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date: 23 May 2018

Magnetoreception of Invertebrates

Abstract and Keywords

Exploiting invertebrates, such as the fruit fly Drosophila or nematode Caenorhabditis, with a modifiable genome seems to be key to answering the fundamental question of the molecular principle of magnetoreception. This review presents the state of knowledge on invertebrate sensitivity to geomagnetic field (GMF) over the last 20 years from a number of viewpoints, with particular emphasis on the behavioral aspect of testing. It shows that experimental approaches are generally specific to the particular research teams, and positive replication at other laboratories is practically nonexistent. The questions surrounding an animal compass are fascinating, but to achieve a level of knowledge of the magnetic sense at least closer to the other senses, a standardized, commercially available, and routinely applicable test on the classic invertebrate model to the natural GMF is still badly needed.

Keywords: magnetoreception, invertebrates, insects, mechanisms, orientation, compass, light, cryptochrome, magnetite

One of the basic prerequisites to the survival of organisms is their ability to detect the properties of the environment. In addition to the forms of energy perceivable by the human senses, such as photons, heat, mechanical stimuli, and the energy of chemical bonds, life has ever been surrounded by the geomagnetic field (GMF). The ability of animals to perceive it has been, after decades of research, documented with hundreds of behavioral studies, but fundamental questions related to its mechanism, the localization of receptors, and in some cases, surprisingly, even the merit for its owner remain unanswered. Significant advances in the research, however, have been made in recent years thanks to the unprecedented possibilities provided by the use of techniques of functional genetics and transgenic lines of invertebrates.

This review does not aim to summarize all the reports of magnetoreception in invertebrates since research began more than 50 years ago and refers the reader to reviews devoted to particular taxons previously published (Walker, 1997; Riveros & Srygley, 2010; Wajnberg et al., 2010; Valkova & Vácha, 2012). This work intends rather to record the milestones achieved over the last two decades since the publication of the last summary review from Able (1996) and to show that invertebrates (previously bees, today rather fruit flies or nematodes) have great potential and that it is these inconspicuous organisms that will help resolve some of the burning questions in magnetoreception.

How Should the Term Magnetoreception Be Understood?

Because magnetoreception is, first and foremost, understood as one of the natural senses in animals, such a perspective allows avoiding all types of magnetic (and electromagnetic) fields of manmade origin, although these also may impact organisms and cannot be ignored. The primary concern here will be the research into the sensitivity to the GMF, which is relatively weak (from 25 to 65 uT) and stable over time. Where different magnitudes or fields variable over time are mentioned, this will relate to cases helping to understand the basic GMF reception.

What Purposes Does Reception Serve?

GMF has been generated by liquid materials circulating in the core of the Earth like an enormous dynamo since life first began. GMF protects the atmosphere and biosphere on Earth against the stream of particles from the Sun, and its ever-present polarized axis is extraordinarily suitable for the purpose of orientation. It acts as a directionally fixed force (by an arrow pointing to the planet’s magnetic poles Fig. 1). It provides a stable point in the landscape which, unlike other cues, does not change its position when an animal moves or as the time passes. A magnetic compass may be particularly useful for species moving in dense vegetation, underwater or underground, or under an overcast sky when celestial cues are not available (Gould, 1998).

Magnetoreception of InvertebratesClick to view larger

Figure 1 The geomagnetic field is well represented as an arrow pointing the bearing to the magnetic North (Nm). The length and the inclination of the arrow differ around the globe and may help to set geographical position.

(Based on Shaw et al., 2015)

In addition to compass orientation, the GMF also offers an analogy of a map allowing animals to localize their position even where they have never been before and to determine the direction to their goal. Maps use a system of two perpendicular axes making it possible to define any point in a grid of coordinates. Similarly, the GMF has a north-south, largely homogeneous gradient of magnetic inclination—an angle of magnetic force to the horizontal plane (Fig. 1). An animal capable of measuring the inclination thereby obtains the information on its geographical latitude. There is no similarly homogeneous gradient on the east-west axis (longitude) on the planetary scale and it is not, therefore, possible to assign a unique pair of magnetic coordinates to all points on the Earth. Nevertheless, the intensity of the GMF (length of the arrow) is, at least in limited regions, longitude dependent. An innate or acquired knowledge of these two parameters may form the basis of true navigation (Lohman et al., 2007). For animals with a limited action radius, which includes the majority of invertebrates, the local “magnetic landscape” formed by irregularly deposited minerals in the Earth’s crust may be more important to their map sense than global gradients. This magnetic relief may become part of a learned image of a given space or provide important orientation cues.

Terrestrial Magnetoreception: Mechanical or Chemical Nature?

From the viewpoint of neurobiology, the finding that there is a sensory input about which we do not know how its energy is transduced into cellular and membrane processes is one of the greatest challenges. In terrestrial animals, the existence of microscopic particles of iron oxides was understood as the only probable answer to this question when research began. Modern genetic techniques used over the last two decades have, however, provided increasing amounts of well-founded evidence for an alternative mechanism based on the chemical reactions sensitivity to the GMF. The two mechanisms may, nevertheless, exist alongside one another, each being used for a different purpose, as suggested for birds (Wiltschko et al., 2006), or separately in different species (Thalau et al., 2006). The possibility of their close cooperation within a single receptor structure cannot be excluded either (Qin et al., 2015).

Magnetite Reception—Ferum Oxide Particle Reception

A number of distinguished works (Eder et al., 2012; Winklhofer & Kirschvink, 2010; reviewed in Shaw et al., 2015) involve the description of a hypothetical mechanism of reception by means of nanoparticles of iron oxides (most frequently magnetite—Fe3O4) in tissues, for which reason only a basic characterization is to be given here. The strength of the ferum oxide particle (FOP) model lies in its simplicity which is underlined by its similarity with other known cellular mechanisms sensitive to mechanical forces and tensions. If microscopic particles with either a permanent or induced magnetic dipole are exposed to the surrounding GMF, mechanical forces act on them. Cell membranes can be extremely sensitive to a force, and there are a number of models as to how the movement of particles of magnetite could affect, for example, the function of ion channels and thereby result in the conversion of the magnetic energy into a change to the membrane potential (Cadiou & McNaughton, 2010; Fig. 2). This model has several characteristic features that are well met in certain animals. Most important, (1) such a magnetoreceptor does not require light to function. (2) It is a receptor sensitive on principle to the polarity of the magnetic field—that is, distinguishing magnetic north from south. (3) Its magnetic properties may also be impacted by a strong and short pulse of the external field. (4) Another supporting argument is the discovery of FOP in animal tissues. Their occurrence and properties have been documented relatively extensively in invertebrates and in social insects in particular (Wajnberg et al., 2010).

Magnetoreception of InvertebratesClick to view larger

Figure 2 Two hypothetical representations of how ferum oxide particle may transform magnetic energy into physical force via opening the cation channel in the cell membrane, hence enabling neural signalisation. Cluster of superparamagnetic particles (left) attached by a cytoskeletal filament to gating domain of force-gated channel moves along the geomagnetic field force. Chain of single-domain grains having stable moment rotates accordingly to the external field (right) and the filament transfers the torque to the channel.

(Based on Shaw et al., 2015)

Greatest attention has been devoted to FOPs in the bodies of tropical ants (Alves et al., 2014; Riveros et al., 2014) and bees (see below). Magnetite, as well as other iron oxides, has been detected by means of a wide range of techniques in the antennae, head, thorax, and abdomen of insects and in the nematode C. elegans (Cranfield et al., 2004). Because a magnetosensitive behavior has been found in respective species, the hypothesis of FOP reception represents a logic synthesis. Nevertheless, finding FOPs is not necessarily the path leading to a GMF receptor. A problem encountered by current research (Edelman et al. 2015) is the fact that iron oxides are a common component of physiological and metabolic processes in the body (Keim et al., 2002; Treiber et al., 2012). Besides, FOPs are widely occurring in nature (Kobayashi et al., 1995; Jandacka et al., 2015), and contamination of the surface of the body or the digestive tract of animals is difficult to avoid. As yet, there is no verified and generally accepted connection between findings of FOPs in invertebrates and either neural or behavioral manifestations of magnetoreception (Shaw et al., 2015). However, a number of indirect behavioral evidences speak in favor of the FOP model.

Returning to the characteristic features mentioned earlier, magnetic orientation in darkness is in total accordance with FOP reception. As, however, the difference between darkness and extremely weak light corresponding to a clear night may be decisive in magnetoreception experiments (Muheim et al., 2002; Bazalova et al., 2016), any assessment of light dependency must result from those experiments only that explicitly validate the complete darkness using infra-redtechnique to observe the animals. Numerous experiments do not follow such a condition. The role of light in bees’ magnetoreception does not provide an entirely consistent picture, though some experiments performed since 1993 (Table 1 and reviewed in Valkova & Vácha, 2012) show that their magnetoreception can function in the dark. A magnetic explanation for the orientation of bumblebees in a circular arena in complete darkness has also been suggested by Chittka et al. (1999), although a key experiment with artificial rotation of the GMF was not performed. The mealworm beetle Tenebrio molitor was originally reported to orient magnetically in darkness (Arendse, 1978), but later attempts at replication (Vácha & Soukopová, 2004) showed a dependence on white light. Recent data on C. elegans (Vidal-Gadea et al., 2015) show its ability of magnetoreception in complete darkness. For invertebrates, no overall conclusion on the influence of light can, therefore, be made.

The ability of a compass to directly distinguish the polarity of a magnetic vector is another property typical for FOP reception. A test in which the vertical component of the field is experimentally reversed is used to differentiate the animals with a polarity compass from those with an inclination compass (Fig. 3). An inclination compass is also known as an axial compass as it can only determine direction and not the polarity of the magnetic axis. The animal must then deduce the polarity (north end from south end) from the inclination. It is as if the compass needle was missing color markings of its north tip, though were able to rotate freely on all axes. Its point, which is tilted toward the ground, then points to the north (in the northern hemisphere). On the equator, where there is zero inclination, this type of compass is unable to distinguish polarity (Fig. 3D). An inclination compass conforms very well to the chemical mechanism. Nevertheless, an FOP mechanism that does not differentiate polarity is conceivable as well (Kirschvink, 1981; Winklhofer & Kirschvink, 2010). In contrast, a polarity compass is not compatible with the radical pair mechanism (see below). Spiny lobsters (Panulirus argus) have demonstrated a typical polarity reaction (Lohman et al., 1995), while an inclination compass has been shown in two species of insect—the mealworm beetle Tenebrio molitor (Vácha et al., 2008a) and the monarch butterfly Danaus plexippus (Guerra et al., 2014). Moreover, Danaus fixed to a flight simulator was disorientated when the vertical component was adjusted to zero. Although bees are also thought to use a polarity compass (Winklhofer & Kirschvink, 2010), no basic test with reversed inclination has been published. Generally speaking, two independent laboratories agree on an inclination compass, which makes it a relatively well-documented phenomenon in insects, but not generally valid for arthropods.

Magnetoreception of InvertebratesClick to view larger

Figure 3 Classical experiment giving evidence of inclination compass. After inversion of vertical component of the field, animal returns back (A → B)—polarity as well as technical compasses would show no reaction. Inversion of both components does not change orientation (A→C) but would reverse polarity and technical compasses bearings. If inclination is zeroed (D), polarity cannot be assessed by an animal.

Another discrimination experiment of true diagnostic significance relies on magnetic pulses. A strong (10–100 mT) and short (1–10 ms) pulse is, in theory, able to reverse the magnetic polarity of single-domain (SD) FOP. The animal should then also reverse its orientation. If its FOPs belong to the superparamagnetic (SPM—without a stable moment) category, the pulse can disrupt the particle organisation and therefore also any directional response (Davila et al., 2005; Winklhofer & Kirschvink, 2010). In invertebrates, pulses have only been used on insects and Caribbean spiny lobsters. Preliminary observations (n = 3, no controls) on honeybees, from which it is impossible to draw any general conclusions, have been reported by Kirschvink and Kobayashi-Kirschvink (1991). Perez et al. (1999) released monarch butterflies after a strong magnetic field treatment, though this was not the pulse but a 10 s exposure to a permanent magnet. Besides, results showing a loss of orientation in the treated butterflies were not, however, entirely convincing due to the apparent effects of wind, sun, and experimental cooling. The experiment with the leaf-cutter ants Atta colombica (Riveros & Srygley, 2008) remains, therefore, the only representative in insects. Rather than change their bearings, the ants lost their orientation after having been exposed to any kind of a magnetic pulse whether parallel or antiparallel. This type of response does not, however, exclude the possibility of a loss of orientation due to a nonspecific short-term stress caused by a field exceeding more than 1,000 times the natural background. Further experiments of this type should be conducted after at least a few hours of recovery period. The effect on the FOP should persist (Davila et al., 2005). Recently, Ernst and Lohmann (2016) succeeded to reverse the orientation of Caribbean spiny lobster by about 180° by applying parallel and antiparallel pulses first and testing them on the next day. This relatively simple experiment still has great informational value in supporting FOP-based compass and could, for this reason, inspire further studies.

Chemical Magnetoreception—Radical Pair Reception

The idea that some (photo)chemical reactions of organisms may be sensitive to the GMF has been convincingly expounded in several reviews over the last decade (Ritz et al., 2010; Mouritsen & Hore, 2012; Dodson et al., 2013; Hore & Mouritsen, 2016), for which reason only some basic facts and resulting assumptions will suffice here. The most likely type of GMF-sensitive reactions are those in which—after excitation by light—a transfer of an electron from donor to the adjacent acceptor molecule is initiated, creating a radical pair (RP). In this transient state, the two molecules share two spin-correlated unpaired electrons. The following course of the reaction depends on the relative orientation of the electrons’ spin, which is sensitive to the strength and direction of the external magnetic field. If the spins are oriented antiparallel (Singlet), the reaction will have a different yield than when they are oriented parallel (Triplet). The magnetic field affects the degree of S-T interconversions and, therefore, also the reaction yield. It is assumed that the most likely partners in the RP are the protein Cryptochrome (Cry) and its co-factor chromophore FAD (Ritz et al., 2000), although other pairs are also worthy of consideration (Lee et al., 2014). The proposed reaction is probably light driven, and color of the light may affect its progress. The likely receptor organ where RP reactions may occur is the retina (Schulten & Windemuth, 1986), where Cry may regulate the transmission of information from the photoreceptors of the eye. For instance, attenuation of light transduction is conceivable when the insect ommatidium is parallel to the magnetic axis (Fig. 4). Because only an islet of ommatidia in the semicircular compound eye would then be impacted, a magnetically induced pattern, for example, a dark spot, may be generated toward the magnetic pole. Findings of Cry in the retina of insects (Mazzotta et al., 2013; Bazalova et al., 2016) are consistent with this hypothesis.

Magnetoreception of InvertebratesClick to view larger

Figure 4 Scheme of chemical magnetoreception hypothesis. Left: Pair of radicals (D and A molecules) is created by light. Orientation of magnetic powerlines (arrows, OA-orientation A, OB-orientation B) controls transitions between singlet and triplet states, hence the rate of different products. Right: Insect ommatidium looking straight at the North is impacted by different products than the others and might “see” it.

As for FOPs, certain characteristics can be found for chemical magnetoreception. (1) It is light dependent. (2) A chemical compass cannot detect the field polarity. (3) A strong artificial magnetic pulse should have no lasting effect. (4) An experimentally applied radiofrequency (RF) magnetic field is able to interfere with unpaired electrons S-T transitions and disable the compass sensitivity. (5) The compass is dependent on the presence of Cry. Table 1 provides an overview of papers on invertebrates from the last 20 years documenting some of the typical features of FOP and RP reception.

Table 1 Selected Characteristic Parameters of Magnetoreception on Invertebrate Species From the Last 20 Years

Animal

Light and Color Dependent

Works in Darkness

Polar Compass

Axial—Inclination Compass

RF Sensitivity

Pulse Sensitivity

Cry Dependent

Reference

Fly

D. melanogaster

Yes

Yes

Phillips and Sayeed, 1993; Dommer et al., 2008; Gegear et al., 2008;

No

Bae et al., 2016

Butterfly

D. plexippus

Yes

Yes

See the text

Guerra et al., 2014;

Perez et al., 1999

Bee

A. mellifera

Yes

See the text

Leucht, 1984;

Schmitt and Esch, 1993;

Yes

Kirshvink and Kirschvink 1991;

Liang et al., 2016

Ant

A. colombica

Yes

Riveros and Srygley, 2008

F. pratensis

Yes

Camlitepe et al., 2005

Cockroach

P. americana

Yes

No

Yes

Yes

Bazalova et al., 2016;

B. germanica

Vácha et al., 2009

Beetle

T. molitor

Yes

Arendse, 1978;

Yes

No

Yes

Vácha and Soukopová, 2004; Vácha et al., 2008a, 2008b

Nematode

C. elegans

Yes

Vidal-Gadea, et al., 2015

Amphipode

G. antarctica

Yes

Tomanova and Vácha, 2016

Lobster

P. argus

Yes

Lohman et al., 1995;

Yes

Ernst and Lohmann, 2016

Notes. To be presented, the reports must describe the conditions explicitly. Preliminary observations without adequate controls are not included.

Light dependency of the magnetic reception has been considered earlier. But what about its color? The hypothesis that magnetoreception in insects is functional only within a certain spectral window of light can be considered one of the best documented phenomena currently corroborated by data from three independent laboratories. Drosophila is capable of distinguishing between two arms of a T-maze under broad-spectrum light if a magnetic anomaly is present in one of them. This ability is, however, lost when short-wave UV and the blue parts have been filtered out (Gegear et al., 2008; Gegear et al., 2010; Foley et al., 2011). The same laboratory has reported a similar spectral limitation in monarch butterflies tested in a flight simulator (Guerra et al., 2014). Another group (Bazalova et al., 2016) has, in agreement with the earlier findings, found that light, from short wavelengths up to the green/cyan region of the spectrum (about 510 nm), was required for magnetoreception in two species of cockroaches. Other experiments with colors of light show that both the fruit fly and the mealworm beetle change their magnetic compass bearing by 90° in a color-dependent manner (Phillips & Sayeed, 1993; Vácha et al., 2008b, respectively), which can be explained by an interplay of two antagonistic pigments being involved in the RP magnetoreception system (Phillips et al., 2010).

It must be admitted that there are also magnetoreception models based on the light-independent mechanism using FOP that explain the effects of different wavelengths by parallel influences of light-sensitive though magnetically irrelevant events (Jensen, 2010; Kirschvink et al., 2010). Nevertheless, after the addition of recent molecular genetic data, the resulting picture is closer to the RP hypothesis. Magnetoreception in both Drosophila and cockroaches was turned off by gene knockout of Cry and by RNAi silencing (Gegear et al., 2008; Gegear et al., 2010; Foley et al., 2011; Bazalova et al., 2016). Moreover, the magnetoreception of cockroaches spectrally close to FAD absorption was also influenced by a weak radio-frequency field (see later; Vácha et al., 2009). The spectral dependence of insect magnetoreception seems, therefore, to be more indicative of the direct and sole involvement of the light-dependent reception mechanism than secondary events.

As the effects of a strong magnetic pulse point sufficiently selectively to an FOP reception mechanism, the disruptive effect of a weak radio frequency (RF) field is considered best explained by an RP mechanism (Ritz et al., 2004; Maeda et al., 2015). In theory, electron(s) of the RP possibly interact with an external magnetic field in a frequency-dependent manner (Ritz et al., 2009). If an RF is applied in addition to the Earth’s field, it causes resonance effects on electrons interfering with their singlet-triplet interconversion, likely hindering sensitivity to the GMF (Ritz et al., 2009) and possibly modifying final reception pattern (Landler et al., 2015). The effects of RF on magnetoreception in invertebrates has, to date, been studied in only one species of insect (Vácha et al., 2009) and the marine crustacean Gondogeneia antarctica living in shallow waters along the Antarctica coast (Tomanova & Vácha, 2016). The hypothesis of jamming effects of RF fields of very low intensity comparable to data obtained in birds (Ritz et al., 2009; Engels et al., 2014) has been confirmed in both species. The effects of weak anthropogenic RF on animal orientation (Engels et al., 2014) are a serious issue that goes beyond the importance of the search for a compass mechanism.

A look back at the literature on magnetoreception reveals strong motivation to interpret the data from the viewpoint of one or other model of reception (despite the fact that the field offers many no less fascinating problems). The FOP model, particularly for insects, seemed the only type of reception under consideration some 20 years ago (Hsu & Li, 1994; Kirschvink et al., 2001). Recently, we witness a boom of papers advocating the Cry-based RP model of reception.

Types of Magnetosensitive Orientation Behavior

In a number of invertebrate species, the question that raises itself is whether animals such as worms, fruit flies, and cockroaches need a magnetic compass at all, given the short distances they travel. It has to be said that, unlike migrating species such as monarch butterflies or social species such as honeybees and ants, we can only speculate as to the answer. Magnetic compass orientation in the world of distances of centimeters may, however, be as important as in the world of ranges of kilometers (Wyeth, 2010). It is well known that magnetotactic bacteria’s inner FOP moves them along magnetic field lines which are (except on the equator) always inclined so that the bacteria may avoid the oxygen very close above. This is an extremely simple system effective in a liquid environment where the force of gravity is not very reliable. Gravity is, by contrast, available to fruit flies that fly and walk in a dry environment. An immutable, omnipresent force independent of fly’s movement that has the same direction at all times is undoubtedly useful, and doubly so during flight. However, disadvantage of gravity is that it is vertical by definition and can contribute nothing to the search for the forward direction. In contrast, GMF force can be perceived by flies as another guidepost, also pointing in the horizontal plane. It may be incorporated into the set of other directional cues and help them orient.

Compass

A magnetic compass sense uses the angle (azimuth) between the travel path and a straight line to the magnetic north. The azimuth allows the animal to maintain a steady direction of travel. By its very nature, this does not allow for any correction; it does not give the animal any information about its current position in relation to its goal (Mouritsen et al., 2013). It can, however, be traded off, or calibrated, by means of other senses (Gould, 1998). Animals have a number of directional cues from the external environment at their disposal, such as the sun, gravity, polarized light, stars, wind, scent, landscape features, and so on which form a complex in which the magnetic field is only part of the mosaic. It does not seem to play a dominant role in the hierarchy of compass systems. Monarch butterflies use a time-compensated solar compass as dominant and apparently resort to the magnetic compass only on cloudy days. Clock-shifted monarchs fly in the predicted shifted way under clear skies even when the GMF remains unmanipulated (Merlin et al., 2009). Unlike the solar compass, however, the magnetic compass requires no time compensations and can therefore be used to calibrate the solar compass (Guerra & Reppert, 2015). The relationship between the magnetic compass and other compasses was investigated by Ugolini (2001) and Ugolini and Ciofini (2016) in the equatorial sandhopper Talorchestia martensii. The magnetic compass prevailed only when the position of the sun and landscape did not allow easy azimuth determination. Similarly, when testing Atta colombica ants in the wild, Banks and Srygley (2003) and Riveros and Srygley (2008) showed that greater weight was given to the celestial compass than to the magnetic compass. Using the same species, Riveros et al. (2014) investigated the resolution of the conflict between egocentric orientation based on remembered records of movement from proprioreceptors (path integration) and the magnetic direction which they artificially rotated by 90°. Their experiment can be interpreted that the ants choose evenly between the two directions without giving preference to either. When gravity and GMF vector are in conflict, honeybees apparently prefer gravity to determine the vertical during their waggle dance on the comb surface. The reduction of the field to 2% or its rotation had no effect on the success of recruitment (Lambinet et al., 2014).

Map

The map sense allows animals more than just to maintain their direction of travel. It also gives them the capability for true navigation (Able, 1991) with the possibility of correction—that is, for localization of their geographic position in relation to their goal. The magnetic map sense relies on great precision of GMF measurement. Considering planetary gradients, magnetic inclination will only change by 0.9° along a 100 km travel in the north-south direction.

Evidence of true magnetic navigation capability exists in only one invertebrate, the spiny lobster—a migratory marine crustacean living in the Caribbean and along the southeastern US coast. The distance they travel during foraging may be from a few kilometers to hundreds of kilometers. Boles and Lohmann (2003) divided lobsters caught in Florida into two groups and exposed them to two different magnetic fields in a laboratory (Fig. 5). The group exposed to a field corresponding to a position 400 km to the north marched in the south-southwest direction, while the group exposed to a field of a southern location moved in the northerly direction.

Magnetoreception of InvertebratesClick to view larger

Figure 5 Spiny lobsters recognize their geographical position in Florida according to magnetic field parameters. When exposed to two simulated magnetic fields corresponding to places 400 km north and south (red dots) from their capture site (empty dot) in a laboratory, they chose right direction home.

(Based on Boles and Lohmann, 2003)

It is not known whether there are other invertebrate migrants capable of true magnetic navigation. The greatest attention was focused on monarch butterflies because of their incredible navigational skills. Mouritsen et al. (2013) asked whether the butterflies were guided by a compass or a map. In one of their tests they relocated a group of butterflies 2,500 km west from Ontario to Alberta and compared their migratory direction in a flight simulator. The butterflies continued to migrate in the same southwest direction as before the relocation without any compensation, clearly relying on compass orientation only. Until more comparative data on map magnetoreception is available, the spiny lobster will remain the only likely magnetic navigator among the invertebrates.

Alignment

Whereas compass and map magnetic orientation can be used by animals to find travel routes, there is one type of behavior known as magnetic alignment whose importance for animals, both vertebrate and invertebrate, remains an enigma. Alignment or position behavior can be defined as maintaining body axis orientation with respect to the magnetic field (Able, 1996; Begall et al., 2012). The phenomenon whereby resting termites, flies, and honeybees orient their bodies in the direction of the two main magnetic axes was noted by researchers from several independent laboratories at the very beginning of research into the magnetic compass (see Vácha et al., 2010; Painter et al., 2013). This quadrimodal distribution is, however, sometimes also observed in moving individuals; that is, alignment is not only limited to resting animals. Examples include the quadrimodally oriented waggle dances of honeybees on horizontal combs (Martin & Lindauer, 1977) and the recent finding that fruit fly larvae gently placed at the center of an agar plate move in four magnetically perpendicular directions (Painter et al., 2013). This behavior has been verified by several laboratories as truly magnetically oriented, as field weakening led to its disruption (Painter et al., 2013), while the rotation of the horizontal component led to a precisely corresponding shift of the quadrimodal distribution of resting positions in cockroaches (Vácha et al., 2010).

Although magnetic alignment is relatively well and independently documented behavior, we have absolutely no experimental evidence of its adaptive importance. The only exception seems to be meridionally elongated termite mounds built to minimize overheating possibly along the main geomagnetic axis (Jacklyn & Munro, 2002). Being frequently reported also on vertebrates (Begall et al., 2012), alignment is a mysterious and provoking phenomenon of animal magnetic sensitivity.

Behavioral Tests in Invertebrates

In the “hunt for the magnetoreceptor” (Wehner, 1992), the use of invertebrates has huge advantages over vertebrates. When searching for innervated structures responding to the GMF, the possibility of using thousands of small, sometimes translucent animals with a compilable genome and simple behavior observable in a laboratory and, moreover, having only a limited number of neurons is invaluable.

How is it then possible that we still do not know the principle of the receptor? One possible answer may lie in the very first step of investigation—observation of behavior. The basis of every neurophysiological or cellular analysis of reception is a routinely reliable behavioral test. Although assays on invertebrates that investigate their learning or smell are basically standardized, there is as yet no commercially available test of magnetoreception that could, for example, get to the practical lessons of sensory physiology. There are no two laboratories publishing results obtained by the same assay over the long term.

The problem may also be that magnetic orientation ranks relatively low in the hierarchy of the other senses. Magnetic orientation may be disrupted by overlooked cues or sources of interference including anthropogenic RFs, to which animal compasses are surprisingly susceptible (Engels et al., 2014; Tomanova & Vácha, 2016). Because behavioral tests are often conducted under unnatural conditions, the motivation of the animal to move in a certain direction is a potential pitfall. Whereas the migration instinct is spontaneous in migrants like monarch, Drosophila or mealworm beetles need first to be motivated by reward or punishment for preferring a particular magnetic direction. Experiments must therefore consist of two parts: training and testing. Conditioning, however, carries the risk of the animal learning to respond to a cue other than the magnetic field. The test environment may vary slightly from the training environment, or the handling when the animals are taken from training to test conditions may stress them.

Selected invertebrate taxa on which major discoveries have been made will be considered next, and their current status and potential prospects will be discussed.

Fruit Fly Drosophila melanogaster

It is not surprising that there has been increasing interest in magnetoreception in Drosophila over the last decade (Dommer et al., 2008; Gegear et al., 2008, 2010; Foley et al., 2011; Painter et al., 2013). Given the importance of what is perhaps the most popular invertebrate model organism and the importance of the issue investigated, the level of interest in it should perhaps be even greater. The fact that there is evidently no routinely used laboratory assay for adult Drosophila orientation behavior in the GMF speaks volumes about how difficult behavioral research into magnetoreception is. One of the two laboratories where the aforementioned experiments with the fruit fly have been conducted uses an orientation test with Drosophila larvae crawling over agar (trained—Dommer et al., 2008; naïve—Painter et al., 2013). Another group works with adults in a conditional choice chamber test with a magnetic anomaly (similar to that used in honeybees by Walker and Bitterman, 1989, though stronger) applied in one arm of a T-maze (Gegear et al., 2008). Although seemingly weak (only around 57% chose one arm rather than the other), the response of the flies was nevertheless stable. Evidence of the great potential of genetically modifiable lines in conjunction with a functional assay is provided by the fact that it has not only been convincingly demonstrated that Drosophila magnetoreception is linked to the gene for DmCry (D. melanogaster Cry), but also that lost function in mutants can be restored by the human cry gene by genomic rescue techniques (Foley et al., 2011; but see Fedele et al., 2014b). Both laboratories agree that magnetoreception in the fruit fly is dependent on the color of light. Despite these ground-breaking discoveries, there are still a number of outstanding issues to be resolved of which the advantages of gene manipulation in Drosophila could prove essential. To point out only some, it is not known for certain whether Cry is really the GMF direction receptor, just as what signal role Cry plays in reception and with what partners.

It is to be hoped that an assay for Drosophila orientation in a homogeneous GMF suitable for routine use that the magnetoreception community is still waiting for will be found. However, due to the jamming effects of even weak RF fields, it is not possible to simply apply assays tried out in, for example, research on spatial learning and vision where electronic devices generating local interference fields are used.

Monarch

It may not be obvious what fruit flies use a magnetic compass or map for, but the answer is self-evident in the case of monarch butterflies. Every autumn, swarms of millions of monarchs perform spectacular migrations from the northwest of North America to wintering sites in the mountains of central Mexico. On this journey of up to 4,000 kilometers (Reppert et al., 2010), they orient on the basis of an innate orientation program primarily by means of a time-compensated solar compass (Mouritsen & Frost, 2002; Froy et al., 2003). The problem of whether their compass orientation also includes a magnetic component or not has been tackled by two groups. Whereas Mouritsen and Frost (2002) found no effect of the magnetic field in tethered butterflies in a flight simulator and the butterflies were disoriented without the solar compass, Guerra et al. (2014) demonstrated the existence of magnetic orientation. The latter group suggests differences in illumination as a possible reason for this discrepancy.

Guerra et al. (2014) also demonstrated that migrating butterflies use an inclination compass, just like beetles (Vácha et al., 2008a), and that the light falling on the antennae plays a key role in orientation. The use of a flight simulator in the laboratory eliminates a number of problems associated with factors that are difficult to control and that have proved problematic in previous studies (Etheredge et al., 1999; Perez et al., 1999). The advantage of the assay is that animals captured in the autumn do not require special training. If the laboratory behavioral magnetoreception test proves replicable, monarchs may be a key model in research into magnetic navigation in invertebrates with the use of molecular genetic approaches.

Cockroaches

Blattella germanica and Periplaneta americana are classic model species in which a relatively weak but consistent increase in locomotor activity was observed if the GMF was periodically rotated (Vácha, 2006). This assay combined with genetic techniques demonstrated that Cry was the molecule that mediated response to a mere shift in the direction of the horizontal magnetic axis, which is a key property of the compass function (Bazalova et al., 2016). Although this type of behavioral response does not give the answer to the question of what is the adaptive advantage of reception, it can potentially be used in a wide variety of organisms (Liang et al., 2016) and questions on GMF reception, thanks to its simplicity and almost zero handling of animals. The hindering factor, as in other magnetoreception assays in invertebrates, is the as-yet-unfulfilled condition of its independent verification by some other laboratory.

Honeybee

Leaving aside pioneering insect tests in the 1960s and 1970s, which have been dealt with elsewhere, the honeybee was the first invertebrate in which magnetoreception was described by several laboratories and in several types of behavior (reviewed in Able, 1996; Válková & Vácha, 2012). It is also one of the few species in which the magnetoreception assay has been successfully replicated independently (Walker & Bitterman, 1989; replicated by Kirschvink & Kobayashi-Kirschvink, 1991, and very recently by Lambinet et al., 2017). Bees had to learn to discriminate between two feeders differing only by the presence of a magnetic anomaly. They proved able to detect local GMF distortions extremely sensitively (Kirschvink et al., 1997). However, while the discrimination test on bees dominated in the 1980s and 1990s as one of the most fruitful approaches, no such test, either positive or negative, has been published in recent decades. And yet, the questions are far from having been answered. Quite the opposite. Although from the aforementioned list of evidence in favor of one or the other reception mechanism, only reception in complete darkness is fully documented in bees (Table 1), the FOP model in bees is given greater weight (Hsu & Li, 1994) than is warranted by the experiments. Nevertheless, everything remains open (reviewed in Valkova & Vácha, 2012). Evidence for the use of FOP magnetoreceptors) is indirect (reviewed in Shaw et al., 2015) or is explicitly referred to in original papers as only preliminary (pulse experiments: Kirschvink and Kobayashi Kirschvink, 1991; glued magnetic wires: Walker & Bitterman, 1989) and badly needs independent replication, elaboration, and follow-ups. The bee has huge potential in research into a possible link between magnetoreception and visual perception. But also a replication of pulse experiments, the application of RF fields and magnetic map experiments could help move this species back to the forefront and help in understanding the neural processing of magnetic information.

Ants

Ants, other social insects, have been a much studied group in recent years, undoubtedly due to their long journeys for food and back to the nest. Wajnberg et al. (2010) summarize the results of a number of experiments showing that ants use a magnetic compass sense. For example, under laboratory conditions, ants trained to visit a feeder located to the north change the direction of their search for food in the test correspondingly when the field has been rotated (Camlitepe et al., 2005). Buehlmann et al. (2012) suggest that ants travelling between the nest and the feeder will learn to use a magnetic anomaly surrounding a permanent magnet as a landmark. Sandoval et al. (2012) monitored spontaneous movement of untrained ants of the Solenopsis sp. from the center of a circular arena and found a roughly axial orientation along the north-south axis which shifts correspondingly after the field has been rotated by 90°. Spontaneous movement of naive individuals along the north-south axis is reminiscent of alignment. It might be a case of the simplest orientation using the magnetic field, when the magnetic axis is the only or the strongest directional cue for an animal which is not motivated to prefer a particular azimuth.

As in the case of bees, evidence of magnetic orientation in ants over the last two decades has been linked to findings of iron oxides in their tissues (reviewed in Wajnberg et al., 2010). Hymenoptera, therefore, seem to be the insect group in which the discovery of the sought-after link between magnetosensitive behavior and FOP could be expected first.

Sea Crustaceans

The use of the GMF for orientation is surprisingly well documented in crustaceans. The geomagnetic vector gives a map sense to the decapod spiny lobster Panulirus (Boles & Lohmann, 2003) as well as the vital seashore direction (Y-axis) to amphipods living in a changeable coastline habitat. Supratidal sandhoppers (Crustacea, Amphipoda, Talitridae) live on the wet sand of sandy beaches among the remains of seaweed thrown ashore and washed by the waves. They migrate between the sea and the burrowing zone, switching among searching the food and protection from predators, from being swept away by the waves, and from direct sunlight and drying out. To find the Y-axis direction, they use a whole range of orienting cues (reviewed in Scapini, 2006), including magnetic cues (Ugolini, 2001; Ugolini, 2002; Ugolini et al., 2003; Rothsey, 2006; terHorst, 2012; Ugolini, 2016). In littoral crustaceans living in shallow water in the subtidal zone, Tomanova and Vácha (2016) demonstrated seaward magnetic orientation along the Y-axis in G. antarctica.

Caenorhabditis elegans

A unique phenomenon of vertical magnetic compass has recently been described in the nematode Caenorhabditis elegans (Vidal-Gadea et al., 2015). In a nutrient-rich substrate, well-fed worms migrated up, while starved worms migrated down. The reason for and advantages of this migration remain unclear. What is even more remarkable is that they did not primarily use gravity but the magnetic vector direction for maintaining the vertical axis. When geographically distinct populations had to move along a horizontal surface, they preferred a magnetic azimuth corresponding to the deflection of the vertical from the magnetic vector in their home location. The perplexing question—how the nematodes can maintain any direct direction in the medium by simply following the azimuth—remains unanswered. Such a task is achievable if the movement takes place along the Earth’s surface, but in a three-dimensional space it would probably lead to a spiral. There obviously must be some other accompanying sense in play. For extensive behavioral screens, the authors developed a test in which naive individuals moved along a horizontal tray toward a permanent magnet. Such a kind of behavior in a strong and extremely inhomogeneous field is puzzling and not easy to reconcile with, for example, Njus et al. (2015) or even contradictory to Landler et al. (2016).

Antenna, Eye, or Abdomen?

The magnetic field penetrates all tissues, and a considerable hindrance in the search for a magnetic receptor is that—unlike all the other senses monitoring the outside world—the receptor may be anywhere in the body. In insects, the search for an organ of reception naturally centers on their antennae, multisensory organs adapted to receive stimuli of a physical and chemical nature; the eye, whose structure makes it ideal for the RP mechanism; and the abdomen.

Antennae

Invasive and noninvasive experiments conducted so far in which the assumed magnetoreception functions of antennae were disabled give a contradictory picture. Although ablation of the antennae of the cockroach P. americana had no significant effect on its magnetically induced restlessness (Vácha et al., 2008c), painting the antennae of monarchs black (Guerra et al., 2014) resulted in a loss of orientation in a migration simulator. The authors argue that the antennae are necessary for the correct direction of migration for a number of reasons. First, they are the seat of a variety of sensory inputs and, second, they are essential for a time-compensated sun compass. Because the sun constantly changes its position in the sky, determining the azimuth from the sun (unlike the magnetic azimuth) must at all times be compensated for the passage of time by means of an internal clock whose proper function—and proper orientation—is assured by its synchronization (entrainment) to the light-dark cycle mediated by a Cry molecule present, inter alia, in the antennae. However, Cry is also a prime candidate for a chemical magnetoreceptor. Having had their antennae painted black, time-desynchronized individuals, moreover, probably deprived of the magnetic compass as well moved in circles in the flight simulator (Guerra et al., 2012, 2014). The antennae of monarchs might therefore be a possible component of their light-dependent magnetoreceptor. Indeed, very recently Bae et al. (2016), using genetic rescuing methods, show that Cry gene expression in Johnston’s organ in the second antennal segment is indispensable for magnetic sensitivity in Drosophila.

Insects’ antennae are also promising in terms of FOP reception (reviewed in Wajnberg et al., 2010; Shaw et al., 2015). SPM particles in the antennae have been found in bees (Lucano et al., 2006) and ants (Wajnberg et al., 2004; Abracado et al., 2008; Wajnberg et al., 2010; Alves et al. 2014).

Eye

The same simple method of restricting access to light used on the antennae, that is, covering them with black paint, was used by Bazalova et al. (2016) on the eyes of the cockroach B. germanica. Magnetic sensitivity was disrupted by dark paint, but preserved if translucent paint was used. Because Cry was found in the retina of fruit flies (Mazzotta et al., 2013), between the retina and the lamina in cockroaches (Bazalova et al., 2016) as well as deeper in eye stalks (Fleissner et al., 2001), the eye is another potential site of light-dependent reception in insects. Although electrophysiological measurements of the visual pathway of insects could provide long-awaited direct evidence of a compass in the eye, we have no recent or conclusive evidence except for preliminary intracellular recordings from the retinal cells of the blowfly (Phillips, 1987; Phillips et al., 2010).

The eye has been the key organ in the search for a magnetoreceptor since the formulation of the RP hypothesis—irrespective of whether it is a compound or a camera eye. They both meet several fundamental conditions: They are richly innervated structures easily accessible to light, furthermore containing Cry. Like the crustacean statocyst (Hertwig et al., 1991) signaling the gravity axis, the retina is also a hemispherical or a cup-like structure that allows immediate detection of the direction of respective field lines. If the reception epithelium was flat, the animal would have to perform scanning movements to search for the magnetic axis direction, which, however, has not been reported under normal field intensities (but see Ugolini, 2006). This condition obviously is also applicable to the FOP model, possibly giving a guide in the search for the optimal reception structure whose architecture may correspond to that of the eye or the statocyst. The eye, therefore, seems a suitable reception structure, and the question of whether magnetic and visual patterns overlap and what this would mean for vision may be considered (Phillips et al., 2010).

There is no direct evidence so far to help answer the intriguing question of whether animals can actually see the magnetic field. The question itself may be fallacious because, especially in invertebrates, it is impossible to empathize with, for example, honeybees or fruit fly larvae and comprehend how they perceive and differentiate between streams of information from different receptors. Literature on magnetoreception nevertheless offers some models of what magnetically evoked images could possibly be formed in the visual field of the eye (Solov’yov et al., 2010) and speculates whether, superimposed on visual images, they could be used for spatial orientation and distance measurement (Phillips et al., 2010; Cerveny et al., 2011). Of course, we have no idea whether this competition in the visual system occurs at all. It has, on the other hand, been found that part of the visual information, even if transmitted by the optic nerves, may be processed separately from image analysis. This is known in parallel processing of “what” and “where” information of moving objects, which has been described in vertebrate and even in insect vision (Strausfeld & Lee, 1991).

In compound eyes, the situation is further complicated by the fact that (1) perhaps only some of the retinula cells of individual ommatidia are magneto-sensitive (Phillips et al., 2010); (2) just as information on the polarized light plane is preferentially perceived by an island of ommatidia inside the dorsal rim of the insect eye (Homberg, 2004), only some of the ommatidia may be specialized in magnetoreception; and (3) the organ of reception may even lie beneath the retina in the region of the lamina still accessible to light (Bazalova et al., 2016). In all the aforementioned cases, magnetosensitive outputs may travel separately from visual outputs. These tracks may then be processed in centers other than the visual cortex, though these centers have not, as yet, been found in invertebrates.

In the future, it may be useful to try to take advantage of genetic and optogenetic methods for analyzing activity in the visual pathway, including mediators and communication with glial cells under the influence of a magnetic field.

Insect Abdomen

Thanks to the finding of iron oxides clusters, the insect abdomen has so far been mentioned as a possible seat of magnetoreception in the context of the FOP hypothesis. Most of the existing data comes from honeybees. In the previously described discriminatory test (Walker & Bitterman, 1989), small pieces of magnetic and nonmagnetic wire were attached to the honeybee abdomen and chest. Magnetic wires attached in the region of the anteriodorsal abdomen, which has been reported as the major area of FOP concentration (Gould et al., 1978), interfered most seriously with the successful completion of the feeder discrimination test in the bees. The tests were, however, considered explicitly as merely preliminary information. Very recently, Liang et al. (2016) showed that cutting the ventral nerve cord between the abdomen and the thorax cancels conditioned proboscis response (PER) to magnetic stimuli. Because the olfactory conditioning persisted, the abdomen turns out to be crucial for magnetic sensing in bees. In line with previous findings, Lambinet et al. (2017) indicated the presence of ferromagnetic material in the honeybee abdomen unlike head or thorax. Importantly, after permanent magnet treatment, magnetization was altered as well as magnetic reception disappeared. Should the behavioral effect be persisting (not only a result of temporary overactivation of receptor) it would support FOP mode of reception strongly.

Iron granules have also been located in sheets of trophocyte cells in the subcuticular fat layer of the ventral abdomen (Hsu & Li, 1994). The same authors claimed that a magnetic field induces magnetic granules to shrink, resulting in a cytoskeletally triggered release of calcium which may affect neural activity (Hsu et al., 2007). The first of these studies attracted broad criticism (see Shaw et al., 2015), and verification of the second study—just as verification of all the experiments presented in this chapter devoted primarily to insects—is still lacking, leaving the connection between the FOP in trophocytes and the behavioral performance unresolved (Shaw et al., 2015).

Mollusks and Worms: Electrophysiology and Neuroanatomy

A recording of altered electrical activity of the primary sensory cell in response to the application of the GMF may rightly be considered the strongest proof of its magnetoreception. To date, however, this kind of receptor evidence remains to be done. The complications that need to be overcome in classical electrophysiological measurements are not insignificant and are due to, for example, the slight currents induced as artifacts in living tissues and sensitive instruments when magnetic stimulus is applied (Liedvogel & Mouritsen, 2010). It is important to ensure that the instruments are neither magnetic nor generating spurious signals interfering with reception mechanisms and so on. All these pitfalls are probably the reason why a direct recording of activity from a magnetosensitive cell or a channel in its membrane is still awaited.

The classic advantage of invertebrates, specifically in research into sensory physiology, is the simplicity of their nervous system and their robustness in invasive measurements or lesions (Lohman et al., 1991). However, although electrophysiological studies of insects have been an intensely developed discipline for decades, direct recordings of neural responses to the MGF are rather exceptional (Korall & Martin, 1987; Phillips, 1987) and do not provide clear evidence of a receptor. However, the small and translucent bodies of invertebrates will probably also be a key advantage in the future, replacing classical electrode electrophysiology with optogenetic methods (Gong et al., 2015).

A series of tests on the marine mollusk Tritonia diomedea was conducted between 1987 and 2006. This marine nudibranch mollusk having about 7,000 neurons in six fused ganglia played an important role in research on memory (Cain et al., 2005). In a Y-maze test, it also demonstrated a body alignment in response to the rotation of GMF (Lohman & Wilows, 1987). Follow-up in-cell electrophysiology showed an altered frequency of action potentials (APs) in six neurons in the brain after periodic GMF rotation. The long latency (1–15 min) after the application of rotation was notable (Lohmann et al., 1991; Popescu & Willows, 1999; Wang et al., 2003), indicating that they are locomotion-controlling efferent motor neurons (Cain et al., 2005) rather than primary receptor neurons. Pavlova et al. returned to this model in 2011. Their confirmation of Tritonia sensitivity to 60° field rotation was an independent confirmation of GMF reception in the mollusk, though they were not successful in identifying the receptor. It is apparently not located in any particular organ, but widely dispersed in peripheral body tissues.

A decade later, the aforementioned study on the nematode Caenorhabditis elegans by Vidal-Gadea et al. (2015) got closer than any other to date to a definition of primary neurons supposedly responsive to magnetic stimulation even if synaptically isolated from other neurons. It showed the great potential of mass application of transgenic lines in neurophysiology. Using behavioral screening, the authors identified genes expressed in neurons responsible for magnetotaxis. As a noninvasive indicator of neural activity, the authors used calcium imaging—microscopic fluorescence detection of intracellular calcium. An immediate increase in fluorescence was recorded at rotations of a permanent magnet in the vicinity of the restrained animal. No increase in fluorescence was found in control neurons or neurons with respective mutations. To show that the neurons really are the primary receptors, worms with genetically impaired synaptic transmission were used. Though the work shows clearly the power of research techniques based on transgene invertebrate, quite recently, Landler et al. (2016) failed to replicate key behavioral findings of the study.

The problem of receptor localization is connected with another—and no less important—problem of where and how magnetic information is processed in the brain. Tracing the receptor pathway down to, for example, the mushroom bodies in the insect brain may give an insight into how animals handle, filter, and integrate the information with other senses and the memory, and how, finally, it controls motor responses (Cain et al., 2005). Strangely enough, modern evidence of this kind in invertebrates is lacking. In vertebrates, however, enhanced activity of specific brain areas possibly processing the magnetic information has already been localized via detection of early genes expression signaling neural activation ( Nemec et al., 2001; Wu & Dickman, 2012; Lefeldt et al., 2014).

Unnatural Fields and Nonorientation Sensitivity

In the beginning, we confined our definition of magnetoreception to weak, static GMF-type fields only. The reason is obvious: Other fields are unnatural, of anthropogenic origin, and animals could not have developed specific receptors for them. There is, however, abundant literature on the effects of artificial fields that are particularly important for human health (the 50/60 Hz field around appliances and various fields 100 or more times exceeding GMF intensity, RF fields, etc.). These fields may interfere with GMF detectors, although they did not primarily evolve for them, and therefore cannot be omitted completely.

Bees’ sensitivity to 10 Hz and 60 Hz AC fields was investigated by Kirschvink et al. (1992, 1997), who used the well-proven conditional paradigm (Walker & Bitterman, 1989) and found negative correlation between frequency and sensitivity. 60 Hz magnetic field also reduced opioid-induced analgesia in the snail Cepaea in the presence of light only (Prato et al., 1996).

The importance of GMF in the animals’ life can manifest itself in experiments, rare to date, in which the GMF is maximally suppressed (near-zero field [NZF]). Wan et al. (2014) raised two species of planthoppers in a field attenuated to about 1% and found, inter alia, a lower weight in adults and reduced fertility in females reared from eggs in the NZF. Recently, the same group described changed behavioral display of planthoppers like flight capacity and positive phototaxis under NZF (Wan et al., 2016). A remarkable finding has been reported by Zhang et al. (2004). They reared D. melanogaster for 19 successive generations in an NZF and monitored the ability of visual operant conditioning. In the flight simulator, the flies learned to avoid a target associated with a heat shock. The authors reported impairment in learning and memory, accumulated from generation to generation and finally resulting in complete amnesia in the tenth generation in NZF. The experiment should inspire replications lacking to date, particularly because memory testing of Drosophila is a widespread and standardized procedure.

Research into chemical magnetoreception is remarkably interconnected with investigation of the molecular mechanisms governing circadian rhythms in the Cry molecule. In the Danaus clockwork feedback loop, Cry even plays two roles: Drosophila-like type 1 Cry might serve as a photoreceptor synchronizing inner clock rhythms with day and night cycle and vertebrate-like type 2 Cry as a part of transcription regulating complex (reviewed in Kyriacou, 2009). Thus, an intriguing question presents itself: Is there a link between the Cry role in magnetoreception and the circadian clock control? If the clock is sensitive to the magnetic field, is it a phenomenon that has a practical use in the life of animals, or is it only a man-made artificial phenomenon similar to the influence of anthropogenic RF fields? If there is a natural link, could minute daily GMF fluctuations play the role of a synchronizer? Or does it play an as-yet-unknown role in coordinating the temporal and spatial orientation of animals? Two independent studies have already shown that a magnetic field actually does change the period of the internal clock in the Drosophila wildtype, while no such effect was observed in the Cry knockout lines (Yoshii et al., 2009; Fedele et al., 2014a), which opens the door to a potentially extremely interesting field that might be called magnetochronobiology.

Cryptochrome seems to lie at the intersection of magnetoreception and other types of not classical compass behavior, that is, the negative geotaxis in Drosophila (Fedele et al., 2014b). Fruit flies instinctively climb up against gravity. It is quite remarkable that geotaxis is dependent on Cry and the presence of blue light. The finding that this behavior was significantly suppressed when an MGF was applied is equally interesting. Recently Bae et al. (2016) describe switch into even positive geotaxis when MGF of about twofold intensity of the Earth was used. Both teams use mutant strains to show, inter alia, that Cry really is the magnetoreception mediator and to locate the cells responsible for mediating magnetoreception. MGF-dependent geotaxis resembles the digging down into food response of nematodes mentioned earlier, and altogether the papers open an interesting topic of MGF as a cue for vertical movements during the navigation in nature.

A potential of Cryptochrome molecule to provide cellular signal pathways with sensitivity to MGFs inspires more and more studies based on a versatile Drosophila model. Among other Cry-dependent phenotypes investigated, Wu et al. (2016) report enhanced courtship activity of fruit fly males or Marley et al. (2014) show larger seizure response of fruit fly larvae in both cases after exposure to MGFs of several orders stronger than GMF. Quite recently, the hot problem of Cry role in magnetosensitive signaling was tackled by the same group (Giachello et al. 2016) on Drosophila neurons. Exploiting electrophysiological and genetic techniques like ectopic expression by means of GAL4/UAS system they showed that Cry-dependent depolarization under light flashes was potentiated by strong MGF (0.1T) even in neurons naturaly expressing no Cry. The role of Cry different from magnetoreceptive one seems not likely then (Giachello et al. 2016). To what extent findings mentioned in this column reflect natural sensitivity exploited by animals in a wild or, contrastingly, artificial and unspecific impacts of man-made fields on signaling pathways often involving Cry, is hard to judge now. In every respect the field concerned shows inspiring potential for control of cell signalization and biomedical concerns. Here, invertebrates with a modifiable genome have proved an extremely suitable model subject and will probably do so as well in the future.

Conclusion and Prospects

The search for the molecular principle of the signaling mechanism from the receptor molecule or structure to the activated neural cell remains the cardinal question of current magnetoreception research.

But even when this question has been answered satisfactorily, there will still be room for investigating problems which, from a biological standpoint, may be equally fascinating. For instance, we can still only speculate what adaptive advantage the magnetic sense may give to such an important species like the fruit fly. A similarly little explored area is the cooperation between the magnetic input and other sensory inputs. Their interplay and processing in the brain, likely out of human experience, may inspire new insights.

Just as the entire group of invertebrates is extremely heterogeneous, any attempt to provide an overall picture of their magnetoreception is also heterogeneous. A consistent description cannot, however, be obtained as yet, even within the framework of related taxa. The heterogeneity concerns, unfortunately, also the research itself and agreement between two laboratories, even in one and the same species are more the exception than the rule. The reason may be that no two laboratories use the same testing procedure. Testing difficulties may discourage attempts to reproduce results already published, though reproducibility remains the gold standard, and only conclusions verified by independent teams should be considered truly sound. Laboratories should not be discouraged by a seeming lack of originality if they “only” replicate a magnetoreception test. Such replication studies already appear in research into magnetoreception in vertebrates (Hein et al., 2011; Kishkinev et al., 2012), and given the current existence of large amounts of yet unverified data, their results can be considered to be as valuable as original studies (Shaw et al., 2015). As magnetoreception is inherently multidisciplinary research, it would always be extremely appropriate to ensure cooperation with experts from the respective fields of physics, chemistry, and biology. Fortunately, the principles of blinding the experimental protocol using a random sequence of treatments and the least possible interference from the experimenter (Kirschvink et al., 2010) are also becoming the norm.

Invertebrates have always played an essential role in advancing our understanding of the primary molecular mechanisms of the sensory neurophysiology. The mysterious ability to sense the Earth’s magnetic field will probably be no exception. Exploiting the potential of genetically modified lines, automated behavioral tests on hundreds of individuals as well as advanced optogenetic techniques monitoring neural activity will, however, not be possible as long as there are no standardized, validated, and widely applicable assays of magnetoreception under natural conditions. Until several laboratories could share and elaborate identical results of such an assay, research into magnetoreception in invertebrates will remain a mosaic of individual concepts and a challenge missed.

Acknowledgments

Author acknowledges Czech Grant Agency for its support (GACR 13-11908J).

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