RESUMEN
Migratory songbirds may navigate by extracting positional information from the geomagnetic field, potentially with a magnetic-particle-based receptor. Previous studies assessed this hypothesis experimentally by exposing birds to a strong but brief magnetic pulse aimed at remagnetizing the particles and evoking an altered behaviour. Critically, such studies were not ideally designed because they lacked an adequate sham treatment controlling for the induced electric field that is fundamentally associated with a magnetic pulse. Consequently, we designed a sham-controlled magnetic-pulse experiment, with sham and treatment pulse producing a similar induced electric field, while limiting the sham magnetic field to a value that is deemed insufficient to remagnetize particles. We tested this novel approach by pulsing more than 250 wild, migrating European robins (Erithacus rubecula) during two autumn seasons. After pulsing them, five traits of free-flight migratory behaviour were observed, but no effect of the pulse could be found. Notably, one of the traits, the migratory motivation of adults, was significantly affected in only one of the two study years. Considering the problem of reproducing experiments with wild animals, we recommend a multi-year approach encompassing large sample size, blinded design and built-in sham control to obtain future insights into the role of magnetic-particle-based magnetoreception in bird navigation.
Asunto(s)
Migración Animal , Pájaros Cantores , Animales , Pájaros Cantores/fisiología , Migración Animal/fisiología , Campos Magnéticos , Vuelo Animal/fisiologíaRESUMEN
Migrating animals perform astonishing seasonal movements by orienting and navigating over thousands of kilometres with great precision. Many migratory species use cues from the sun, stars, landmarks, olfaction and the Earth's magnetic field for this task. Among vertebrates, songbirds are the most studied taxon in magnetic-cue-related research. Despite multiple studies, we still lack a clear understanding of when, where and how magnetic cues affect the decision-making process of birds and hence, their realised migratory behaviour in the wild. This understanding is especially important to interpret the results of laboratory experiments in an ecologically appropriate way. In this review, we summarise the current findings about the role of magnetic cues for migratory decisions in songbirds. First, we review the methodological principles for orientation and navigation research, specifically by comparing experiments on caged birds with experiments on free-flying birds. While cage experiments can show the sensory abilities of birds, studies with free-flying birds can characterise the ecological roles of magnetic cues. Second, we review the migratory stages, from stopover to endurance flight, in which songbirds use magnetic cues for their migratory decisions and incorporate this into a novel conceptual framework. While we lack studies examining whether and when magnetic cues affect orientation or navigation decisions during flight, the role of magnetic cues during stopover is relatively well studied, but mostly in the laboratory. Notably, many such studies have produced contradictory results so that understanding the biological importance of magnetic cues for decisions in free-flying songbirds is not straightforward. One potential explanation is that reproducibility of magnetic-cue experiments is low, probably because variability in the behavioural responses of birds among experiments is high. We are convinced that parts of this variability can be explained by species-specific and context-dependent reactions of birds to the study conditions and by the bird's high flexibility in whether they include magnetic cues in a decision or not. Ultimately, this review should help researchers in the challenging field of magnetoreception to design experiments meticulously and interpret results of such studies carefully by considering the migration ecology of their focal species.
Asunto(s)
Migración Animal , Señales (Psicología) , Pájaros Cantores , Animales , Migración Animal/fisiología , Pájaros Cantores/fisiología , Campos MagnéticosRESUMEN
AbstractMigrating birds perform extreme endurance exercise when flying. This shifts the balance between the production of reactive oxygen species and the antioxidant defense system toward the former, potentially generating oxidative damages. In between migratory flights, birds make stopovers, where besides accumulating fuel (mainly fats), they are assumed to rest and recover from the strenuous flight. We performed a series of studies on both temporarily caged (northern wheatears) and free-flying (northern wheatears and European robins) migrants to investigate whether migrants recover during stopover by decreasing the amount of oxidative lipid damage (malondialdehyde [MDA]) and/or increasing the total nonenzymatic antioxidant capacity (AOX). In caged wheatears, MDA decreased within a single day. These birds were able to simultaneously accumulate considerable amounts of fuel. Also, in the free-flying wheatears, there was a decrease in MDA during stopover; however, this process seemed incompatible with refueling. The reason for this difference could relate to constraints in the wild that are absent in caged birds, such as food limitation/composition and locomotor activity. In the robins, there was a near significant decrease in MDA concentration in relation to how long the birds were already at stopover, suggesting that this species also physiologically recovers during stopover. AOX did not change during stopover in either of the wheatear studies. For the robins, however, uric acid-corrected AOX declined during stopover. Our results show that during stopover, migrating birds rapidly reduce oxidative lipid damage, thereby likely recovering their physiological state. In addition to the commonly accepted function of refueling, stopovers thus probably serve physiological recovery.
Asunto(s)
Antioxidantes , Pájaros Cantores , Animales , Pájaros Cantores/fisiología , Alimentos , Lípidos , Migración Animal/fisiología , Estaciones del AñoRESUMEN
BACKGROUND: Birds have extremely elevated metabolic rates during migratory endurance flight and consequently can become physiologically exhausted. One feature of exhaustion is oxidative damage, which occurs when the antioxidant defense system is overwhelmed by the production of damaging reactive oxygen species (ROS). Migrating birds have been shown to decrease the amount of oxidative lipid damage during stopovers, relatively stationary periods in between migratory flights. It has therefore been argued that, in addition to accumulating fuel, one of the functions of stopover is to restore the oxidative balance. If this is so, we would expect that migrating birds are unlikely to resume migration from stopover when they still have high amounts of lipid damage. METHODS: To test this hypothesis, we measured parameters of the oxidative balance and related these to stopover departure decisions of song thrushes (Turdus philomelos) and northern wheatears (Oenanthe oenanthe), a medium- and long-distance songbird migrant, respectively. We measured malondialdehyde (MDA) concentration, a biomarker for oxidative lipid damage, and total non-enzymatic antioxidant capacity (AOX), an overall biomarker of protection against ROS. Stopover departure decisions were determined using a fully automated telemetry system set-up on our small island study site. RESULTS: The decision to resume migration was not related with MDA concentration in either study species, also not when this was corrected for circulating fatty acid concentrations. Similarly, AOX did not affect this decision, also not when corrected for uric-acid concentration. The time within the night when birds departed also was not affected by MDA concentration or AOX. However, confirming earlier observations, we found that in both species, fat individuals were more likely to depart than lean individuals, and fat northern wheatears departed earlier within the night than lean conspecifics. Northern wheatears additionally departed earlier in spring with more southerly winds. CONCLUSIONS: We found no support for the idea that stopovers departure decisions are influenced by parameters of the oxidative balance. We discuss possible reasons for this unexpected finding.
RESUMEN
Current evidence suggests that migratory animals extract map information from the geomagnetic field for true navigation. The sensory basis underlying this feat is elusive, but presumably involves magnetic particles. A common experimental manipulation procedure consists of pre-treating animals with a magnetic pulse, with the aim of re-magnetising particles to alter the internal representation of the external field prior to a navigation task. Although pulsing provoked deflected bearings in caged songbirds, analogous studies with free-flying songbirds yielded inconsistent results. Here, we pulsed European robins (Erithacus rubecula) at an offshore stopover site during spring migration and monitored their free-flight behaviour with a regional-scale network of radio-receiving stations. We found no pulse effect on departure probability, nocturnal departure timing departure direction or consistency of flight direction. This suggests either no use of the geomagnetic map by our birds, or that magnetic pulses do not affect the sensory system underlying geomagnetic map detection.
Asunto(s)
Pájaros Cantores , Migración Animal , Animales , Fenómenos Magnéticos , Magnetismo , Estaciones del AñoRESUMEN
Naïve migrants reach their wintering grounds following a clock-and-compass strategy. During these inaugural migrations, birds internalise, among others, cues from the Earth's magnetic field to create a geomagnetic map, with which they navigate to destinations familiar to them on subsequent migrations. Geomagnetic map cues are thought to be sensed by a magnetic-particle-based receptor, which can be specifically affected by a magnetic pulse. Indeed, the orientation of experienced but not naïve birds was compromised after magnetic pulsing, indicating geomagnetic map use. Little is known about the importance of this putative magnetoreceptor for navigation and decision-making in free-flying migrants. Therefore, we studied in unprecedented detail how a magnetic pulse would affect departure probability, nocturnal departure timing, departure direction and consistency in flight direction over 50-100 km in experienced and naïve long-distant migrant songbirds using a large-scale radio-tracking system. Contrary to our expectations and despite a high sample size (ntotal = 137) for a free-flight study, we found no significant after-effect of the magnetic pulse on the migratory traits, suggesting the geomagnetic map is not essential for the intermediate autumn migration phase. These findings warrant re-thinking about perception and use of geomagnetic maps for migratory decisions within a sensory and ecological context.
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Oenanthe , Pájaros Cantores , Migración Animal , Animales , Campos MagnéticosRESUMEN
The light-dependent magnetic compass sense of night-migratory songbirds can be disrupted by weak radiofrequency fields. This finding supports a quantum mechanical, radical-pair-based mechanism of magnetoreception as observed for isolated cryptochrome 4, a protein found in birds' retinas. The exact identity of the magnetically sensitive radicals in cryptochrome is uncertain in vivo, but their formation seems to require a bound flavin adenine dinucleotide chromophore and a chain of four tryptophan residues within the protein. Resulting from the hyperfine interactions of nuclear spins with the unpaired electrons, the sensitivity of the radicals to radiofrequency magnetic fields depends strongly on the number of magnetic nuclei (hydrogen and nitrogen atoms) they contain. Quantum-chemical calculations suggested that electromagnetic noise in the frequency range 75-85 MHz could give information about the identity of the radicals involved. Here, we show that broadband 75-85 MHz radiofrequency fields prevent a night-migratory songbird from using its magnetic compass in behavioural experiments. These results indicate that at least one of the components of the radical pair involved in the sensory process of avian magnetoreception must contain a substantial number of strong hyperfine interactions as would be the case if a flavin-tryptophan radical pair were the magnetic sensor.
Asunto(s)
Pájaros Cantores , Taxia , Migración Animal , Animales , Criptocromos/metabolismo , Flavinas , Campos Magnéticos , Pájaros Cantores/metabolismo , TriptófanoRESUMEN
BACKGROUND: The long-tailed duck (Clangula hyemalis) was categorized as ´Vulnerable` by the IUCN after a study revealed a rapid wintering population decline of 65% between 1992-1993 and 2007-2009 in the Baltic Sea. As knowledge about the European long-tailed duck's life cycle and movement ecology is limited, we investigate its year-round spatiotemporal distribution patterns. Specifically, we aimed to identify the wintering grounds, timing of migration and staging of this population via light-level geolocation. RESULTS: Of the 48 female long-tailed ducks tagged on Kolguev Island (western Russian Arctic), 19 were recaptured to obtain data. After breeding and moulting at freshwater lakes, ducks went out to sea around Kolguev Island and to marine waters ranging from the White Sea to Novaya Zemlya Archipelago for 33 ± 10 days. After a rapid autumn migration, 18 of 19 birds spent their winter in the Baltic Sea and one bird in the White Sea, where they stayed for 212 ± 3 days. There, they used areas known to host long-tailed ducks, but areas differed among individuals. After a rapid spring migration in mid-May, the birds spent 23 ± 3 days at sea in coastal areas between the White Sea and Kolguev Island, before returning to their freshwater breeding habitats in June. CONCLUSIONS: The Baltic Sea represents the most important wintering area for female long-tailed ducks from Kolguev Island. Important spring and autumn staging areas include the Barents Sea and the White Sea. Climate change will render these habitats more exposed to human impacts in the form of fisheries, marine traffic and oil exploitation in near future. Threats that now operate in the wintering areas may thus spread to the higher latitude staging areas and further increase the pressure on long-tailed ducks.