR), and exercise endurance times of short-distance and long-distance migratory birds. RESULTS: As expected, RMRmin did not vary between short-distance and long-distance migrants but differed between the species within a migration strategy and between sexes. Unexpectedly, MMR did not vary with migration strategy, but MMR and blood haemoglobin content were positively related among the birds tested. Exercise endurance times differed substantially between migration strategies with long-distance migrants sustaining exercise for > 60% longer than short-distance migrants. Blood haemoglobin content had a significant positive effect on endurance among all birds examined. CONCLUSIONS: The lack of difference in RMRmin and MMR between long- and short-distance migrants during this stage of migration suggests that the attributes favouring the greater aerobic endurance of long-distance migrants did not come at the expense of increased maintenance costs or require greater aerobic capacity.

Quantifying year-round nocturnal bird migration with a fluid dynamics model.

To understand the influence of biomass flows on ecosystems, we need to characterize and quantify migrations at various spatial and temporal scales. Representing the movements of migrating birds as a fluid, we applied a flow model to bird density and velocity maps retrieved from the European weather radar network, covering almost a year. We quantified how many birds take-off, fly, and land across Western Europe to (1) track bird migration waves between nights, (2) cumulate the number of birds on the ground and (3) quantify the seasonal flow into and out of the study area through several regional transects. Our results identified several migration waves that crossed the study area in 4 days only and included up to 188 million (M) birds that took-off in a single night. In spring, we estimated that 494 M birds entered the study area, 251 M left it, and 243 M birds remained within the study area. In autumn, 314 M birds entered the study area while 858 M left it. In addition to identifying fundamental quantities, our study highlights the potential of combining interdisciplinary data and methods to elucidate the dynamics of avian migration from nightly to yearly time scales and from regional to continental spatial scales.

Effects of blood parasite infections on spatiotemporal migration patterns and activity budgets in a long-distance migratory passerine.

How blood parasite infections influence the migration of hosts remains a lively debated issue as past studies found negative, positive, or no response to infections. This particularly applies to small birds, for which monitoring of detailed migration behavior over a whole annual cycle has been technically unachievable so far. Here, we investigate how bird migration is influenced by parasite infections. To this end, we tracked great reed warblers (Acrocephalus arundinaceus) with multisensor loggers, characterized general migration patterns as well as detailed flight bout durations, resting times and flight heights, and related these to the genus and intensity of their avian haemosporidian infections. We found migration distances to be shorter and the onset of autumn migration to be delayed with increasing intensity of blood parasite infection, in particular for birds with Plasmodium and mixed-genus infections. Additionally, the durations of migratory flight bout were prolonged for infected compared to uninfected birds. But since severely infected birds and particularly birds with mixed-genus infections had shorter resting times, initial delays seemed to be compensated for and the timing in other periods of the annual cycle was not compromised by infection. Overall, our multisensor logger approach revealed that avian blood parasites have mostly subtle effects on migratory performance and that effects can occur in specific periods of the year only.

Climatic drivers of (changes in) bat migration phenology at Bracken Cave (USA).

Climate change is drastically changing the timing of biological events across the globe. Changes in the phenology of seasonal migrations between the breeding and wintering grounds have been observed across biological taxa, including birds, mammals, and insects. For birds, strong links have been shown between changes in migration phenology and changes in weather conditions at the wintering, stopover, and breeding areas. For other animal taxa, the current understanding of, and evidence for, climate (change) influences on migration still remains rather limited, mainly due to the lack of long-term phenology datasets. Bracken Cave in Texas (USA) holds one of the largest bat colonies of the world. Using weather radar data, a unique 23-year (1995-2017) long time series was recently produced of the spring and autumn migration phenology of Brazilian free-tailed bats (Tadarida brasiliensis) at Bracken Cave. Here, we analyse these migration phenology time series in combination with gridded temperature, precipitation, and wind data across Mexico and southern USA, to identify the climatic drivers of (changes in) bat migration phenology. Perhaps surprisingly, our extensive spatiotemporal search did not find temperature to influence either spring or autumn migration. Instead, spring migration phenology seems to be predominantly driven by wind conditions at likely wintering or spring stopover areas during the migration period. Autumn migration phenology, on the other hand, seems to be dominated by precipitation to the east and north-east of Bracken Cave. Long-term changes towards more frequent migration and favourable wind conditions have, furthermore, allowed spring migration to occur 16 days earlier. Our results illustrate how some of the remaining knowledge gaps on the influence of climate (change) on bat migration and abundance can be addressed using weather radar analyses.

Environmental variability, reliability of information and the timing of migration.

The timing of migration and migratory steps is highly relevant for fitness. Because environmental conditions vary between years, the optimal time for migration varies accordingly. Therefore, migratory animals could clearly benefit from acquiring information as to when it is the best time to migrate in a specific year. Thus, environmental predictability and variability are fundamental characteristics of migration systems but their relationship and consequence for migratory progression has remained unexplored. We develop a simple dynamic model to identify the optimal migration behaviour in environments that differ in predictability, variability and the number of intermediate stop-over sites. Our results indicate that higher predictability along migration routes enables organisms to better time migration when phenology deviates from its long-term average and thus, increases fitness. Information is particularly valuable in highly variable environments and in the final migration-step, i.e. before the destination. Furthermore, we show that a general strategy for obtaining information in relatively uninformative but variable environments is using intermediate stop-over sites that enable migrants to better predict conditions ahead. Our study contributes to a better understanding of the relationship between animal movement and environmental predictability-an important, yet underappreciated factor that strongly influences migratory progression.

Light-level geolocator analyses: A user's guide.

Light-level geolocator tags use ambient light recordings to estimate the whereabouts of an individual over the time it carried the device. Over the past decade, these tags have emerged as an important tool and have been used extensively for tracking animal migrations, most commonly small birds. Analysing geolocator data can be daunting to new and experienced scientists alike. Over the past decades, several methods with fundamental differences in the analytical approach have been developed to cope with the various caveats and the often complicated data. Here, we explain the concepts behind the analyses of geolocator data and provide a practical guide for the common steps encompassing most analyses - annotation of twilights, calibration, estimating and refining locations, and extraction of movement patterns - describing good practices and common pitfalls for each step. We discuss criteria for deciding whether or not geolocators can answer proposed research questions, provide guidance in choosing an appropriate analysis method and introduce key features of the newest open-source analysis tools. We provide advice for how to interpret and report results, highlighting parameters that should be reported in publications and included in data archiving. Finally, we introduce a comprehensive supplementary online manual that applies the concepts to several datasets, demonstrates the use of open-source analysis tools with step-by-step instructions and code and details our recommendations for interpreting, reporting and archiving.

A full annual perspective on sex-biased migration timing in long-distance migratory birds.

In many taxa, the most common form of sex-biased migration timing is protandry-the earlier arrival of males at breeding areas. Here we test this concept across the annual cycle of long-distance migratory birds. Using more than 350 migration tracks of small-bodied trans-Saharan migrants, we quantify differences in male and female migration schedules and test for proximate determinants of sex-specific timing. In autumn, males started migration about 2 days earlier, but this difference did not carry over to arrival at the non-breeding sites. In spring, males on average departed from the African non-breeding sites about 3 days earlier and reached breeding sites ca 4 days ahead of females. A cross-species comparison revealed large variation in the level of protandry and protogyny across the annual cycle. While we found tight links between individual timing of departure and arrival within each migration season, only for males the timing of spring migration was linked to the timing of previous autumn migration. In conclusion, our results demonstrate that protandry is not exclusively a reproductive strategy but rather occurs year-round and the two main proximate determinants for the magnitude of sex-biased arrival times in autumn and spring are sex-specific differences in departure timing and migration duration.

Moult-related reduction of aerobic scope in passerine birds.

It is well established that the nutrient and energy requirements of birds increase substantially during moult, but it is not known if these increased demands affect their aerobic capacity. We quantified the absolute aerobic scope of house and Spanish sparrows, Passer domesticus and P. hispaniolensis, respectively, before and during sequential stages of their moult period. The absolute aerobic scope (AAS) is the difference between maximum metabolic rate (MMR) during peak locomotor activities and minimum resting metabolic rate (RMRmin), thus representing the amount of aerobic power above that committed to maintenance needs available for other activities. As expected, RMRmin increased over the moult period by up to 40 and 63% in house and Spanish sparrows, respectively. Surprisingly, the maximum metabolic rates also decreased during moult in both species, declining as much as 25 and 38% compared with pre-moult values of house and Spanish sparrows, respectively. The concurrent changes in RMRmin and MMR during moult resulted in significant decreases in AAS, being up to 32 and 47% lower than pre-moult levels of house and Spanish sparrows, respectively, during moult stages having substantial feather replacement. We argue that the combination of reduced flight efficiency due to loss of wing feathers and reduced aerobic capacity places moulting birds at greater risk of predation. Such performance constraints likely contribute to most birds temporally separating moult from annual events requiring peak physiological capacity such as breeding and migration.

Miniaturized multi-sensor loggers provide new insight into year-round flight behaviour of small trans-Sahara avian migrants.

BACKGROUND: Over the past decade, the miniaturisation of animal borne tags such as geolocators and GPS-transmitters has revolutionized our knowledge of the whereabouts of migratory species. Novel light-weight multi-sensor loggers (1.4 g), which harbour sensors for measuring ambient light intensity, atmospheric pressure, temperature and acceleration, were fixed to two long-distance migrant bird species - eurasian hoopoe (Upupa epops) and great reed warbler (Acrocephalus arundinaceus). Using acceleration and atmospheric pressure data recorded every 5 and 30 min, respectively, we aimed at reconstructing individual diurnal and seasonal patterns of flight activity and flight altitude and thereby, at describing basic, yet hitherto unknown characteristics of migratory flight behaviour. Furthermore, we wanted to characterise the variability in these migration characteristics between individuals, species and migration periods. RESULTS: The flight duration from breeding to sub-Saharan African non-breeding sites and back was more variable within than between the species. Great reed warblers were airborne for a total of 252 flight hours and thus, only slightly longer than eurasian hoopoes with 232 h. With a few exceptions, both species migrated predominantly nocturnally - departure around dusk and landing before dawn. Mean flight altitudes were higher during pre- than during post-breeding migration (median 1100 to 1600 m a.s.l.) and flight above 3000 m occurred regularly with a few great reed warblers exceeding 6000 m a.s.l. (max. 6458 m a.s.l.). Individuals changed flight altitudes repeatedly during a flight bout, indicating a continuous search for (more) favourable flight conditions. CONCLUSIONS: We found high variation between individuals in the flight behaviour parameters measured - a variation that surprisingly even exceeded the variation between the species. More importantly, our results have shown that multi-sensor loggers have the potential to provide detailed insights into many fundamental aspects of individual behaviour in small aerial migrants. Combining the data recorded on the multiple sensors with, e.g., remote sensing data like weather and habitat quality on the spatial and temporal scale will be a great step forward to explore individual decisions during migration and their consequences.

Host migration strategy and blood parasite infections of three sparrow species sympatrically breeding in Southeast Europe.

Mobile hosts like birds occupy a wide array of habitats in which they encounter various vector and parasite faunas. If the infection probability for vector-borne parasites varies among seasons and biomes, a migratory life can critically influence the infections of a host. The growing body of literature on avian blood parasites suggests that host migrations do not only influence prevalence of infection but can also evoke higher infection intensities and increased parasite diversity in migrant compared to resident host species. We investigated the prevalence, intensity and diversity of Plasmodium and Haemoproteus infections in three closely-related and sympatrically breeding sparrow species with different migration strategies ranging from residential house sparrow and partially migratory tree sparrow to the obligate migratory Spanish sparrow. With a prevalence of 49%, the migratory Spanish sparrows were significantly less frequently infected than the resident house sparrows (82%). The partially migratory tree sparrow showed an intermediate prevalence of 60%. The parasitaemias were similar in all three host species and indicated mostly chronic but also few acute infections. While we found Plasmodium parasites in all three sparrow species, only Spanish sparrows were infected with Haemoproteus parasites in our study. With nine clearly identified parasite lineages in our study and the highest number of lineages per infected individuals (i.e. relative diversity), Spanish sparrows harboured the most diverse parasite fauna. Our results suggest that migration strategies can affect Plasmodium and Haemoproteus infections of sparrows resulting in a lower parasite prevalence and higher parasite diversity in migratory hosts-at least during our host's breeding period. A general scope for all annual cycle periods and across various bird taxa remains to be elucidated.

Spatiotemporal Group Dynamics in a Long-Distance Migratory Bird.

Thousands of species migrate [1]. Though we have some understanding of where and when they travel, we still have very little insight into who migrates with whom and for how long. Group formation is pivotal in allowing individuals to interact, transfer information, and adapt to changing conditions [2]. Yet it is remarkably difficult to infer group membership in migrating animals without being able to directly observe them. Here, we use novel lightweight atmospheric pressure loggers to monitor group dynamics in a small migratory bird, the European bee-eater (Merops apiaster). We present the first evidence of a migratory bird flying together with non-kin of different ages and sexes at all stages of the life cycle. In fact, 49% stay together throughout the annual cycle, never separating longer than 5 days at a time despite the ∼14,000-km journey. Of those that separated for longer, 89% reunited within less than a month with individuals they had previously spent time with, having flown up to 5,000 km apart. These birds were not only using the same non-breeding sites, but also displayed coordinated foraging behaviors-these are unlikely to result from chance encounters in response to the same environmental conditions alone. Better understanding of migratory group dynamics, using the presented methods, could help improve our understanding of collective decision making during large-scale movements.

Diverse migration strategies in hoopoes (Upupa epops) lead to weak spatial but strong temporal connectivity.

The annual cycle of migrating birds is shaped by their seasonal movements between breeding and non-breeding sites. Studying how migratory populations are linked throughout the annual cycle-migratory connectivity, is crucial to understanding the population dynamics of migrating bird species. This requires the consideration not only of spatial scales as has been the main focus to date but also of temporal scales: only when both aspects are taken into account, the degree of migratory connectivity can be properly defined. We investigated the migration behaviour of hoopoes (Upupa epops) from four breeding populations across Europe and characterised migration routes to and from the breeding grounds, location of non-breeding sites and the timing of key migration events. Migration behaviour was found to vary both within and amongst populations, and even though the spatial migratory connectivity amongst the populations was weak, temporal connectivity was strong with differences in timing amongst populations, but consistent timing within populations. The combination of diverse migration routes within populations and co-occurrence on the non-breeding grounds between populations might promote exchange between breeding populations. As a result, it might make hoopoes and other migrating bird species with similar strategies more resilient to future habitat or climatic changes and stabilise population trends.