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Light-dependent magnetic compass in Iberian green frog tadpoles
Abstract
Here, we provide evidence for a wavelength-dependent effect of light on magnetic compass orientation in Pelophylax perezi (order Anura), similar to that observed in Rana catesbeiana (order Anura) and Notophthalmus viridescens (order Urodela), and confirm for the first time in an anuran amphibian that a 90° shift in the direction of magnetic compass orientation under long-wavelength light (≥ 500 nm) is due to a direct effect of light on the underlying magnetoreception mechanism. Although magnetic compass orientation in other animals (e.g., birds and some insects) has been shown to be influenced by the wavelength and/or intensity of light, these two amphibian orders are the only taxa for which there is direct evidence that the magnetic compass is light-dependent. The remarkable similarities in the light-dependent magnetic compasses of anurans and urodeles, which have evolved as separate clades for at least 250 million years, suggest that the light-dependent magnetoreception mechanism is likely to have evolved in the common ancestor of the Lissamphibia (Early Permian, ~294 million years) and, possibly, much earlier. Also, we discuss a number of similarities between the functional properties of the light-dependent magnetic compass in amphibians and blue light-dependent responses to magnetic stimuli in Drosophila melanogaster, which suggest that the wavelength-dependent 90° shift in amphibians may be due to light activation of different redox forms of a cryptochrome photopigment. Finally, we relate these findings to earlier studies showing that the pineal organ of newts is the site of the light-dependent magnetic compass and recent neurophysiological evidence showing magnetic field sensitivity in the frog frontal organ (an outgrowth of the pineal).
... One magnetoreception mechanism provides a source of directional ('compass') information used for shoreward orientation, as well as for the compass component of homing (Phillips 1986a(Phillips ,b, 1987Diego-Rasilla 2003;Diego-Rasilla et al. 2005. The magnetic compass is mediated by a light-dependent magnetoreception mechanism in both newts (Phillips and Borland 1992a,b,c;Deutschlander et al. 1999a,b;Phillips et al. 2001;Diego-Rasilla et al. 2015) and frogs (Freake and Phillips 2005;Diego-Rasilla et al. 2010, 2013Diego-Rasilla and Luengo 2020), and is proposed to involve a light-absorbing molecule that forms radical-pair intermediates, i.e., radical pair mechanism (Schulten and Windemuth 1986;Ritz et al. 2000;Phillips et al. 2010;Kattnig 2020, 2021). Consistent with the involvement of a light-dependent mechanism, newts are not able to use the magnetic compass for shoreward orientation (i.e., 'Y-axis orientation'; N. viridescens; Phillips and Borland 1992c) or homeward orientation (I. ...
... Behavioral experiments with both amphibians and birds have shown that magnetic compass orientation can be altered or eliminated under long-wavelength light (Phillips and Borland, 1992a,b;Wiltschko et al. 1993Wiltschko et al. , 2007Wiltschko et al. , 2011Wiltschko 1995, 2001;Möller et al. 2001;Deutschlander et al. 1999a,b;Rappl et al. 2000;Freake and Phillips 2005;Diego-Rasilla et al. 2010, 2013 Diego-Rasilla and Luengo 2020). However, changes in behavior under long-wavelength light alone do not make a compelling case for reliance on a light-dependent magnetoreception mechanism (see Supplementary Materials). ...
... Evidence for a similar light-dependent magnetic compass has been obtained in studies of tadpoles of Lithobates catesbeianus (bullfrog), Pelophylax perezi (Iberian green frog), and Rana temporaria (European common frog) (Freake and Phillips 2005;Diego-Rasilla et al. 2010, 2013, and in larval L. helveticus (palmate newt) (Diego-Rasilla et al. 2015) (Fig. 7). ...
Sensitivity to the earth’s magnetic field is the least understood of the major sensory systems, despite being virtually ubiquitous in animals and of widespread interest to investigators in a wide range of fields from behavioral ecology to quantum physics. Although research on the use of magnetic cues by migratory birds, fish, and sea turtles is more widely known, much of our current understanding of the functional properties of vertebrate magnetoreception has come from research on amphibians. Studies of amphibians established the presence of a light-dependent magnetic compass, a second non-light-dependent mechanism involving particles of magnetite and/or maghemite, and an interaction between these two magnetoreception mechanisms that underlies the “map” component of homing. Simulated magnetic displacement experiments demonstrated the use of a high-resolution magnetic map for short-range homing to breeding ponds requiring a sampling strategy to detect weak spatial gradients in the magnetic field despite daily temporal variation at least an order of magnitude greater. Overall, reliance on a magnetic map for short-range homing places greater demands on the underlying sensory detection, processing, and memory mechanisms than comparable mechanisms used by long-distance migrants. Moreover, unlike sea turtles and migratory birds, amphibians are exceptionally well suited to serve as model organisms in which to characterize the molecular and biophysical mechanisms underlying the light-dependent ‘quantum compass’.
... Y-axis magnetic compass orientation in amphibians has been shown to be mediated by a light-dependent magnetoreception mechanism (Deutschlander et al., 1999a,b;Diego-Rasilla et al., 2010;Borland 1992a, 1999b;Phillips and Borland, 1999b;Phillips et al., 2001). Furthermore, the light-dependent magnetic compass exhibits similar features in larval frogs and adult newts (Deutschlander et al., 1999a,b;Diego-Rasilla et al., 2010;Phillips et al., 2001Phillips et al., , 2010. ...
... Y-axis magnetic compass orientation in amphibians has been shown to be mediated by a light-dependent magnetoreception mechanism (Deutschlander et al., 1999a,b;Diego-Rasilla et al., 2010;Borland 1992a, 1999b;Phillips and Borland, 1999b;Phillips et al., 2001). Furthermore, the light-dependent magnetic compass exhibits similar features in larval frogs and adult newts (Deutschlander et al., 1999a,b;Diego-Rasilla et al., 2010;Phillips et al., 2001Phillips et al., , 2010. In both groups, the light-dependent mag- netic compass relies on a magnetoreception system receiving two antagonistic inputs, i.e., a high-sensitivity short-wavelength mech- anism and a low-sensitivity long-wavelength mechanism . ...
... In both groups, the light-dependent mag- netic compass relies on a magnetoreception system receiving two antagonistic inputs, i.e., a high-sensitivity short-wavelength mech- anism and a low-sensitivity long-wavelength mechanism . Y-axis magnetic compass orientation of larval frogs and adult newts tested under natural light is indistinguishable from the orientation of those tested under short-wavelength light, showing that full-spectrum light preferentially excites the more sensi- tive short-wavelength input, whilst the long-wavelength input is excited by wavelengths >500 nm (Deutschlander et al., 1999a;Diego-Rasilla et al., 2010). The antagonistic inputs produce a wavelength-dependent 90 • shift in the direction of y-axis mag- netic compass orientation that has been shown to result from a direct effect of light on the underlying magnetoreception mecha- nism ( Diego-Rasilla et al., 2010Phillips and Borland, 1992a). ...
Experiments were conducted to investigate whether larval palmate newts undertake orientation toward or away from the home shoreline (y-axis orientation) using the geomagnetic field to steer the most direct route, and if they accomplish this task through a light-dependent magnetoreception mechanism similar to that found in anuran tadpoles and adult newts. Larval palmate newts trained and then tested under full-spectrum light showed bimodal magnetic compass orientation that coincided with the magnetic direction of the trained y-axis. In contrast, larvae trained under long-wavelength (≥ 500nm) light and then tested under full-spectrum light displayed bimodal orientation perpendicular to the trained y-axis direction. These results offer evidence for the use of magnetic compass cues in orienting urodele amphibian larvae, and provide additional support for the light-dependent magnetoreception mechanism since they are in complete agreement with earlier studies showing that the observed 90° shift in the direction of magnetic compass orientation under long-wavelength light (≥500nm) is due to a direct effect of light on the underlying magnetoreception mechanism. This study is the first to provide evidence of a light-dependent magnetic compass in larval urodeles.
Copyright © 2015. Published by Elsevier B.V.
... Tadpoles are an excellent model system to study the sensory inputs involved in y-axis orientation because they will spontaneously learn the compass direction of the y-axis in a training tank with an artificial shore. Moreover, previous experiments have demonstrated that frog tadpoles are able to learn the direction of an artificial shore within a few days, e.g., 7-day training experiments (Freake et al. 2002;Freake and Phillips 2005) and 5-day training experiments (Diego-Rasilla and Phillips 2007;Diego-Rasilla et al. 2010). ...
... To date, only two species of anurans have been shown to rely on a magnetic compass for y-axis orientation, tadpoles of the bullfrog Lithobates catesbeianus (Freake et al. 2002) and tadpoles of the Iberian green frog Pelophylax perezi (Diego-Rasilla and Phillips 2007). There is also evidence that magnetic compass orientation is light-dependent in tadpoles of both two species of frogs (Freake and Phillips 2005;Diego-Rasilla et al. 2010). Interestingly, the lightdependent magnetic compass of frogs show similar features to that observed in the Eastern red-spotted newt Nothopthalmus viridescens (Phillips and Borland 1992a, b;Deutschlander et al. 1999a, b;Phillips et al. 2001). ...
... The properties of the light-dependent magnetic compasses of both urodele and anuran amphibians are consistent with a magnetoreception that receives antagonistic input from a high-sensitivity short-wavelength sensitive mechanism and a low-sensitivity long-wavelength mechanism (Phillips and Borland 1992a;Phillips et al. 2010). The absolute sensitivity of the short-wavelength mechanism may be as much as two log units higher than that of the long-wavelength mechanism (Dodt and Heerd 1962); natural (i.e., full spectrum) lighting preferentially excites the short-wavelength input, while a highly saturated longwavelength stimulus (wavelengths [500 nm) that rarely, if ever, occurs under natural conditions is necessary to preferentially excite the long-wavelength input (Deutschlander et al. 1999a;Diego-Rasilla et al. 2010). ...
We provide evidence for the use of a magnetic compass for y-axis orientation (i.e., orientation along the shore-deep water axis) by tadpoles of the European common frog (Rana temporaria). Furthermore, our study provides evidence for a wavelength-dependent effect of light on magnetic compass orientation in amphibians. Tadpoles trained and then tested under full-spectrum light displayed magnetic compass orientation that coincided with the trained shore-deep water axes of their training tanks. Conversely, tadpoles trained under long-wavelength (≥500 nm) light and tested under full-spectrum light, and tadpoles trained under full-spectrum light and tested under long-wavelength (≥500 nm) light, exhibited a 90° shift in magnetic compass orientation relative to the trained y-axis direction. Our results are consistent with earlier studies showing that the observed 90° shift in the direction of magnetic compass orientation under long-wavelength (≥500 nm) light is due to a direct effect of light on the underlying magnetoreception mechanism. These findings also show that wavelength-dependent effects of light do not compromise the function of the magnetic compass under a wide range of natural lighting conditions, presumably due to a large asymmetry in the relatively sensitivity of antagonistic short- and long-wavelength inputs to the light-dependent magnetic compass.
... (2) Numerous studies demonstrate a wavelength-dependent effect of light on magnetic compass orientation in tadpoles of Alytes obstricans, Pelophylax perezi, R. temporaria and Lithobates catesbeianus (Diego-Rasilla and Luengo, 2020;Diego-Rasilla et al., 2010, 2013Freake and Phillips, 2005). This is important evidence in favor of the inclination compass as, in theory, the lightdependent chemical compass is inclinational (Ritz et al., 2000), but not crucial proof, as only the horizontal component was varied in these experiments. ...
... Thus, our data directly confirm that European common frogs can use the inclination compass for orientation along the Y-axis, as does N. viridescens (Phillips, 1986). This is also in good agreement with the wavelength-dependent effect of light on magnetic compass orientation in anuran tadpoles (Diego-Rasilla and Luengo, 2020;Diego-Rasilla et al., 2010, 2013Freake and Phillips, 2005). However, we wish to avoid unnecessary speculation regarding the physiological mechanisms of the frog compass, as our study does not address them, e.g. ...
Animals can use two variants of the magnetic compass: “polar compass” or “inclination compass”. Among vertebrates the compass type has been identified for the salmon, mole rats, birds, turtles, and urodeles. However, no experiments have been conducted to determine the compass variant in anurans. To elucidate this, we performed a series of field and laboratory experiments on males of the European common frog during the spawning season. In the field experiments in a large circular arena we identified the direction of stereotypic migration axis on a total of 581 frogs caught during migration from river to ponds or in a breeding pond. We also found that motivation of the frogs varied throughout the day, likely to avoid deadly night freezes, which are common in spring. The laboratory experiments were conducted on a total of 450 frogs in a T-maze placed in a three-axis Merritt coil system. The maze arms were positioned parallel to the natural migration axis inferred on the basis of magnetic field. Both vertical and horizontal components of the magnetic field were altered, and frogs were additionally tested in a vertical magnetic field. We conclude that European common frogs possess inclination magnetic compass, as do newts, birds, and sea turtles, and potentially use it during the spring migration. The vertical magnetic field confuses the frogs, apparently due to the inability to choose a direction. Notably, diurnal variation in motivation of the frogs was identical to that in nature, indicating the presence of internal rhythms controlling this process.
... Studies of birds and amphibians have provided evidence for a magnetic compass that is mediated by a light-dependent quantum process, the radical pair mechanism (RPM), in specialized photoreceptors. Properties of a RPM-based magnetic compass include: (1) sensitivity to the axis, but not polarity, of the magnetic field-animals with this type of 'inclination' compass use the slope or inclination of the magnetic field to distinguish 'poleward' vs. 'equatorward', rather than northward vs. southward, directions (Wiltschko and Wiltschko 1972;Phillips 1986), (2) qualitative changes in the pattern of magnetic input ("magnetic modulation pattern") that depend on magnetic field intensity (Wiltschko 1968;Wiltschko et al. 2006;Winklhofer et al. 2013; and see below), (3) dependence on the presence and/or wavelength of light (Semm et al. 1984;Phillips and Borland 1992a, b;Phillips and Sayeed 1993;Wiltschko et al. 1993;Deutschlander et al. 1999;Wiltschko and Wiltschko 2001;Muheim et al. 2002;Vacha et al. 2008;Diego-Rasilla et al. 2010;Pinzon-Rodriguez and Muheim 2017), (4) disruption by low-level radio frequency (RF) fields (Ritz et al. 2004;Engels et al. 2014;Hore and Mouritsen 2016; and see below). ...
... Moreover, intracellular recordings from the compound eye of flies have provided the only evidence, to date, for a direct effect of an earth-strength magnetic field on the response of a photoreceptor to light (Phillips et al. 2010a). The magnetic field's effect on fly photoreceptors is dependent on the axis, not the polarity, of the magnetic field, and undergoes a wavelength-dependent 90° shift in the axis of response to the magnetic field, consistent with the properties of the lightdependent magnetic compass in a variety of organisms (Phillips and Borland 1992a; Phillips and Sayeed 1993;Freake and Phillips 2005;Vacha et al. 2008;Diego-Rasilla et al. 2010). Consequently, studies of the magnetic compass of flies (Musca, Drosophila), as well as that of other vertebrates, may shed light on the functional properties of the magnetic compass in murine rodents, including sources of unexplained variability that have confounded efforts to better understand this sensory system. ...
A magnetic compass sense has been demonstrated in all major classes of vertebrates, as well as in many invertebrates. In mammals, controlled laboratory studies of mice have provided evidence for a robust magnetic compass that is comparable to, or exceeds, the performance of that in other animals. Nevertheless, the vast majority of laboratory studies of spatial behavior and cognition in murine rodents have failed to produce evidence of sensitivity to magnetic cues. Given the central role that a magnetic compass sense plays in the spatial ecology and cognition of non-mammalian vertebrates, and the potential utility that a global/universal reference frame derived from the magnetic field would have in mammals, the question of why responses to magnetic cues have been so difficult to demonstrate reliably is of considerable importance. In this paper, we review evidence that the magnetic compass of murine rodents shares a number of properties with light-dependent compasses in a wide variety of other animals generally believed to be mediated by a radical pair mechanism (RPM) or related quantum process. Consistent with the RPM, we summarize both published and previously unpublished findings suggesting that the murine rodent compass is sensitive to low-level radio frequency (RF) fields. Finally, we argue that the presence of anthropogenic RF fields in laboratory settings, may be an important source of variability in responses of murine rodents to magnetic cues.
... Adult individuals of other anuran species have not yet been studied, though there are publications demonstrating that tadpoles from Ranidae family (Lithobates catesbeianus, Pelophylax perezi, and Rana temporaria) can use a magnetic field to orient themselves along a so-called Y-axis-an angular direction towards the nearest coastal line (Freake et al. 2002;Freake and Phillips 2005;Diego-Rasilla et al. 2010, 2013. In our previous research, we managed to describe the behavior of adult individuals of Ranidae that could be ecologically appropriate as a model for the study of the probable magnetic orientation. ...
... Frogs in the breeding migratory state preferred to move to the "South-West" arm of the maze-that is in the direction, in which they migrate to spawning ponds in their natural habitat. This suggests that adult marsh frogs are able to choose a proper migratory direction guided by the Earth's magnetic field as was shown earlier in urodeles (Phillips 1986;Phillips et al. 2001Diego-Rasilla 2003 and the larvae of anurans (Freake et al. 2002;Freake and Phillips 2005;Diego-Rasilla et al. 2010, 2013. Frogs in the "wintering state" distributed equally between the two arms of the maze. ...
The publication is available at http://rdcu.be/mXEp
Orientation by magnetic cues appears to be adaptive during animal migrations. Whereas the magnetic orientation in birds, mammals, and urodele amphibians is being investigated intensively, the data about anurans are still scarce. This study tests whether marsh frogs could determine migratory direction between the breeding pond and the wintering site by magnetic cues in the laboratory. Adult frogs (N = 32) were individually tested in the T-maze 127 cm long inside the three-axis Helmholtz coil system (diameter 3 m). The arms of the maze were positioned parallel to the natural migratory route of this population when measured in accordance with magnetic field. The frogs were tested under two-motivational conditions mediated by temperature/light regime: the breeding migratory state and the wintering state. The frogs’ choice in a T-maze was evident only when analyzed in accordance with the direction of the magnetic field: they moved along the migratory route
to the breeding pond and followed the reversion of the horizontal component of the magnetic field. This preference has been detected in both sexes only in the breeding migratory state. This suggests that adult ranid frogs can obtain directional information from the Earth’s magnetic field as was shown earlier in urodeles and anuran larvae.
... Magnetic compass orientation in birds (migratory and non-migratory) and several species of other animal taxa (butterflies, newts, frogs, beetles and fruit flies) has been shown to be light-dependent [17,[23][24][25][26][27][28][29][30]. The results of various behavioural studies indicate that both the spectrum wavelength and light intensity play crucial roles in the ability of migratory birds to orient using information from the Earth's magnetic field. ...
Currently, it is generally assumed that migratory birds are oriented in the appropriate migratory direction under UV, blue and green light (short-wavelength) and are unable to use their magnetic compass in total darkness and under yellow and red light (long-wavelength). However, it has also been suggested that the magnetic compass has two sensitivity peaks: in the short and long wavelengths, but with different intensities. In this project, we aimed to study the orientation of long-distance migrants, pied flycatchers (Ficedula hypoleuca), under different narrowband light conditions during autumn and spring migrations. The birds were tested in the natural magnetic field (NMF) and a changed magnetic field (CMF) rotated counterclockwise by 120° under dim green (autumn) and yellow (spring and autumn) light, which are on the ‘threshold’ between the short-wavelength and long-wavelength light. We showed that pied flycatchers (i) were completely disoriented under green light both in the NMF and CMF but (ii) showed the migratory direction in the NMF and the appropriate response to CMF under yellow light. Our data contradict the results of previous experiments under narrowband green and yellow light and raise doubts about the existence of only short-wavelength magnetoreception. The parameters of natural light change dramatically in spectral composition and intensity after local sunset, and the avian magnetic compass should be adapted to function properly under such constantly changing light conditions.
... Shakhparonov et al. (2017) studied adults of Pelophylax ridibundus and obtained similar results in comparison with the afore mentioned investigations. Diego- Rasilla et al. (2010) and Freake et al. (2002) proposed that the existing mechanisms of anurans and urodeles are traces of the evolution of sensory capacity in amphibians. Consequently, the sensitivity function of magnetoreception could have been present in a common ancestor of Lissamphibia, originating in the Lower Permian Period (Zhang & Wake, 2009). ...
El campo magnético de la Tierra (EMF) es una de las fuentes de información direccional más uniformes y accesibles que los animales pueden usar en los movimientos de comportamiento. El presente estudio tuvo como objetivo determinar la capacidad de Rhinella arenarum para percibir los campos electromagnéticos. Para evaluar la influencia de los campos electromagnéticos en los anuros in situ, recolectamos cuarenta y cuatro especímenes adultos de R. arenarum durante la temporada de reproducción. Registramos el movimiento de cada sapo desde el centro hasta la periferia de un arenero circular utilizando una cámara de visión nocturna. Repetimos el experimento después de cinco minutos, con un campo magnético inducido adicional (IMF), que fue creado empleando dos bobinas de aire Helmholtz. Los movimientos de los sapos bajo la presencia de EMF y IMF fueron significativamente diferentes. Concluimos que R. arenarum podría usar el EMF como mecanismo de navegación y sistema de ubicación, para viajar largas distancias hasta los estanques de desove año tras año.
... Later work, which focused on the magnetic sense, showed that larval anurans and newts can be trained to a magnetic field direction using a y-axis assay (Freake et al., 2002;Rodríguez-García and Diego-Rasilla, 2006;Diego-Rasilla and Phillips, 2007). Such response is based on a light-dependent magnetic compass, which might indicate a so-called radical pair based mechanism (Freake and Phillips, 2005;Diego-Rasilla, Luengo, and Phillips, 2010. ...
Most amphibians have a complex life cycle with an aquatic larval and an adult (semi-) terrestrial stage. However, studies concerning spatial behaviour and orientation mainly focus on either the aquatic larvae or the adult animals on land. Consequently, behavioural changes that happen during metamorphosis and the consequences for emigration and population distribution are less understood. This paper aims to summarize the knowledge concerning specific topics of early amphibian life history stages and proposes several testable hypotheses within the following fields of research: larval and juvenile orientation, influences of environmental and genetic factors on juvenile emigration, their habitat choice later in life as well as population biology. I argue that studying larval and juvenile amphibian spatial behaviour is an understudied field of research, however, could considerably improve our understanding of amphibian ecology.
... A pesar de eso, se sabe que la iluminación artificial puede influir en el comportamiento de las ranas nocturnas (Buchanan, 1993). Un efecto negativo bien documentado de la perturbación lumínica es el que ocurre en el caso de las tortugas marinas (Salmon, 2006), cuando la brújula magnética presente en estos organismos se ve afectada por longitudes de onda de luz superiores a 500 nm (Diego-Rasilla et al., 2010), un rango espectral que cae dentro de las lámparas de vapor de sodio colocadas a menudo a lo largo de las carreteras (Rydell, 1992). Por lo tanto, dicha iluminación artificial puede desalentar a las hembras en la selección del sitio de anidación (Salmon et al., 2000) o interferir en la habilidad de las crías para orientarse y causarles la muerte (Witherington y Martin, 2000;Tuxbury y Salmon, 2005;Karmrowski et al., 2012), ya que en lugar de dirigirse al mar lo hacen hacia las carreteras y asentamientos humanos. ...
The current chapter contains a global literature review of roads and railroads’ impact on fauna to establish a theoretical framework applicable to protected natural areas. To do this, it categorizes the negative impacts into four central classes: a) the direct and indirect elimination of the habitat, b) the barrier effect caused by the restriction of movement and the mortality of individuals due to collisions with vehicles and trains, c)
the deterioration of the habitat quality due to micro-environmental changes, pollution, noise and artificial light, and d) the attraction effect, caused by the creation of artificial habitats and corridors.
... Groddjurens magnetiska kompass är ljuskänslig på samma sätt som för fåglar, och kan störas av ljus med långa våglängder (gult och rött)( Diego-Rasilla et al. 2010). ...
Lysdiod-belysning (Light Emitting Diode; LED) används i allt större omfattning utomhus på vägar och gator och utgör idag ofta enda valbara alternativet. Det finns många fördelar med att använda LED-belysning men det har alltmer börjat uppmärksammas att artificiellt ljus även har många ekologiska nackdelar eftersom det sker en påverkan på djur och natur. Biologiska effekter av artificiella ljuskällor är sedan tidigare väl studerat och det är därför exempelvis känt att det finns effekter på många olika typer av arter.
Detta projekt har fokuserat på att sammanfatta vilka specifika ekologiska effekter som LED-belysningen kan orsaka samt hur dessa kan åtgärdas. Syftet med rapporten har varit att: kartlägga påverkan av LED-belysning på djur och natur, identifiera särskilt känsliga djur eller organismer men också att utreda under vilka förhållanden eller förutsättningar (områden, tid på dygnet/året) som en ekologisk påverkan kan förväntas ske, samt slutligen att ge konkreta rekommendationer för att minimera påverkan på djur och natur. Rekommendationerna är särskilt anpassade till att vara tillämpbara i de nordiska länderna.
En systematisk litteratursökning genomfördes under 2017 för att hitta relevant litteratur om effekter av LED-belysning på djur och natur. Sökningen var en bra utgångspunkt men räckte inte för att identifiera alla typer av relevanta underlag som krävdes för att utföra projektet och därför har litteratursökningar utförts kontinuerligt under projektets gång, utifrån vilken typ av information som behövdes när kapitlen författades.
I rapporten redovisas kunskap om LED som ljuskälla och dess egenskaper jämförs exempelvis med andra ljuskällor. Arbetet inkluderar att ljus uppfattas olika och påverkar olika beroende av art och har sammanställts uppdelat i olika djurgrupper för att få en översikt över hur djur påverkas av artificiellt ljus. Effekter av LED-belysning på arters fysiologi, beteende och ekologi har utgått från hittills utförda studier inom området och visar på varierande resultat beroende på vilka arter som studerats. Samtidigt saknas studier för väldigt många arter; ibland saknas kunskap om påverkan på hela grupper av djur såsom exempelvis större däggdjur, groddjur och många fågelarter. En viktig slutsats är att det inte går att utesluta att förekomsten av himlaglim kan ha ekologiska konsekvenser över stora geografiska områden.
Prioriteringar för naturvårdande åtgärder har behandlats utifrån ett nationellt/nordiskt perspektiv men även ur perspektivet att det finns både områden och ljuskänsliga arter som behöver extra skydd från artificiellt ljus. I rapporten har även redovisats hur man kan göra anpassningar till olika miljöer och ekosystem, samt hur man skulle kunna arbeta med zoner och på landskapsnivå med dessa frågor i det vidare arbetet. För stadsmiljöer och urbana miljöer är det relevant att reducera himlaglim och att säkerställa att områden med skyddade arter inte blir belysta. Vattenära miljöer bör speciellt beaktas på grund av förekomsten av många skyddade och ljuskänsliga arter, exempelvis bör säkerställas att inte ljuskällorna sprider ljus i vattnet eller åstadkommer polarisering.
Rekommendationerna för hur man ska minimera ekologisk påverkan är uppdelad i fem (redan etablerade) områden: förhindra och begränsa nya områden från att belysas, begränsa omfattningen av belysta områden, begränsa tiden med belysning, begränsa belysningsstyrkan/ljuskvantiteten samt anpassningar i ljusets våglängdsfördelning.
Slutsatserna sammanfattar de rekommendationer som särskilt bör prioriteras förutsatt att man ämnar ha belysning utomhus. LED-belysning har många fördelar och erbjuder bra möjligheter att reducera ekologisk påverkan. Störst potential att reducera ekologisk påverkan både direkt och indirekt genom himlaglim och via påverkan av vitt ljus på seendet samt icke-visuellt ljus (främst blått ljus < 500 nm) är att reducera spilljus och ljusföroreningar från belysningen genom att begränsa ljusets rumsliga spridning från ljuskällor.
Exempelvis rekommenderas att alla typer av uppljus bör elimineras utan undantag för att reducera mortaliteten av migrerande och skyddade arter. Bakljus, framljus och luminans bör genom god ljusdesign starkt begränsas i den fysiska miljön för att reducera ljusföroreningar i omgivningen. Begränsningar i ljusets spridning kommer att reducera risken att aktivera dagsljusseendet hos arter som har både fotopisk och skotopisk syn samtidigt som påverkan på nattaktiva arter kommer att reduceras eftersom arealen som är belyst kommer att minskas.
För extra ljuskänsliga och skyddade arter som potentiellt kan vara påverkade negativt av himlaglim är det oklart ifall några av de föreslagna åtgärderna räcker. Därför är det rimligt att ansvaret för att säkerställa mörkerområden för dessa arters fortlevnad bör ligga hos de som förvaltar artskydd (till exempel kommuner och länsstyrelser som beslutar om och förvaltar naturreservat). Det är i beslutsprocessen och i förvaltningen som önskvärda begränsningar i ljusföroreningarna kan beskrivas och implementeras.
För att stärka skyddet av arter som förflyttar sig bör rekommendationerna som tagits fram implementeras i någon form på en övergripande nationell nivå. Skyddade miljöer såsom Natura 2000-områden kan/bör använda sig av de i rapporten föreslagna striktare riktlinjerna (som tagits fram av IDA, International Dark Association) för att säkerställa en minimal ljuspåverkan på skyddade arter.
Mängden blått ljus i utomhusbelysningen bör förmodligen reduceras eftersom det är väl känt att sådant ljus kan påverka många arters dygnsrytm. Det kommer inte inom en rimlig framtidshorisont gå att få fram tillräckligt med kunskap om de exakta nivåerna för exponering till blått ljus och dess konsekvenserna för alla olika typer av arter som kan påverkas och därför bör försiktighetsprincipen tillämpas. Alla kommersiellt tillgängliga ljuskällor på marknaden bör redovisa mängden förekommande blått ljus (speciellt avseende < 500 nm) för att underlätta val av produkter med låga mängder blått ljus.
Nattsläckning och nattreduktion bör tillämpas så långt det är möjligt för att undvika ekologisk påverkan på största möjliga antalet arter och för att reducera attraktionen hos migrerande arter.
En utmaning med att ta fram rekommendationerna avseende ekologisk påverkan av utomhusbelysning är att det finns brister i de vetenskapliga studier som utförts. Exempelvis redovisas inte tillräckligt mycket information för att upprepa experimenten och det kan saknas grundläggande information om ljuskällor eller experimentdesign som gör att resultaten inte är användbara.
Ljusföroreningar bör beaktas i högre grad i arbetet med ljusplanering men även i arbetet med naturmiljöfrågor och på landskapsnivå för att säkerställa att inte skyddade arter påverkas. Planeringen av infrastruktur med tillhörande utomhusbelysning måste därför integreras i arbetet med övriga miljöfrågor i kommuner och på regional och nationell nivå.
... Magnetoreception can be involved in many aspects of spatial behaviour: as a compass for local and long-distance movements (Wiltschko and Wiltschko, 1972;Landler et al., 2015;Phillips et al., 2013;Diego-Rasilla et al., 2010;Dommer et al., 2008;Freake et al., 2002) as a source of geographic position information (i.e., a magnetic map Phillips, 1986;Philips et al., 1995;Deutschlander et al., 2012) as a reference that reduces errors in path integration (Kimchi et al., 2004;Philips et al., 2010) and potentially as a spherical coordinate system that helps to encode the organism's immediate surrounding and to incorporate local landmark arrays into a global map of familiar space (Landler et al., 2015;Phillips et al., 2010). Consequently, loss of a magnetic sense could impact both long-distance movements (e.g. ...
The Earth's magnetic field is involved in spatial behaviours ranging from long-distance migration to non-goal directed behaviours, such as spontaneous magnetic alignment (SMA). Mercury is a harmful pollutant most often generated from anthropogenic sources that can bio-accumulate in animal tissue over a lifetime. We compared SMA of hatchling snapping turtles from mothers captured at reference (i.e., low mercury) and mercury contaminated sites. Reference turtles showed radio frequency-dependent SMA along the north-south axis, consistent with previous studies of SMA, while turtles with high levels of maternally inherited mercury failed to show consistent magnetic alignment. In contrast, there was no difference between reference and mercury exposed turtles on standard performance measures. The magnetic field plays an important role in animal orientation behaviour and may also help to integrate spatial information from a variety of sensory modalities. As a consequence, mercury may compromise the performance of turtles in a wide variety of spatial tasks. Future research is needed to determine the threshold for mercury effects on snapping turtles, whether mercury exposure compromises spatial behaviour of adult turtles, and whether mercury has a direct effect on the magnetoreception mechanism(s) that mediate SMA or a more general effect on the nervous system.
... Behavioural evidence from various animals suggests that access to light of specific characteristics (wavelength and intensity) is necessary for magnetic compass reception (reviewed by Wiltschko et al., 2010;Phillips et al., 2010b). Insects and amphibians trained and tested under wavelengths of light shorter than 450 nm displayed oriented behaviour towards a trained magnetic compass direction, but shifted their orientation by ∼90 deg when tested under longer wavelengths (Phillips and Borland, 1992a,b;Phillips and Sayeed, 1993;Vacha, 2004;Dommer et al., 2008;Diego-Rasilla et al., 2010. Young, inexperienced homing pigeons (Columba livia) were unable to orient towards home when transported to the release site in complete darkness or under red light (650 nm), but were well oriented when transported under green (565 nm) or full-spectrum light Wiltschko, 1981, 1998). ...
Birds have a light-dependent magnetic compass that provides information about the spatial alignment of the geomagnetic field. It is proposed to be located in the avian retina and mediated by a lightinduced, radical-pair mechanism involving cryptochromes as sensory receptor molecules. To investigate how the behavioural responses of birds under different light spectra match with cryptochromes as the primary magnetoreceptor, we examined the spectral properties of the magnetic compass in zebra finches. We trained birds to relocate a food reward in a spatial orientation task using magnetic compass cues. The birds were well oriented along the trained magnetic compass axis when trained and tested under low-irradiance 521 nm green light. In the presence of a 1.4 MHz radio-frequency electromagnetic (RF)-field, the birds were disoriented, which supports the involvement of radical-pair reactions in the primary magnetoreception process. Birds trained and tested under 638 nm red light showed a weak tendency to orient ~45 deg clockwise of the trained magnetic direction. Under low-irradiance 460 nm blue light, they tended to orient along the trained magnetic compass axis, but were disoriented under higher irradiance light. Zebra finches trained and tested under high-irradiance 430 nm indigo light were well oriented along the trained magnetic compass axis, but disoriented in the presence of a RF-field. We conclude that magnetic compass responses of zebra finches are similar to those observed in nocturnally migrating birds and agree with cryptochromes as the primary magnetoreceptor, suggesting that light-dependent, radicalpair- mediated magnetoreception is a common property for all birds, including non-migratory species.
... magnetotactic bacteria [19], protists [20], gastropods [21], crustaceans [22], insects [23], bony fish [24], amphibians [25], sea turtles [26], birds [27], and migratory whales [28]. ...
The purpose of this document is to provide the general guidelines for the design of ground return electrode stations for HVDC transmission systems. The document is organised in eight chapters: Ch 1 describes HVDC configurations that have electrodes as the ground return path.
Ch 2 describes various types of electrodes. HVDC electrodes can be of three fundamental types or categories, i.e. land, shore (pond or beach) and sea. This chapter introduces the different types of electrodes and typical configurations, their advantages and drawbacks, and summarizes high level considerations for the selection of type of electrode and configuration.
Ch 3 focuses on the electrode site selection process. The current site selection practice includes geophysical, geological, social and environmental condition investigations. Physical constructability aspects and general requirements relevant to site selection.
Ch 4 describes the potential impact of electrodes on infrastructure and the environment as well as mitigation of adverse effects caused by operation of the electrodes.
Ch 5 covers electrode design aspects. Electrode design includes the following aspects which are described in the body of chapter: design criteria, interference, operating duties, electrode life cycle, reliability, temperature rise, and chemical emissions. The design criteria include safety requirement for humans and animals and discriminate between steady state and short-time operating conditions.
Ch 6 addresses the neutral line (or electrode line) between the converter stations and the electrode stations. Neutral lines can be built as overhead lines or using insulated cables for undersea or underground lines. Both electrode line technologies are described.
Ch 7 describes auxiliary systems for electrode stations including the station service supply and monitoring of electrode stations.
Ch 8 covers the testing and commissioning of electrodes.
... Reptilian parietal eye can discriminate between different wavelengths of light through chromatic antagonism; i.e., opposing responses consisting of short-wavelength-sensitive hyperpolarisation and greensensitive depolarisation (Solessio and Engbretson 1993;Wada et al. 2012). Antagonistic spectral mechanism in photoreceptors of the parietal eye of lizards exhibits spectral features similar to those found in the pineal complex of amphibians (Dodt and Heerd 1962;Eldred and Nolte 1978;Korf et al. 1981) and is consistent with the properties of the lightdependent magnetic compass found in newts and frogs (Diego-Rasilla et al. 2010Phillips et al. 2010a). In fact, short-wavelength and long-wavelength inputs to the magnetic compass of amphibians are mediated by extraocular photoreceptors located in the pineal complex (Deutschlander et al. 1999a, b;Phillips et al. 2001). ...
Several species of vertebrates exhibit spontaneous longitudinal body axis alignment relative to the Earth’s magnetic field (i.e., magnetic alignment) while they are performing different behavioural tasks. Since magnetoreception is still not fully understood, studying magnetic alignment provides evidence for magnetoreception and broadens current knowledge of magnetic sense in animals. Furthermore, magnetic alignment widens the roles of magnetic sensitivity in animals and may contribute to shed new light on magnetoreception. In this context, spontaneous alignment in two species of lacertid lizards (Podarcis muralis and Podarcis lilfordi) during basking periods was monitored. Alignments in 255 P. muralis and 456 P. lilfordi were measured over a 5-year period. The possible influence of the sun’s position (i.e., altitude and azimuth) and geomagnetic field values corresponding to the moment in which a particular lizard was observed on lizards’ body axis orientation was evaluated. Both species exhibited a highly significant bimodal orientation along the north-northeast and south-southwest magnetic axis. The evidence from this study suggests that free-living lacertid lizards exhibit magnetic alignment behaviour, since their body alignments cannot be explained by an effect of the sun’s position. On the contrary, lizard orientations were significantly correlated with geomagnetic field values at the time of each observation. We suggest that this behaviour might provide lizards with a constant directional reference while they are sun basking. This directional reference might improve their mental map of space to accomplish efficient escape behaviour. This study is the first to provide spontaneous magnetic alignment behaviour in free-living reptiles.
... For example, short-distance palmate newts rely on acoustic cues for orientation to breeding ponds, while for long-distance homing, they use magnetic compass as the sole source of directionality. Tadpoles of European common frog and Iberian green frog use wavelengthdependent effect of light on magnetic compass along the shore-deep water axis [65][66][67]. True navigation has been shown in only one species, the aquatic salamander Notophthalmus viridescens. ...
How migrating animals find their direction to reach migratory destination is an important question of wildlife migration. Animals use a variety of geophysical cues such as the sun compass, stellar constellation, and geomagnetic field of the Earth to accomplish this feat. Endogenous clocks facilitate, to some extent, the challenge of heading toward the right direction. Whereas extensive body of research has focused on the biophysical and neurobiological mechanisms, relatively less is known of the extent of involvement of biological clocks in the migratory orientation. Studies on the innate capability of first year migrants and experimentally displaced experienced migrants to correctly reach their destination indicate that an endogenous time program controls spontaneous changes during the course of migratory journey. Here, we intend to briefly summarize the orientation studies in animals, with emphasis placed on the role of biological clocks in the avian orientation.
... Currently the existence of the magnetic compass systems in birds is not questioned by serious researchers. There are also reports on using magnetic compass by mammals (Burda et al., 1990;Deutschlander et al., 2003;Holland et al., 2006), sea turtles (Lohmann, K.J., 1991; Lohmann, K.J. and Lohmann, C.M.F., 1993), amphibians (Deutschlander et al., 1999;Diego-Rasilla et al., 2010 and bony fishes (Quinn et al., 1981). The sensory mechanism of the magnetic compass of animals remained unknown for a long time after its discovery, but significant progress has been achieved in this field in the last 15-20 years (Wiltschko, R. and Wiltschko, W., 2015). ...
The question of how migrating birds find their way to winter quarters and back has fascinated humans since the beginning of scientific research into avian biology. Migrating birds have been shown to possess compass systems that allow them to select and maintain certain compass directions. Three such systems are known, solar, stellar and magnetic. Their details are not quite clear and need further research. Hierarchy and interaction of compass systems of migrating birds are poorly studied; different species may vary in this respect. During migration, birds learn to use maps that make true navigation possible, i.e. to detect their position relatively to the goal of movement. The physical nature of navigational maps is an object of intensive research; currently the most promising concepts are the geomagnetic and possibly olfactory maps. A significant contribution to the study of formation of navigational maps was made by Soviet/Russian researchers, whose work was published in Zoologicheskii Zhurnal (Sokolov et al., 1984). Migrating birds have no innate map, and first-autumn individuals reach their species-specific wintering areas by using compass sense and counting time that should be spent moving in certain genetically fixed directions. However, in recent years more and more data surface that suggest that juveniles (maybe not of all species) do have some mechanism of controlling their position on the migratory route that allows them to compensate for errors of the spatio-temporal programme of migration.
... В настоящее время существование магнитной компасной системы у птиц не подвергается сомнению. Есть сообщения об использовании магнитного компаса млекопитающими (Burda et al., 1990;Deutschlander et al., 2003;Holland et al., 2006), морскими черепахами (Lohmann K.J., 1991;Lohmann K.J., Lohmann C.M.F., 1993), земноводными (Deutschlander et al., 1999;Diego-Rasilla et al., 2010 и костистыми рыбами (Quinn et al., 1981). Долгое время после открытия магнитного компаса животных его сенсорный механизм оставался неизвестным, однако в последние 15-20 лет в этой области достигнут существенный прогресс (Wiltschko R., Wiltschko W., 2015). ...
... Salmon [25] Invertebrates Honeybee [26] Beetle [27][28][29] Crustacean [30] Mullusk [31,32] Frogs [33][34][35] Salamander [36] Drosophila [37,38] C. Elegans [39] Butterfly [40] Birds [41] European robin [7] Australian Silvereye [42][43][44][45][46] Garden warbler [47][48][49][50] Homing pigeon [9] Pied flycatcher [51] Mammals [52] Mole rat [53] Bat [54,55] Cattle [56,57] Red foxe [58] Dog [10] Dolphin [59] And even experiments with humans have been performed, which however gave inconclusive results [60][61][62][63][64][65][66] . ...
... Similar 90° shifts in orientation under longer wavelengths have also been described in newts and frog and toad tadpoles (Phillips and Borland 1992b ;Freake and Phillips 2005 ;Diego-Rasilla et al. 2010 ; reviewed by Phillips et al. 2001Phillips et al. , 2010a. The shoreward orientation of North American Eastern red-spotted newts trained to learn the magnetic alignment of an artifi cial shore is mediated by a magnetic inclination compass that depends on the wavelength of the ambient light. ...
The magnetic compass of many animals, including insects, amphibians, and birds, needs light of a specific wavelength range to function. Behavioral and physiological evidence suggests the involvement of specialized magnetosensitive photoreceptors that enable the animals to perceive the Earth’s magnetic field as a three-dimensional pattern, providing them with information on the axis and inclination of the magnetic field. Cryptochromes have been suggested as the primary receptor molecules, as they are the only known animal photopigment that can produce spin-correlated radical pairs that last long enough for a magnetic field effect to take place. In this chapter, we summarize the state of the art of the research field and discuss the behavioral, physiological, and biophysical evidence for light-dependent magnetic compass orientation in different animals.
... Some amphibians have been shown to possess a light-dependent sensitivity towards a magnetic field that helps them to orient (Phillips and Borland, 1994;Phillips et al., 2001;Diego-Rasilla et al., 2010) and also migrating turtles make use of the earth's magnetic field, although most likely in a light-independent manner (reviewed in Wiltschko and Wiltschko, 2012). The proposed molecule involved in the radical pair mechanism -one of the hypothesized mechanisms how the earth's magnetic field could be detected (Ritz et al., 2000;Rodgers and Hore, 2009) -is Cryptochrome (reviewed in Liedvogel and Mouritsen, 2010). ...
Cryptochromes (Crys) are light sensing receptors that are present in all eukaryotes. They mainly absorb light in the UV/blue spectrum. The extant Cryptochromes consist of two subfamilies, which are descendants of photolyases but are now involved in the regulation of circadian rhythms. So far, knowledge about the evolution, phylogeny and expression of cry genes is still scarce. The inclusion of cry sequences from a wide range of bilaterian species allowed us to analyze their phylogeny in detail, identifying six major Cryptochrome subgroups. Selective gene inactivations and stabilizations in multiple chordate as well as arthropod lineages, suggest several sub- and/or neofunctionalization events. An expression study performed in zebrafish, the model organism harboring the largest amount of crys, showed indeed only partially overlapping expression of paralogous mRNA, supporting gene sub- and/or neofunctionalization. Moreover, the daily cry expression in the adult zebrafish retina indicated varying oscillation patterns in different cell types. Our extensive phylogenetic analysis provides for the first time an overview of cry evolutionary history. While several, especially parasitic or blind species, have lost all cry genes, crustaceans have retained up to three crys, teleosts possess up to seven, and tetrapods up to four crys. The broad and cyclic expression pattern of all cry transcripts in zebrafish retinal layers implies an involvement in retinal circadian processes and supports the hypothesis of several autonomous circadian clocks present in the vertebrate retina.
© The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
... The Earth's geomagnetic field potentially provides a reliable global positioning system for any organism that can detect and interpret the magnetic landscape in terms of relative position and/or directional orientation. Indeed, over the past 50 years a considerable amount of evidence has been amassed showing that an astounding variety of organisms respond to geomagnetic cues: magnetotactic bacteria (Blakemore 1975;Kirschvink 1980), protists (Bazylinski et al. 2000), gastropods (Lohmann and Willows 1987), crustaceans (Lohmann 1985;Lohmann et al. 1995b;Arendse 1978;Ugolini and Pezzani 1992), insects (Jacklyn 1992;DeJong 1982;Schmidt and Esch 1993;Gegeer et al. 2008;Riveros and Srygley 2010), bony fish (Quinn and Groot 1983;Taylor 1986;Chew and Brown 1987;Walker 1984), amphibians (Phillips 1986;Diego-Rasilla et al. 2010), sea turtles (Lohmann 1991;Light et al. 1993;Lohmann and Lohmann 1994a, 1994b, 1996bGoff et al. 1995), birds (Wiltschko and Merkel 1966;Wiltschlko et al. 2010;Wilzeck et al. 2010), and migratory whales (Klinowska 1985;Kirschvink et al. 1986;Walker et al. 1992). In addition, there are many more citations than just those listed above. ...
An environmental impact assessment (EIA) of electromagnetic (EM) survey techniques used for oil and gas exploration in the marine environment was completed and published in November 2011. The EIA was funded by the member companies of the International Association of Geophysical Contractors (IAGC) EM Subcommittee and prepared by an independent environmental consulting company.
EM survey technologies currently utilized offshore use either the Earth's natural electromagnetic field or an induced low-frequency electromagnetic field transmitted by an antenna towed behind a vessel. The electric and magnetic fields are measured and recorded by an array of receivers. To date, these receivers have usually been deployed on the seafloor and then retrieved to process the measurements. Tests are currently being conducted to commercialize a system that tows the receivers underwater behind the vessel, similar to the method used in most marine seismic surveys. The data from EM surveys can help identify differences in the resistivity of subsurface rocks that may be related to the presence of hydrocarbons.
The goal of the EIA was to provide a comprehensive resource summarizing available literature and potential effects of EM technologies on marine life. Designed for a broad audience, the document provides a basic description of EM survey technologies, naturally-occurring EM fields, and the potential use of these fields by diverse animal groups. The assessment focuses on survey activities considered to have at least some potential to affect marine animals, such as EM, noise, light emissions, and accidental events.
The EIA concluded that EM sources as presently used have no potential for significant effects on animal groups such as fish, seabirds, sea turtles, and marine mammals. In addition, cumulative effects from EM surveys are negligible compared to natural EM anomalies, induced fields from natural water currents, and other anthropogenic EM sources such as those originating from permanently installed undersea equipment.
... Another interesting type of innervation of the frog skin concerns the frontal nerve, which interconnects the frontal organ with the epiphysis (pineal gland) and the brain. The frontal organ is an outgrowth of the pineal gland, and has been reported to be sensitive to magnetic fields (Diego-Rasilla, Luengo & Phillips, 2010). In Rana esculenta the frontal nerve forms, either on its left or its right side, a unilateral branch that runs into the dermis. ...
For over a century, frogs have been studied across various scientific fields, including physiology, embryology, neuroscience, (neuro)endocrinology, ecology, genetics, behavioural science, evolution, drug development, and conservation biology. In some cases, frog skin has proven very successful as a research model, for example aiding in the study of ion transport through tight epithelia, where it has served as a model for the vertebrate distal renal tubule and mammalian epithelia. However, it has rarely been considered in comparative studies involving human skin. Yet, despite certain notable adaptations that have enabled frogs to survive in both aquatic and terrestrial environments, frog skin has many features in common with human skin. Here we present a comprehensive overview of frog (and toad) skin ontogeny, anatomy, cytology, neuroendocrinology and immunology, with special attention to its unique adaptations as well as to its similarities with the mammalian integument, including human skin. We hope to provide a valuable reference point and a source of inspiration for both amphibian investigators and mammalian researchers studying the structural and functional properties of the largest organ of the vertebrate body.
... If the magnetic compass of epigeic rodents is mediated by a radical pair mechanism, as appears to be the case in amphibians and birds [21,25,34,38,39,70,71], magnetic cues could play a variety of previously unforeseen roles in rodent spatial behavior and cognition. When photo-magnetoreceptors mediating a radical pair-based magnetic compass are located in the retina, as may be the case in birds and epigeic rodents [15,72–75], the magnetic field may be perceived as a complex, 3-dimensional pattern of light intensity or color superimposed on the animal’s surroundings and fixed in alignment with respect to the magnetic field [34,36,41]. ...
Magnetoreception has been demonstrated in all five vertebrate classes. In rodents, nest building experiments have shown the use of magnetic cues by two families of molerats, Siberian hamsters and C57BL/6 mice. However, assays widely used to study rodent spatial cognition (e.g. water maze, radial arm maze) have failed to provide evidence for the use of magnetic cues. Here we show that C57BL/6 mice can learn the magnetic direction of a submerged platform in a 4-armed (plus) water maze. Naïve mice were given two brief training trials. In each trial, a mouse was confined to one arm of the maze with the submerged platform at the outer end in a predetermined alignment relative to magnetic north. Between trials, the training arm and magnetic field were rotated by 180(°) so that the mouse had to swim in the same magnetic direction to reach the submerged platform. The directional preference of each mouse was tested once in one of four magnetic field alignments by releasing it at the center of the maze with access to all four arms. Equal numbers of responses were obtained from mice tested in the four symmetrical magnetic field alignments. Findings show that two training trials are sufficient for mice to learn the magnetic direction of the submerged platform in a plus water maze. The success of these experiments may be explained by: (1) absence of alternative directional cues (2), rotation of magnetic field alignment, and (3) electromagnetic shielding to minimize radio frequency interference that has been shown to interfere with magnetic compass orientation of birds. These findings confirm that mice have a well-developed magnetic compass, and give further impetus to the question of whether epigeic rodents (e.g., mice and rats) have a photoreceptor-based magnetic compass similar to that found in amphibians and migratory birds.
... Trials with these animals were conducted in January 2010 between 11:30 a.m. and 12:50 p.m. Individual snails were collected near the shore of the lake, down to a water depth of approximately 50 cm. An arena approach, similar to those used in other orientation studies (Freake et al. 2002; Diego-Rasilla et al. 2010; Walsh et al. 2010), was used to test directional responses (Figure 2 ). The arenas ( = 8 cm) were symmetrical polygons with 16 edges painted on a wooden plate and covered by a transparent plastic sheet. ...
Y -axis orientation, a movement perpendicular to the shore or coastline, enables aquatic animals to stay in a preferred zone in generally unstable habitats. Such behaviour is a widespread phenomenon in many freshwater and intertidal animal taxa. In the present study, an arena approach was used to test the orientation response of pulmonate freshwater snails. Using this experimental design, Y -axis orientation was shown for the first time in a freshwater snail species, the riverine Chilina patagonica. Some cues, potentially mediating Y -axis orientation, appeared to play no role in the shown orientation behaviour, such as chemical, gravity and humidity cues or a sun compass. Magnetic cues, however, could not be excluded. Since no significant differences in orientation were detected between different size classes in C. patagonica, orientation behaviour may not vary substantially throughout the snail’s life history. In contrast to C. patagonica, no consistent orientation response was seen in the related lacustrine species Chilina llanquihuensis. The adaptation of C. patagonica to exhibit orientation along the Y -axis may be driven by the avoidance of high velocities in deeper water.
... When trained under the same short-wavelength light and tested under blue-green light (500nm), beetles shifted their orientation 90deg clockwise relative to the trained magnetic direction (Vácha et al., 2008). While the wavelength-dependent effects of light on magnetic compass orientation in flies and beetles could result from a change in the behavioral response rather than a change in the directional input used to guide behavior, similar wavelength-dependent 90deg shifts in magnetic compass orientation in both anuran and urodele amphibians have been shown to result from a direct effect of light on the underlying magnetoreception mechanism (Phillips and Borland, 1992;Freake and Phillips, 2005;Diego-Rasilla et al., 2010). Furthermore, preliminary evidence for photoreceptors sensitive to the alignment of an earth-strength magnetic field has been obtained in neurophysiological recordings from the frontal organ (an The Journal of Experimental Biology 216 (7) Topographic Magnetic 4ϫ ...
We provide evidence for spontaneous quadramodal magnetic orientation in a larval insect. Second instar Berlin, Canton-S, and Oregon-R X Canton-S strains of Drosophila melanogaster exhibited quadramodal orientation with clusters of bearings along the four anti-cardinal compass directions (i.e. 45°, 135°, 225°, 315°). In double-blind experiments, Canton-S Drosophila larvae exhibited quadramodal orientation in the presence of an earth-strength magnetic field, while this response was abolished when the horizontal component of the magnetic field was cancelled, indicating that the quadramodal behavior is dependent on magnetic cues, and may reflect properties of the underlying magnetoreception mechanism. In addition, a reanalysis of data from studies of learned magnetic compass orientation by adult Drosophila melanogaster and C57BL/6 mice reveals patterns of response similar to those exhibited by larval flies suggesting that a common magnetoreception mechanism(s) may underlie these behaviors. Therefore, characterizing the mechanism(s) of magnetoreception in flies may hold the key to understanding the magnetic sense in a wide array of terrestrial organisms.
... Aktuellere Studien zeigten bei Larven des Ochsenfrosches (Lithobates catesbeianus) und des Iberischen Grünfrosches (Pelophylax perezi) eine lichtabhängige magnetische Orientierung , Freake & PhiLLiPs 2005, dieGo-rasiLLa & PhiLLiPs 2007, dieGo-rasiLLa et al. 2010. Die Tiere wurden entlang einer Y-Achse trainiert (die Achse normal auf die Uferlinie) und in Arenen, in denen das Magnetfeld mittels Spulen gedreht wurde, getestet. ...
The geomagnetic field provides various cues for spatial orientation in animals. To date, magnetic orientation has been proven in more than 40 species. This paper presents an overview of the current knowledge in this field, focusing on amphibians. In several animals a light-dependence of compass orientation was observed in behavioural experiments. To explain these results the theory of a radical pair reaction as the basis of magnetoreception was formulated. Moreover, another, light-independent but magnetite-based magnetic sense has been proposed for position finding on an internal magnetic map. In amphibians most studies were performed on urodeles, only few on anuran larvae. In arena-experiments, conducted during the spawning migration, we demonstrated orientation towards the spawning pond after displacement in the European Common Toad. This experimental set-up provides good opportunities to test magnetic orientation of the Common Toad.
... Tadpoles of the Bullfrog (Lithobates catesbeianus) and the Iberian Green Frog (Pelophylax perezi) could be trained to swim along a Y-axis, using the magnetic field as a cue [14,15]. In both species magnetic orientation by tadpoles is also light-dependent [16,17]. Adults of our target species, the European Common Toad (Bufo bufo), are able to locate their home pond even if it is filled up with soil [18]. ...
Magnetic orientation is a taxonomically widespread phenomenon in the animal kingdom, but has been little studied in anuran amphibians. We collected Common Toads (Bufo bufo) during their migration towards their spawning pond and tested them shortly after displacement for possible magnetic orientation in arena experiments. Animals were tested in two different set-ups, in the geomagnetic field and in a reversed magnetic field. To the best of our knowledge, this is the first study testing orientation of adult anurans with a controlled magnetic field of a known strength and alignment.
After displacement, toads oriented themselves unimodally under the geomagnetic field, following their former migration direction (d-axis). When the magnetic field was reversed, the distribution of bearings changed from a unimodal to a bimodal pattern, but still along the d-axis. The clustering of bearings was only significant after the toads reached the outer circle, 60.5 cm from their starting point. At a virtual inner circle (diameter 39 cm) and at the start of the experiment, orientation of toads did not show any significant pattern.
The experimental set-up used in our study is suitable to test orientation behaviour of the Common Toad. We speculate that toads had not enough time to relocate their position on an internal map. Hence, they followed their former migration direction. Bimodality in orientation when exposed to the reversed magnetic field could be the result of a cue conflict, between magnetic and possibly celestial cues. For maintaining their migration direction toads use, at least partly, the geomagnetic field as a reference system.
Polarization sensitivity (PS) in amphibians has been examined in some species of anurans and urodelans. Gymnophiones, on account of their tiny eyes and fossorial or aquatic lifestyles are considered unlikely candidates for PS. Some anura and urodela have been shown to detect the direction of polarization with photoreceptors of the pineal organ rather than their lateral eyes. An ordered array of light-absorbing visual molecules is paramount for PS, but an ordered array of radical pairs generated through photo-induced electron transfer is also essential for magnetoreception, which suggests that there is some interaction between the two senses. An anatomical requirement for PS is a constant and characteristic orientation of the photoreceptor’s disc membranes. A closer look at ultrastructural modifications in different retinal regions of species that are expected to be polarization sensitive, seems warranted. Polarization sensitivity may help to relocate breeding sites in philotropic species and to improve visibility of prey in predatory larval and adult urodeles plus those few anurans that hunt underwater. Furthermore, it could possibly be of assistance in separating overlapping shadows and play a role during courtship in species with distinct sexually dimorphic colouration.
One of the most unusual features of the avian magnetic compass is its sensitivity to weak oscillating magnetic fields (OMF) in the radiofrequency range. This effect, observed earlier in numerous experiments in European robins Erithacus rubecula and garden warblers Sylvia borin, is usually associated with the radical-pair magnetoreception in the eye, which is the mainstream biophysical model of the avian magnetic compass. We studied the effect of OMF on the orientation behavior of a long-distance migrant, the pied flycatcher Ficedula hypoleuca. The OMF with an amplitude of 190 nT disoriented pied flycatchers, similarly to the species studied earlier. However, the application of OMP with an amplitude of 17 nT did not lead to disorientation in pied flycatchers when tested in round arenas: the birds showed their correct season-specific migratory direction. This finding is in stark contrast with previous results, obtained in garden warblers at exactly the same place and under the same conditions: garden warblers were disoriented by OMF which was an order of magnitude weaker. Moreover, the threshold of sensitivity to OMF amplitude in pied flycatchers is found to be higher than that in both species previously studied, the European robin and the garden warbler. We discuss the variable sensitivity of avian compass to OMF in the context of migration ecology of two long-distance African migrants, the pied flycatcher and garden warbler, and the short-distance migrant, the European robin.
Significance statement
Birds are known to use a magnetic compass to determine the proper direction of their flight during seasonal migrations. Many previous experiments demonstrated that operation of this compass is disrupted by weak oscillating magnetic fields (OMF) in the radiofrequency range. Among the two bird species studied so far, a long-distance migrant, garden warbler, is more sensitive to OMF than a short-distance migrant, European robin. This might be a result of finer tuning of the magnetic compass of long-distance migrants, making it less robust to perturbations. In our experiments, however, the magnetic compass of another long-distance migrant, pied flycatcher, remained operational under OMF even stronger than that which disrupted magnetic orientation of European robins. This unexpected result demonstrates high variability of navigational systems of birds and raises questions about their adaptation to behavioral patterns of birds on their migration routes.
The evolution, diversity, and limits of vertebrate cognition are a source of fascination for behavioral biologists, but most work has been confined to mammals and birds, limiting our ability to identify fundamental principles of brain-behavior relationships underlying vertebrate cognition. In contrast to amniotes (reptiles, birds, mammals), amphibian brains differ in complexity and in neural connections in fundamental ways, yet how these differences relate to cognition has rarely been explored. For example, the pallium (i.e., cerebrum) of amphibians has less structural heterogeneity, receives less sensory information, and has relatively few descending connections. One might predict these neurobiological features would limit the complexity of sensory associations, behavioral flexibility, and executive control. Indeed, behavioral studies of amphibians show that response learning, likely controlled by the striatum of the subpallium, predominates over allocentric associations during spatial navigation. Further, while landmark learning is widely evident, complex spatial associations appear less common, perhaps due to a constraint on the complexity of sensory representation in the medial pallium (hippocampus). Finally, while amphibians can flexibly modify previously learned responses through habituation, extinction, and reversal of response learning (e.g., turn left vs. turn right), reversals of visual discriminations are more variable among species. Despite these apparent limitations, at least one amphibian, the parental poison frog Dendrobates auratus, is capable of both spatial learning and higher-order contingency learning, abilities that depend on the hippocampus in mammals. Understanding the neurobiological adaptations that underpin the cognitive abilities of D. auratus will enable us to identify structure-function relationships underlying cognition in amphibians, and in turn, provide critical insight into the evolution of vertebrate cognition.
Ambient levels of nonionizing electromagnetic fields (EMF) have risen sharply in the last five decades to become a ubiquitous, continuous, biologically active environmental pollutant, even in rural and remote areas. Many species of flora and fauna, because of unique physiologies and habitats, are sensitive to exogenous EMF in ways that surpass human reactivity. This can lead to complex endogenous reactions that are highly variable, largely unseen, and a possible contributing factor in species extinctions, sometimes localized. Non-human magnetoreception mechanisms are explored. Numerous studies across all frequencies and taxa indicate that current low-level anthropogenic EMF can have myriad adverse and synergistic effects, including on orientation and migration, food finding, reproduction, mating, nest and den building, territorial maintenance and defense, and on vitality, longevity and survivorship itself. Effects have been observed in mammals such as bats, cervids, cetaceans, and pinnipeds among others, and on birds, insects, amphibians, reptiles, microbes and many species of flora. Cyto- and geno-toxic effects have long been observed in laboratory research on animal models that can be extrapolated to wildlife. Unusual multi-system mechanisms can come into play with non-human species — including in aquatic environments — that rely on the Earth’s natural geomagnetic fields for critical life-sustaining information. Part 2 of this 3-part series includes four online supplement tables of effects seen in animals from both ELF and RFR at vanishingly low intensities. Taken as a whole, this indicates enough information to raise concerns about ambient exposures to nonionizing radiation at ecosystem levels. Wildlife loss is often unseen and undocumented until tipping points are reached. It is time to recognize ambient EMF as a novel form of pollution and develop rules at regulatory agencies that designate air as ‘habitat’ so EMF can be regulated like other pollutants. Long-term chronic low-level EMF exposure standards, which do not now exist, should be set accordingly for wildlife, and environmental laws should be strictly enforced — a subject explored in Part 3.
We provide the first evidence for y-axis magnetic compass orientation in Alytes obstetricans. Evidence for wavelength-dependent effect of light on magnetic compass orientation is also shown. In the first series of experiments, two groups of tadpoles were tested shortly after being collected from a pond with a natural shoreline and a clearly defined y-axis under two different lighting conditions (full-spectrum and long-wavelength light). Magnetic bearings from tadpoles tested under full-spectrum natural skylight displayed bimodal distribution along an axis that coincided with the magnetic direction of the y-axis in their home pond, while those tested under long-wavelength light failed to exhibit a consistent overall direction of orientation relative to the magnetic field, although a subset of tadpoles exhibited magnetic compass orientation that was rotated about 90° counter-clockwise of the magnetic direction of the y-axis in their home pond. In the second series of experiments, tadpoles were collected from a watering trough without a defined y-axis, trained to learn the direction of the y-axis in tanks with an artificial shore at one end and tested under full-spectrum natural skylight. Tadpoles from the two trained groups showed bimodal magnetic compass orientation along the shore–deep water magnetic axis of their respective training tanks. The present findings widen the number of species with y-axis magnetic compass orientation to include Alytidae, a family of primitive semiterrestrial frogs.
The magnetic compass is an important element of the avian navigation system, which allows migratory birds to solve complex tasks of moving between distant breeding and wintering locations.
The photochemical magnetoreception in the eye is believed to be the primary biophysical mechanism behind the magnetic sense of birds. It was shown previously that birds were disoriented in presence of weak oscillating magnetic fields (OMF) with frequencies in the megahertz range. The OMF effect was considered to be a fingerprint of the photochemical magnetoreception in the eye. In this work, we used miniaturized portable magnetic coils attached to the bird’s head to specifically target the compass receptor. We performed behavioural experiments on orientation of long-distance migrants, garden warblers (Sylvia borin), in round arenas. The OMF with the amplitude of about 5 nT was applied locally to the birds’ eyes. Surprisingly, the birds were not disoriented and showed the seasonally appropriate migratory direction. On the contrary, the same birds placed in a homogeneous 5 nT OMF generated by large stationary coils showed clear disorientation. On the basis of these findings, we suggest that the
disruption of magnetic orientation of birds by oscillating magnetic fields is not related to photochemical magnetoreceptors in their eyes
This review discusses chiral-at-metal complexes and introduces enantiomorphs from assembly structure. Owing to the diverse coordination number and activity of metal ions as chiral centers, abundant structures for chiral selectivity, catalysis, and polarized light-response are the notable advantages of the chiral-at-metal complexes. The rational design and preparation of linear multi-dentate ligands is a good choice to improve the stability of chiral complexes, such as multi-bonding structure for high stability as a self-limiting system. The bio-significance and potential application of chiral-at-metal complexes are discussed, such as the synergistic effect of catalysis and chiral selectivity of the metal center in enzymes. Enzyme could be remolded to replace the original central metal ions with highly active rare earth or precious metal ions to form artificial metalloenzyme or to remove the “redundant” part around the metal center to improve the accessibility of substrate. The polarized light-response mechanism of chiral opsin is introduced in relation to its role in animal migration. Metal-organic frameworks (MOFs) are crystalline and porous materials built from metal nodes or clusters and organic linkers and provide the possibility to prepare artificial enantiomorphs. The preparations, applications, and characterization methods of MOF enatiomorphs are therefore introduced. We hope this review inspires researchers at all levels of their career to consider the title topic in their own research in terms of its application and potential value.
Natural light plays an integral role in biological systems, one that can be disrupted by the intrusion of other light sources. Specifically, artificial lighting, including road lighting, poses negative effects on plant and animal physiology, animal behaviour and predation rates. These effects are cumulative as multiple, artificial light sources contribute. 1 Light functions as a natural stimulus. 2 Metrics used to quantify artificially produced light are generally not biologically relevant. 3 Species response to artificial light varies by visual system. 4 Light emitted varies relative to the type of lighting technology. 5 Planning for road lighting must include zoning relative to light levels and light-fixture placement. 6 Mitigating the negative effects of road lighting requires research collaboration. Negative effects of artificial lighting, including road lighting, are manageable. By better understanding the ecosystems through which roads pass and how light affects resident organisms, we can adapt lighting fixtures, fixture design and zoning to minimise site-specific effects, as well as contributions to cumulative light pollution.
The astounding diversity of life that we see today is the product of species multiplication and morphological divergence through geological time. Evidence from the fossil record shows that this evolutionary radiation has not occurred at an even rate. Instead, relatively short-lasting phases of evolution have produced the major radiations that are seen in many taxonomic groups, such as flowering plants during the late Cretaceous. This volume surveys patterns of major evolutionary radiation and their possible causes.
The scapulocoracoid of Czatkobatrachus polonicus Evans and Borsuk-Białynicka, 1998, a stem-frog from the Early Triassic karst locality of Czatkowice (Southern Poland), is described. The overall type of scapulocoracoid is plesiomorphic, but the subcircular shape and laterally oriented glenoid is considered synapomorphic of Salientia. The supraglenoid foramen is considered homologous to the scapular cleft of the Anura. In Czatkobatrachus, the supraglenoid foramen occupies an intermediate position between that of the early tetrapod foramen and the scapular cleft of Anura. The cleft scapula is probably synapomorphic for the Anura. In early salientian phylogeny, the shift in position of the supraglenoid foramen may have been associated with an anterior rotation of the forelimb. This change in position of the forelimb may reflect an evolutionary shift from a mainly locomotory function to static functions (support, balance, eventually shock-absorption). Laterally extended limbs may have been more effective than posterolateral ones in absorbing landing stresses, until the specialised shock-absorption pectoral mechanism of crown-group Anura had developed. The glenoid shape and position, and the slender scapular blade, of Czatkobatrachus, in combination with the well-ossified joint surfaces on the humerus and ulna, all support a primarily terrestrial rather than aquatic mode of life. The new Polish material also permits clarification of the pectoral anatomy of the contemporaneous Madagascan genus Triadobatrachus.
Differences in integumentary permeability dictate alternative life history strategies in amphibians and reptiles. Limiting resources for amphibians are chiefly associated with availability of water and, as a consequence, amphibian migrations are chiefly associated with movements to and from aquatic breeding habitats. These cyclic migrations from breeding to overwintering sites may be direct, or may be interrupted by periods of residence at foraging sites. In general, migrations take place over relatively short distances and are constrained by the problem of water balance associated with exposure during longer overland journeys. Many amphibians exhibit complex mechanisms of orientation involving multiple sensory modalities and are capable of precise homing abilities. Among reptiles, migrations are chiefly associated with travel to and from egg laying sites, as displayed by turtles, or communal hibernacula, as is characteristic of some snakes. Marine turtles, in particular, undertake long distance migrations (up to thousands of kilometers) to reach nesting beaches and, sometimes, foraging grounds. In these chelonians, complex patterns of movement vary ontogenetically, as well as by gender and species. A variety of cues are used to locate destinations, including celestial, geomagnetic, olfactory, auditory, thermal, wave, and current pattern signals; however, evidence of a map-compass system of navigation is equivocal. The migratory patterns of amphibians and reptiles often bring them into conflict with human resource utilization. For amphibians, breeding migrations that cross busy roads or areas turned over to agricultural production lead to mass mortality. Marine turtle migratory pathways often result in conflicts with fishery activities. Knowledge of life history strategies and associated migratory behavior is essential for effective conservation measures.
Many biochemical, physiological and behavioural processes show circadian rhythms which are generated by an internal timekeeping mechanism referred to as the biological clock. According to rapidly developing models, the core oscillator driving this clock is composed of an autoregulatory transcription- (post) translation-based feedback loop involving a set of 'clock' genes1-6. Molecular docks do not oscillate with an exact 24-hour rhythmicity but are entrained to solar day/night rhythms by light. The mammalian proteins Cry1 and Cry2, which are members of the family of plant blue-light receptors (cryptochromes) and photolyases, have been proposed as candidate light receptors for photoentrainment of the biological clock7-10. Here we show that mice lacking the Cry1 or Cry2 protein display accelerated and delayed free-running periodicity of locomotor activity, respectively. Strikingly, in the absence of both proteins, an instantaneous and complete loss of free- running rhythmicity is observed. This suggests that, in addition to a possible photoreceptor and antagonistic clock-adjusting function, both proteins are essential for the maintenance of circadian rhythmicity.
Triturus alpestris has been found to be adept at homing, and previous studies have found that its orientation behaviour during breeding migration can be explained, at least in part, by the use of olfactory cues from the breeding pond. Nonetheless, the use of chemical cues from the pond probably does not support a guidance strategy when the newts are far from the pond. Hence, T. alpestris may rely on other orientation cues. In this study, alpine newts were tested in a circular arena to determine the sensory cues used to locate breeding ponds. Animals were collected from a permanent pond situated in northern Spain, taken to the experimental site 9020 m distant, and tested for orientation under a variety of conditions (i.e., orientation under a clear night sky, orientation under dark conditions, and orientation under a clear night sky in the presence of an altered geomagnetic field). The possibility of a non-homing directional bias was also tested. Newts chose a compass course in the direction of their breeding pond only when the ambient geomagnetic field and the celestial cues were simultaneously available. Conversely, animals failed to orient only when celestial cues or the geomagnetic field were the sole orientation cues available.
Experiments were carried out to investigate whether premetamorphic larvae of Boscas newt (Triturus boscai) are capable of using the geomagnetic field for Y-axis orientation (i.e., orientation toward and away from shore). Larvae were trained outdoor in two different training configurations, using one training tank aligned along the magnetic north–south axis, with shore facing north, and another training tank positioned with its length along the east–west axis, with shore located west. After training, premetamorphic newts were tested in an outdoor circular arena surrounded by a pair of orthogonally aligned cube-surface coils used to alter the alignment of the Earths magnetic field. Each newt was tested only once, in one of four magnetic field alignments: ambient magnetic field (i.e., magnetic north at North), and three altered fields (magnetic north rotated to East, West, South). Distributions of magnetic bearings from tested larvae indicated that they oriented bimodally along the magnetic direction of the trained Y-axis. These findings demonstrate that T. boscai larvae are sensitive to the geomagnetic field and can use it for orienting along a learned Y-axis. This study is the first to provide evidence of Y-axis orientation, accomplished by a magnetic compass, in larval urodeles.
Magnetic compass orientation by amphibians, and some insects, is mediated by a light-dependent magnetoreception mechanism. Cryptochrome photopigments, best known for their role in circadian rhythms, are proposed to mediate such responses. In this paper, we explore light-dependent properties of magnetic sensing at three levels: (i) behavioural (wavelength-dependent effects of light on magnetic compass orientation), (ii) physiological (photoreceptors/photopigment systems with properties suggesting a role in magnetoreception), and (iii) molecular (cryptochrome-based and non-cryptochrome-based signalling pathways that are compatible with behavioural responses). Our goal is to identify photoreceptors and signalling pathways that are likely to play a specialized role in magnetoreception in order to definitively answer the question of whether the effects of light on magnetic compass orientation are mediated by a light-dependent magnetoreception mechanism, or instead are due to input from a non-light-dependent (e.g. magnetite-based) magnetoreception mechanism that secondarily interacts with other light-dependent processes.
Cryptochromes have been suggested to be the primary magnetoreceptor molecules underlying light-dependent magnetic compass detection in migratory birds. Here we review and evaluate (i) what is known about these candidate magnetoreceptor molecules, (ii) what characteristics cryptochrome molecules must fulfil to possibly underlie light-dependent, radical pair based magnetoreception, (iii) what evidence supports the involvement of cryptochromes in magnetoreception, and (iv) what needs to be addressed in future research. The review focuses primarily on our knowledge of cryptochromes in the context of magnetoreception.
Since 1960, magnetic fields have been discussed as Zeitgebers for circadian clocks, but the mechanism by which clocks perceive and process magnetic information has remained unknown. Recently, the radical-pair model involving light-activated photoreceptors as magnetic field sensors has gained considerable support, and the blue-light photoreceptor cryptochrome (CRY) has been proposed as a suitable molecule to mediate such magnetosensitivity. Since CRY is expressed in the circadian clock neurons and acts as a critical photoreceptor of Drosophila's clock, we aimed to test the role of CRY in magnetosensitivity of the circadian clock. In response to light, CRY causes slowing of the clock, ultimately leading to arrhythmic behavior. We expected that in the presence of applied magnetic fields, the impact of CRY on clock rhythmicity should be altered. Furthermore, according to the radical-pair hypothesis this response should be dependent on wavelength and on the field strength applied. We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms. This effect was maximal at 300 muT, and reduced at both higher and lower field strengths. Clock response to magnetic fields was present in blue light, but absent under red-light illumination, which does not activate CRY. Furthermore, cry(b) and cry(OUT) mutants did not show any response, and flies overexpressing CRY in the clock neurons exhibited an enhanced response to the field. We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism. CRY is widespread throughout biological systems and has been suggested as receptor for magnetic compass orientation in migratory birds. The present data establish the circadian clock of Drosophila as a model system for CRY-dependent magnetic sensitivity. Furthermore, given that CRY occurs in multiple tissues of Drosophila, including those potentially implicated in fly orientation, future studies may yield insights that could be applicable to the magnetic compass of migratory birds and even to potential magnetic field effects in humans.
Indoor tests of Bullfrog tadpoles and the eft and adult stages of Eastern Red Spotted Newts under linearly polarized light indicate that these two species can perceive the e-vector for spatial orientation. Other tests out of doors, under clear blue skies after sunset, indicate that both species can use the polarization patterns of the natural sky for orientation. Further, outdoor tests of Bullfrog tadpoles after sunset indicate that the reception of linearly polarized light does not reside in the eyes, but probably is associated with the pineal complex.
Schulten K. Magnetic field effects in chemistry and biology // Festkörperprobleme / J. Treusch, ed.
Braunschweig, 1982. V. 22. P. 61–83.
Electron transfer processes which generate radical pairs in coherent electron spin states (singlet or triplet) are affected by weak magnetic fields [Schulten et al, Z. physik. Chem. Neue Folge 101 (1976) 371]. Based on this finding we suggest a reaction mechanism for a chemical compass which exhibits a sensitivity on the orientation of the geomagnetic field originating from an anisotropy of the hyperfine interaction experienced by unpaired electron spins in a redox process. It is argued that such mechanism may explain the ability of many biological species to orient themselves inthe geomagnetic field.
Migratory birds possess a physiological magnetic compass that helps them
to find north during their migratory flights, but the mechanism
underlying this ability is not understood. In vitro experiments show
that two types of mechanisms are in principle capable of detecting
earth-strength magnetic fields in biological systems: the use of
biological magnetic materials such as magnetite crystals, or
magnetically sensitive chemical reactions. We have recently demonstrated
that oscillating magnetic fields can provide a viable diagnostic test to
identify the existence of a radical-pair mechanism as they will not
affect the properties of magnetite-based sensors, but disrupt a
radical-pair based mechanism through resonance effects. European robins,
a species of migratory birds, were disoriented in a magnetic orientation
test when a very weak (100 nT) oscillating field of 1.3 or 7 MHz was
added to the geomagnetic field. Moreover, the effect of the oscillating
field depended on the alignment of oscillating field with the
geomagnetic field and showed an intensity dependence consistent with
theoretical expectations from the radical pair mechanism, thereby
providing evidence for the existence of a radical-pair mechanism in
birds. We will discuss future avenues of research towards identifying
not only the mechanism, but also the chemical nature of the receptors
underlying magnetoreception, and in particular the photoreceptor
chryptochrome, an emerging candidate for the long sought after
magnetoreceptor.
The Earth's magnetic field provides an important source of directional information for terrestrial organisms, but the sensory receptor or receptors responsible for magnetic field detection have yet to be identified. Theoretical models of the mechanism of magnetoreception have implicated specialized photoreceptors. the proposed mechanism would amplify the weak interaction of the geomagnetic field with a single electron spin to the level of photo detection, resulting in a modulation of the photoreceptor response to light. Although behavioural, and neurophysiological studies have established a link between magnetic field sensitivity and the visual system, definitive evidence for the use of a light-dependent mechanism has been lacking. Here we show that magnetic compass orientation in a semiaquatic salamander is affected by the wavelength of light, and that this wavelength-dependence is due to a direct effect of light on the underlying magnetoreception mechanism.
Concern about the effect of halocarbons on the concentration of ozone in the stratosphere has led to considerable interest in that part of halocarbon chemistry which produces the species responsible for ozone depletion. Here, the energy disposal and branching ratios in the reactions of O(1D2) with CHCl3 and CHF3 have been measured using an implementation of time-resolved Fourier transform spectroscopy, and the results are reported. The reaction with CHCl3 produces OH, HCl, and CO as primary products. The OH vibrational excitation indicates simple abstraction dynamics. The HCl has much lower vibrational excitation characteristic of a longer-lived insertion elimination process which also produces CO in the decomposition of the internally excited Cl2CO product. Only HF is observed in the reaction with CHF3. In this case the vibrational distribution is nonmonotonic, indicating contributions from two microscopic channels.
The use of a magnetic compass plays a significant role in the daily and seasonal movements of numerous organisms; however among amphibians, magnetic compass orientation has been convincingly demonstrated only in eastern red-spotted newts, Notophthalmus viridescens, with some indirect evidence coming from several species of bufonid toads. In this study, larval bullfrogs, Rana catesbeiana, were trained in outdoor tanks with two different Y-axis (shore/deep water) directions and then tested in an indoor arena in one of four symmetrical alignments of an earth-strength magnetic field. The tadpoles oriented bimodally along the correct magnetic direction of the Y-axis experienced during training, demonstrating that this anuran species is able to learn and orient along the Y-axis by sensing the geomagnetic field.
Orientation toward and away from shore (y-axis orientation) plays an important role in the daily and seasonal movements of amphibians. A variety of studies have shown that amphibians use both celestial cues and the geomagnetic field for y-axis orientation. However, few studies have addressed how quickly amphibians are able to learn the direction of a new shore. In the present laboratory-based experiments, we show that the Eastern Red-Spotted Newt, Notophthalmus viridescens, is able to learn the direction of the y-axis with respect to the geomagnetic field within 12–16 h. In conjunction with previous findings, our results suggest that the geomagnetic field is an important and readily used cue for orientation in amphibians.
The shoreward magnetic compass orientation of male eastern red-spotted newts (Notophthalmus viridescens) was examined in a visually-symmetrical indoor arena. Groups of newts were first trained in a water-filled outdoor tank with an artificial shore at one end and then exposed to a rapid elevation of the training tank water temperature just prior to testing. The directional response of individual newts was observed in the indoor arena in one of four horizontal alignments of the magnetic field (magnetic north at north, east, south or west). Magnetic bearings were pooled from the four magnetic field alignments for analysis. In each test, newts were alternately tested under either 450 nm or 550 nm light (of equal quantal flux) and under full spectrum light. Newts tested under full spectrum light exhibited shoreward magnetic orientation. The distribution of magnetic bearings exhibited by newts under 450 nm light was indistinguishable from that of full spectrum controls. In contrast, the distribution of bearings obtained under 550 nm light differed significantly from controls, exhibiting a shift in orientation of approximately 90° counterclockwise. This wavelength-dependent effect of light on magnetic compass orientation in newts is consistent with the proposed involvement of the visual system in magnetoreception.
Young Fowler's toads from on and near the shores of a lake were tested in a circular pen 60 feet in diameter. Under a variety of conditions (e.g. including group tests, individual tests, simultaneous testing of two groups from different shores, long distance displacement, and transit to the test pen both in view of the sky and in lightproof containers), the toads oriented under the sun to a compass direction (Y-axis) corresponding to a line bisecting the home shoreline at right angles. This orientation persisted after 72 hours in darkness, indicating the existence of an internal clock mechanism. Reorientation to a new shore was evident in 24 hours and was virtually complete after 48 hours. Orientation failed or was partially inhibited in small toads tested under dense cloud cover, at noon, and after sunset. Also, the type of orientation exhibited under the sun was evident at night under the moon, but to a lesser extent under starry skies. These mechanisms are useful in foraging and in dispersal from nursery shores. Adults are oriented at night to the breeding site even without benefit of a chorus for reference. Adults oriented to the Y-axis of the breeding site. A recorded chorus distracted migrating adults pursuing a compass course toward a pond. Non-breeding adults compensated for a displacement made in view of the sun. Celestial orientation is considered a basic orientational mechanism which most likely developed early in anuran history.
IntroductionOutliersGoodness-Of-FitRobust MethodsBootstrap MethodsDensity EstimationBayesian Methods
Other Methods
Cryptochromes are blue, ultraviolet-A photoreceptors. They were first characterized for Arabidopsis and are also found in ferns and algae; they appear to be ubiquitous in the plant kingdom. They are flavoproteins similar
in sequence to photolyases, their presumptive evolutionary ancestors. Cryptochromes mediate a variety of light responses,
including entrainment of circadian rhythms inArabidopsis, Drosophila, and mammals. Sequence comparison indicates that the plant and animal cryptochrome families have distinct evolutionary histories,
with the plant cryptochromes being of ancient evolutionary origin and the animal cryptochromes having evolved relatively recently.
This process of repeated evolution may have coincided with the origin in animals of a modified circadian clock based on the
PERIOD, TIMELESS, CLOCK, and CYCLE proteins.
Apparatus and techniques were developed to test bufonid's use of celestial cues to find preferred directions in controlled experiments. Toads were trained to select an escape direction relative to a sun lamp and were found to maintain a course at the same angle to the light cue when the apparatus was rotated, the light moved, when tested outdoors under the sun, and if various lamps (e.g., bright incandescent, dim incandescent, infrared, and red flood) were substituted for the sun lamp. Reference objects, learned muscular movements, sounds, and odors were eliminated as possible orientational cues in this investigation. Toads could not orient to the learned direction when the light cue was obscured and the shadows were evenly distributed. B. w. f owleri possess a clocking mechanism and are able to compensate for the apparent 15° per hour movement of the cue throughout a diel cycle. The azimuth of the cue seems to be more important than the altitude to toads. Trained animals can be diverted from a trained direction by conspecific calls after injections of sex hormones. Celestial orientation is considered a basic orientational mechanism and apparently functions in conjunction with other mechanisms in the natural environment of toads.
Experiments were carried out to investigate whether Iberian green frog tadpoles Pelophylax perezi (formerly Rana perezi) are able of using the geomagnetic field for y-axis orientation (i.e. orientation toward and away from shore). Tadpoles were trained outdoor for 5 d, in two differ- ent training configurations: (i) a training tank aligned along the mag- netic north-south axis, with shore facing south, and (ii) a training tank aligned along the magnetic east-west axis, with shore located east, and similar to the shore-deep water axis ('y-axis') found in their home stream, which flows from south to north. After training, tadpoles were individually tested for magnetic orientation in a water-filled circular outdoor arena surrounded by a pair of orthogonally aligned cube-sur- face-coils used to alter the alignment of the earth's magnetic field. Tad- poles held in the east-west training tank oriented towards shore, indicating that they were able to distinguish between the shoreward and waterward direction along the y-axis. Tadpoles trained in the tank that was aligned along the north-south axis showed bimodal magnetic compass orientation along the shore-deep water magnetic axis. These findings provide evidence for the use of magnetic compass cues for y-axis orientation by P. perezi tadpoles.
Previous studies have demonstrated the presence of a light-dependent magnetic compass in a urodele amphibian, the eastern red-spotted newt Notophthalmus viridescens, mediated by extraocular photoreceptors located in or near the pineal organ. Newts tested under long-wavelength (≥500 nm) light exhibited a 90° shift in the direction of orientation relative to newts tested under full spectrum (white) or short-wavelength light. Here we report that bullfrog tadpoles Rana catesbeiana (an anuran amphibian) exhibit a 90° shift in the direction of magnetic compass orientation under long-wavelength (≥500 nm) light similar to that observed in newts, suggesting that a common light-dependent mechanism mediates these responses. These findings suggest that a light-dependent magnetic compass may have been the ancestral state in this group of vertebrates.
Spatial orientation corresponding to the bearing of thee-vector of linearly polarized light can be demonstrated in sighted and eyeless salamanders (Ambystoma tigrinum) trained under linearly polarized light. However, if opaque polyethylene plastic is inserted over the skull of these animals, whether they are sighted or eyeless, orientation is uniform within the test arena. Bidirectional oriented movement is restored in both groups, however, when transparent plastic is substituted in the same animals. A discussion of the possible mechanism for perception of polarized light by extraocular photoreceptors (EOPs) is given.Durch Dressur unter linear polarisiertem Licht wird beiAmbystoma tigrinum sowohl mit als auch ohne Augen eine Orientierung nach deme-Vektor linear polarisierten Lichtes nachgewiesen. Wird jedoch ber dem Schdel (unter der Haut) eine opake Polythylen-Scheibe eingeschoben, so findet sich weder bei geblendeten noch bei Tieren mit Augen eine Orientierung nach deme-Vektor. Wird die opake Plastikscheibe durch eine transparente ersetzt, so tritt in jedem Fall die Orientierung ( 180 ) wieder auf. Die mglichen Mechanismen der Wahrnehmung polarisierten Lichtes durch extraokulare Rezeptoren werden diskutiert.
Chemical and biological photoprocesses which involve bimolecular reactions between non-zero spin intermediates, e.g. doublet
molecules 2A+2B, often produce the intermediate molecular pair in a pure overall spin state, e.g. a singlet state 1(2A+2B). and select for the reaction channels again such spin states, e.g. a triplet state 3(2A+2B). The necessery transition 1(2A+2B)→3(2A+2B) is affected by magnetic interactions (hyperfine, Zeeman, zero field splitting) and can be influenced by magnetic fields.
Examples are photoinduced electron transfer processes, e.g. the primary reaction of photosynthesis.
A system of five, equally‐spaced, square coils which provides a uniform magnetic field over a considerable volume is described. The region of uniformity is easily accessible from outside the coils. The method used to design the system is discussed.
Ultraviolet stimuli cause a long-lasting inhibition, reversible by long-wavelength stimuli, of normal dark activity of the frog frontal organ. Inhibition can be both initiated and abolished in the absence of sodium ions and presumably, receptor potentials. Inhibition and its abolition may arise from photointerconversions of two states of a single visual pigment.
It has been suggested that chemical reactions proceeding through radical pair intermediates could form the basis of bird’s ability to sense the geomagnetic field as a source of compass information [Biophys. J. 78 (2000) 707]. We present calculations of anisotropic reaction product yields for a flavin–tryptophan radical pair subject to a magnetic field of ∼50 μT. The anisotropic response of the reaction is found to be dominated by two nitrogen nuclei in the flavin radical which have near-axial hyperfine interactions with almost collinear principal axes. It is shown that the anisotropy of the product yields is not strongly dependent on the lifetime of the radical pair in the range 1–5 μs, and that it can be tuned by small variations in the hyperfine tensors of the nuclear spins in the two radicals.
Although many animals use the Earth's magnetic field for orientation and navigation, the precise biophysical mechanisms underlying magnetic sensing have been elusive. One theoretical model proposes that geomagnetic fields are perceived by chemical reactions involving specialized photoreceptors. However, the specific photoreceptor involved in such magnetoreception has not been demonstrated conclusively in any animal. Here we show that the ultraviolet-A/blue-light photoreceptor cryptochrome (Cry) is necessary for light-dependent magnetosensitive responses in Drosophila melanogaster. In a binary-choice behavioural assay for magnetosensitivity, wild-type flies show significant naive and trained responses to a magnetic field under full-spectrum light ( approximately 300-700 nm) but do not respond to the field when wavelengths in the Cry-sensitive, ultraviolet-A/blue-light part of the spectrum (<420 nm) are blocked. Notably, Cry-deficient cry(0) and cry(b) flies do not show either naive or trained responses to a magnetic field under full-spectrum light. Moreover, Cry-dependent magnetosensitivity does not require a functioning circadian clock. Our work provides, to our knowledge, the first genetic evidence for a Cry-based magnetosensitive system in any animal.
Consisting of more than six thousand species, amphibians are more diverse than mammals and are found on every continent save Antarctica. Despite the abundance and diversity of these animals, many aspects of the biology of amphibians remain unstudied or misunderstood. The Ecology and Behavior of Amphibians aims to fill this gap in the literature on this remarkable taxon. It is a celebration of the diversity of amphibian life and the ecological and behavioral adaptations that have made it a successful component of terrestrial and aquatic ecosystems. Synthesizing seventy years of research on amphibian biology, Kentwood D. Wells addresses all major areas of inquiry, including phylogeny, classification, and morphology; aspects of physiological ecology such as water and temperature relations, respiration, metabolism, and energetics; movements and orientation; communication and social behavior; reproduction and parental care; ecology and behavior of amphibian larvae and ecological aspects of metamorphosis; ecological impact of predation on amphibian populations and antipredator defenses; and aspects of amphibian community ecology. With an eye towards modern concerns, The Ecology and Behavior of Amphibians concludes with a chapter devoted to amphibian conservation. An unprecedented scholarly contribution to amphibian biology, this book is eagerly anticipated among specialists.
Phylogenetic relationships among the salamander families have been difficult to resolve, largely because the window of time in which major lineages diverged was very short relative to the subsequently long evolutionary history of each family. We present seven new complete mitochondrial genomes representing five salamander families that have no or few mitogenome records in GenBank in order to assess the phylogenetic relationships of all salamander families from a mitogenomic perspective. Phylogenetic analyses of two data sets-one combining the entire mitogenome sequence except for the D-loop, and the other combining the deduced amino acid sequences of all 13 mitochondrial protein-coding genes-produce nearly identical well-resolved topologies. The monophyly of each family is supported, including the controversial Proteidae. The internally fertilizing salamanders are demonstrated to be a clade, concordant with recent results using nuclear genes. The internally fertilizing salamanders include two well-supported clades: one is composed of Ambystomatidae, Dicamptodontidae, and Salamandridae, the other Proteidae, Rhyacotritonidae, Amphiumidae, and Plethodontidae. In contrast to results from nuclear loci, our results support the conventional morphological hypothesis that Sirenidae is the sister-group to all other salamanders and they statistically reject the hypothesis from nuclear genes that the suborder Cryptobranchoidea (Cryptobranchidae+Hynobiidae) branched earlier than the Sirenidae. Using recently recommended fossil calibration points and a "soft bound" calibration strategy, we recalculated evolutionary timescales for tetrapods with an emphasis on living salamanders, under a Bayesian framework with and without a rate-autocorrelation assumption. Our dating results indicate: (i) the widely used rate-autocorrelation assumption in relaxed clock analyses is problematic and the accuracy of molecular dating for early lissamphibian evolution is questionable; (ii) the initial diversification of living amphibians occurred later than recent estimates would suggest, from the Late Carboniferous to the Early Permian (approximately 294 MYA); (iii) living salamanders originated during the Early Jurassic (approximately 183 MYA), and (iv) most salamander families had diverged from each other by Late Cretaceous. A likelihood-based ancestral area reconstruction analysis favors a distribution throughout Laurasia in the Early Jurassic for the common ancestor of all living salamanders.
The annual migration of the Monarch butterfly (Danaus plexippus) from eastern North America to central Mexico is one of nature's most inspiring spectacles. Recent studies including one in BMC Biology, have begun to dissect the molecular and neurogenetic basis for this most complex behavior.
In the last decades, it has been demonstrated that many animal species orient in the Earth magnetic field. One of the best-studied examples is the use of the geomagnetic field by migratory birds for orientation and navigation. However, the biophysical mechanism underlying animal magnetoreception is still not understood. One theory for magnetoreception in birds invokes the so-called radical-pair model. This mechanism involves a pair of reactive radicals, whose chemical fate can be influenced by the orientation with respect to the magnetic field of the Earth through Zeeman and hyperfine interactions. The fact that the geomagnetic field is weak, i.e., approximately 0.5 G, puts a severe constraint on the radical pair that can establish the magnetic compass sense. For a noticeable change of the reaction yield in a redirected geomagnetic field, the hyperfine interaction has to be as weak as the Earth field Zeeman interaction, i.e., unusually weak for an organic compound. Such weak hyperfine interaction can be achieved if one of the radicals is completely devoid of this interaction as realized in a radical pair containing an oxygen molecule as one of the radicals. Accordingly, we investigate here a possible radical pair-based reaction in the photoreceptor cryptochrome that reduces the protein's flavin group from its signaling state FADH* to the inactive state FADH- (which reacts to the likewise inactive FAD) by means of the superoxide radical, O2*-. We argue that the spin dynamics in the suggested reaction can act as a geomagnetic compass and that the very low physiological concentration (nM-microM) of otherwise toxic O2*- is sufficient, even favorable, for the biological function.
Migratory birds travel vast distances each year, finding their way by various means, including a remarkable ability to perceive the Earth's magnetic field. Although it has been known for 40 years that birds possess a magnetic compass, avian magnetoreception is poorly understood at all levels from the primary biophysical detection events, signal transduction pathways and neurophysiology, to the processing of information in the brain. It has been proposed that the primary detector is a specialized ocular photoreceptor that plays host to magnetically sensitive photochemical reactions having radical pairs as fleeting intermediates. Here, we present a physical chemist's perspective on the "radical pair mechanism" of compass magnetoreception in birds. We outline the essential chemical requirements for detecting the direction of an Earth-strength approximately 50 microT magnetic field and comment on the likelihood that these might be satisfied in a biologically plausible receptor. Our survey concludes with a discussion of cryptochrome, the photoactive protein that has been put forward as the magnetoreceptor molecule.
(Graph Presented) Compass component: Blue-light excitation of the photoreceptor cryptochrome generates a transient radical pair by electron transfer from a tryptophan (Trp) at the surface to the flavin cofactor in the center of the protein (see picture; FAD=flavin adenine dinucleotide). Simulated EPR spectra show that the electronic coupling parameters of these radical pairs are suitable for animal magnetoreception.