44

International Journal of Radiation Biology, January 2013; 89(1): 44–50

© 2013 Informa UK, Ltd.

ISSN 0955-3002 print / ISSN 1362-3095 online

DOI: 10.3109/09553002.2012.715786

Correspondence: Dajana Todorovic, MSc, Institute for Biological Research, University of Belgrade, Department of Insect Physiology and Biochemistry,

Laboratory for Magnetobiology and Behaviour, Despota Stefana Blvd. 142, 11060 Belgrade, Serbia. Tel: � 381 11 2078 300. Fax: � 381 11 2761 433.

E-mail: dajana@ibiss.bg.ac.rs

(Received 18 October 2011 ; revised 14 June 2012; accepted 8 July 2012 )

The infl uence of static magnetic fi eld (50 mT) on development and motor behaviour of Tenebrio (Insecta, Coleoptera)

Dajana Todorovic 1 , Tamara Markovic 1 , Zlatko Prolic 1 , Spomenko Mihajlovic 2 , Sne ž ana Rau š 1 , Ljiljana Nikolic 1 & Branka Janac 1

1 Institute for Biological Research, University of Belgrade, Serbia, and 2 Republic Geodetic Authority ,

Sector for Geodetic Works , Department of Geomagnetism and Aeronomy , Serbia

Introduction

Living organisms are highly complex dynamic systems that

have been evolving for over 2 million years in the presence of

a natural geomagnetic fi eld. Considering of the latest increase

of the electromagnetic pollution, as a consequence of inten-

sive industrialization, additional static and alternating mag-

netic fi elds are common in the living environment. Th us, the

infl uence of static magnetic fi elds on biological systems has

been a topic of considerable interest for many years (Hong

1995, Rosen 2003). At the current state of knowledge, the bio-

logical eff ects of static magnetic fi elds have yet to be unequivo-

cally interpreted. Th e increasing amount of data reporting the

bioeff ects of static magnetic fi elds provides a path to under-

stand the mode of their action on living organisms.

Like many organisms, insects have the ability to detect

and respond to magnetic fi elds of diff erent characteris-

tics. Reports in the literature concerning the infl uence of

static magnetic fi eld on insects ’ development (Ramirez

et al. 1983, Ho et al. 1992, Prolic and Nenadovic 1994, 1995,

Prolic et al. 2001, Pan and Liu 2004, Savic et al. 2011), viability

(Rau š et al. 2009), genetic material (Prolic and And–elkovic

1992, Takashima et al. 2004), and the metabolic pathways

(Kefuss et al. 1999) are available. Finally, natural magnetic

fi eld alteration induced by the presence of diff erent static

magnets could have an impact on the daily activities, spatial

orientation and behaviour of insects (Klotz and Jander 2003,

V á cha 2006, 2007, V á cha et al. 2008).

Reaction and adaptation to the changes in the environ-

ment are distinctive to each living organism. In insects, the

neuro-endocrine system releases neurohormones that are

involved in the regulation of various life processes, includ-

ing development and behaviour, as well as in the response

of organisms on the external ecological factors such as mag-

netic fi elds (Osborne 1996, Henrich et al. 1999). Until now,

results related to the eff ects of magnetic fi elds on the neuro-

endocrine system of insects are sparse (Peric-Mataruga et al.

2006, 2008, Ilijin et al. 2011).

In view of these facts, the aim of this work was to investi-

gate the eff ects of static magnetic fi eld (50 mT) on duration

of pupa-adult development and motor behaviour of adults

in two Tenebrio species. Th e pupae of Tenebrio obscurus and

T. molitor were placed closer to the North (N) pole, or closer

to the South (S) pole of magnetic dipole until the moment

of adult eclosion. Th ese results contribute to a better

understanding of the species-specifi c responses in variable

environmental conditions.

Abstract

Purpose : There is considerable concern about potential eff ects

associated with exposure to magnetic fi elds on organisms.

Therefore, duration of pupa-adult development and motor

behaviour of adults were analyzed in Tenebrio obscursus and

T. molitor after exposure to static magnetic fi eld (50 mT).

Material and methods : The experimental groups were: Control

(kept 5 m from the magnets), groups which pupae and adults

were placed closer to the North pole, or closer to the South pole

of magnetic dipole. The pupae were exposed to the magnetic

fi eld until the moment of adult eclosion. The pupa-adult

development dynamics were recorded daily. Subsequently,

behaviour (distance travelled, average speed and immobility) of

adults exposed to the magnetic fi eld was monitored in a circular

open fi eld arena.

Results : Static magnetic field did not affect pupa-adult

developmental dynamic of examined Tenebrio species. Exposure

to magnetic fi eld did not signifi cantly change motor behaviour

of T. obscurus adults. The changes in the motor behaviour of

T. molitor induced by static magnetic fi eld were opposite in

two experimental groups developed closer to the North pole or

closer to the South pole of magnetic dipole.

Conclusion : Static magnetic fi eld (50 mT) did not aff ect on pupa-

adult development dynamic of two examined Tenebrio species,

but modulated their motor behaviour.

Keywords: static magnetic fi eld , behaviour , development ,

T. obscurus , T. molitor

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

Eff ects of static magnetic fi eld in Tenebrio 45

Material and methods

Insects Mealworm beetles, T. obscurus and T. molitor (Insecta,

Coleoptera), are holometabolous insects whose life cycle

goes through the egg, larva, pupae, and adult stadium. In our

experiment, we used the pupae from the population bred in

the Institute for Biological Research ‘ Sini š a Stankovic ’ . Th ey

were reared in the standard conditions on a dry medium

of wheat bran ( ‘ Kikindski mlin ’ , Kikinda, Serbia) with about

0.5% dry yeast ( ‘ Centroproizvod ’ , Belgrade, Serbia), in con-

tainers (Volume � 1000 ml), at a temperature of 23 ° C � 1 ° C,

relative humidity 65% � 10%, the light intensity of 100 lux,

and a 12 h:12 h light/dark cycle.

The pupae are immobile and do not take food during

this period (lasting 2 – 3 weeks). Pupa is a very suitable

model system because of a short development and great

susceptibility to external influences. Also, this stage fea-

tures dynamic changes in metabolic reactions and the

histolysis-histogenesis processes.

Magnetic fi eld As a source of static magnetic fi eld, a cylindrical magnet

(37 mm height and 45 mm diameter) was used. Magnetic fi eld

was measured by a gaussmeter (Hirst GM05 Gaussmeter,

with the probe PT 2837; Hirst Magnetic Instruments Ltd,

Tesla House, Tregoniggie, Cornwall, UK).

During the experiment, average values of the local

geomagnetic field (44 ° 38 ′ N; 20 ° 46 ′ E), measured by

Geomagnetic systems magnetometers – GSM-19 v6.0

proton magnetometer (Gem Systems Inc, Ontario, Canada)

were in the range of 41840 – 41874 nT for the vertical

component, and 22621 – 22718 nT for the horizontal compo-

nent (Department for the Geomagnetism and Aeronomy,

Republic Geodetic Authority, Republic of Serbia).

Experimental procedure Th e process of pupation was carefully observed and 0 – 24 h

old pupae ( T. obscurus and T. molitor ) were randomly

divided into three groups.

Th e control group (N T. obscurus � 8; N T. molitor � 12) consisted

of pupae that completed their life span outside of the reach

of the magnetic fi eld, (5 m distance from the magnet). Th e

pupae that were exposed to static magnetic fi eld (50 mT)

until to the moment of adult eclosion formed the other two

groups. One group was placed closer to the N pole – N group

(N T. obscurus � 6; N T. molitor � 11), while the other one was placed

closer to the S pole – S group (N T. obscurus � 8; N T. molitor � 11) of

magnetic dipole.

Pupae (head towards the magnetic pole) were lined up

in the cell plate dish in the way that they were exposed to

the relative homogeneous static magnetic fi eld (B � 50 mT),

measured in the line of pupae head at a distance of 2 mm

from the magnetic pole (Figure 1).

Th e longitudinal axis of the pupae coincided with the

main axis of the magnet. Th e pupa-adult development

dynamics were daily recorded at 10:00 h. After adult eclo-

sion, every single insect was put into a dish containing

food and then returned to the N or S magnetic pole for an

additional period of 24 h. Afterwards, the adult was placed

Figure 1. Static magnetic fi eld exposure system: side view (A) and view from above (B). 1 – cell plate dish, 2 – cylindrical magnet, 3 – magnetic fi eld lines. Pupae (head towards the magnetic pole) were placed only in grey marked cells (a – f ) were magnetic fi eld was relative homogenous (50 � 0.5 mT). Average vertical (C) and horizontal (Dl) magnetic fi eld variations in the cells where Tenebrio pupae were placed.

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

46 D. Todorovi ć et al .

into the Petri dish (Radius � 14 cm) where its behaviour

was recorded for 15 min ( ‘ open fi eld ’ test).

Motor behaviour Th e behaviour of T. obscurus and T. molitor adults was

registered by a ‘ Logitech ’ web-camera (Logitech Inc.,

Fremont, CA, USA) placed at the distance of approx. 30 cm

above the Petri dish and connected to a computer. Any-maze

software (v.4.73, Stoelting Co., Wood Dale, IL, USA) was used

to analyze of animals behaviour. In this experiment three

parameters of insect behaviour were analyzed: Distance

travelled (m), average speed (m/s), and immobility (s). Th e

animal had to remain immobile for at least 5 sec for it to be

considered as immobility. Th e distance travelled and average

speed are a measure of locomotor activity or movement.

Th e whole experimental procedure was carried out in a

room with controlled conditions: temperature (23 � 1 ° C),

humidity (70 � 10%), and light intensity (600 lux).

Data processing Th e results of development dynamics are presented in the

Tables, whereas the results of motor behaviour are presented

by graphs, as mean � standard error of mean (SEM). Prior to

the statistical analysis, the distribution of the data was tested

by Kolmogorov-Smirnov test. Since the data did not show

normal distribution, Kruskal-Wallis analysis of variance fol-

lowed by post hoc Mann-Whitney U test was used to evaluate

the diff erences between the two species of Tenebrio in both

development and behaviour, as well as the eff ect of the static

magnetic fi eld.

In all cases, P � 0.05, P � 0.01 and P � 0.001 were

considered as signifi cant, highly signifi cant and very highly

signifi cant diff erences, respectively.

Results

Pupa-adult development and spontaneous motor behaviour of T. obscurus and T. molitor Th e average duration of T. obscurus and T. molitor pupa

stadium is shown in Table I. Signifi cant diff erence has not

been found in pupa-adult development dynamics between

the examined species of Tenebrio (Mann-Whitney U test:

U � 44, N T. obscurus � 8, N T. molitor � 14, P � 0.41).

Regarding spontaneous motor behaviour, T. obscurus

adults had signifi cantly higher locomotor activity, presented

as distance travelled and average speed (Mann-Whitney U

test: U � 0.00, N T. obscurus � 8, N T. molitor � 12, P � 0.0002), and

consequently less immobility time ( U � 10, N T. obscurus � 8,

N T. molitor � 12, P � 0.003) compared to T. molitor ones

(Figure 2).

The eff ect of static magnetic fi eld ( 50 mT ) on pupa-adult development of T. obscurus and T. molitor In T. obscurus (Kruskal-Wallis test: H 2 , 27 � 0.01, P � 0.99)

and T. molitor ( H 2 , 51 � 1.25, P � 0.53), there were no signifi -

cant diff erences in duration of pupa-adult development of

N and S groups compared to control group, as well as between

the N and S groups (Table II).

The eff ect of static magnetic fi eld ( 50 mT ) on motor behaviour of T. obscurus and T. molitor Exposure to static magnetic fi eld decreased locomotor

activity of T. obscurus adults, particularly those which pupa-

adult development was completed closer to the S magnetic

pole (Figure 3). However, these diff erences were not signifi -

cant compared to control group, as well as between the N and

S groups for all examined behaviour parameters (Kruskal-

Wallis test): distance travelled ( H 2 , 22 � 2.63, P � 0.27), aver-

age speed ( H 2 , 22 � 3.18, P � 0.20), and immobility time

( H 2 , 22 � 1.60, P � 0.45).

In T. molitor adults, it was found that exposure to static

magnetic fi eld has possibility to modulate distance trav-

elled ( H 2 , 34 � 15.55, P � 0.001), average speed ( H 2 , 34 � 14.44,

P � 0.001), and immobility time ( H 2 , 34 � 10.98, P � 0.004),

whereby this eff ect was diff erent in N and S groups

(Figure 4).

In the N group, signifi cantly increased distance travelled

( U � 27, N N group � 11, N Control � 12, P � 0.02) and average

speed ( U � 27.5, N N group � 11, N Control � 12, P � 0.02), as

well as consequently decreased immobility time ( U � 28,

N N group � 11, N Control � 12, P � 0.02) of T. molitor adults

compared to control group were observed. On the other

hand, in S group, decreased locomotor activity was observed,

but this eff ect was signifi cant only for distance travelled

Table I. Duration (days) of T. obscurus and T. molitor pupa-adult development.

T. obscurus 10.38 � 0.26 ( n � 8) T. molitor 10.57 � 0.36 ( n � 14)

Results are presented as mean � SEM.

Figure 2. Spontaneous behaviour of T. obscurus ( n � 8) and T. molitor ( n � 12) adults. Results are presented as mean � SEM. ∗ ∗ P � 0.01 and ∗ ∗ ∗ P � 0.001 (Kruskal-Wallis ANOVA followed by Mann-Whitney U test).

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

Eff ects of static magnetic fi eld in Tenebrio 47

1999). Their synthesis is regulated by neurohormones of

the protocrebral neurosecretory neurones (Gilbert et al.

1996). It has already been shown that strong static

magnetic field (230 and 320 mT) modifies cytological

characteristics and activity of protocerebral mediodorsal

neurosecretory neurones in T. molitor and Lymantria

dispar (Peric-Mataruga et al. 2006, Ilijin et al. 2011). In

our study, static magnetic field (50 mT), regardless of

the magnetic pole, had no influence on development of

T. obscurus and T. molitor pupae. One of the possible

explanations could be that the applied static magnetic

field strength induced changes in neuro-endocrine sys-

tem, but insufficient to affect insect development.

Biogenic amines such as dopamine, norepinephrine,

serotonin, octopamine and tyramine are responsible

for motor behaviour regulation (Pfl ü ger and Duch 2000,

Saraswati et al. 2004, Fussnecker et al. 2006, Brembs et al.

2007, Dernovici et al. 2007, Socha et al. 2008). It is shown that

dopamine and norepinephrine have an ability to enhance

the walking activity in Pyrrhocoris apterus (Socha et al.

2008). Th e serotonin receptor SER-1 (also known as 5HT2ce)

is involved in locomotor activity control and has eff ects

on speed and direction of movement in Caenorhabditis

elegans (Dernovici et al. 2007). Octopamine has been

recognized as a stress hormone which has a great

infl uence on locomotor activity (Saraswati et al. 2004,

Fussnecker et al. 2006), habituation, learning and

memory (Adamo et al. 1995, Unoki et al. 2006). Addi-

tionally, normal locomotor activity of Drosophila larvae

depends on a balance between octopamine and tyramine

(Saraswati et al. 2004). We can propose that static magnetic

fi eld-induced changes in behaviour (distance travelled,

average speed and immobility) of T. obscurus and T. molitor

could be explained by modulation of some steps in synap-

tic transmission mediated by the above-mentioned bio-

genic amines. Observed results could be a consequence

of static magnetic fi eld eff ect on some of Ca 2 � -based

processes responsible for the synthesis and release

of the neuropeptides and neuron activity modulation

(Osborne 1996, N ä ssel 2002). It is possible that applied

static magnetic fi eld (50 mT) directly or indirectly, by

modulation of intercellular Ca 2 � ions fl ux, changes neu-

rotransmitters release and consequently motor behav-

iour of T. obscurus and T. molitor adults. Namely, due to

changes in Ca 2 � ion fl ux in the neurosecretory neurones,

( U � 32, N S group � 11, N Control � 12, P � 0.04). Signifi cant

diff erences were also found between adults where pupa-

adult development was completed closer to the N and S

poles of magnetic dipole for all examined behaviour param-

eters: Distance travelled ( U � 5, N N group � N S group � 11,

P � 0.001), average speed ( U � 7, N N group � N S group � 11,

P � 0.001), and immobility time ( U � 15, N N group �

N S group � 11, P � 0.003).

Discussion

Th e main fi ndings of our study are that static magnetic fi eld

(50 mT) had no eff ect on pupa-adult development dynamic

but modified motor behaviour of adults in examined

Tenebrio species.

Literature data considering the effects of static magnetic

fields on development and viability of insects are contra-

dictory. It has been revealed that static magnetic field

(4.5 mT) does not affect egg-laying, while it increases mor-

tality of eggs, larvae and pupae, as well as decreases adult

viability in Drosophila (Ramirez et al. 1983). Ho et al. (1992)

also reported hatching rate decrease of D. melanogaster

larvae and its lower viability due to the short exposure to

a weak static magnetic field during the early embryogen-

esis. A significant increase of Hylotrupes bajulus viability

and larval mass has been shown after exposure to static

magnetic field of 98 mT (Rau š et al. 2009). Additionally,

static magnetic field of different strength (130 – 180 mT,

320 mT and 375 mT) stimulated the pupal metamorphosis

in Apis melifera , D. melanogaster and T. molitor (Prolic

and Nenadovic 1994, 1995, Prolic et al. 2001). Observed

alteration in development could be attributed to the

influence of static magnetic field on the neuro-endocrine

system implicated in the regulation of all vital processes

in insects. Insect development is controlled by the neuro-

endocrine system and it depends on the balance of two

hormones – ecdyzone and juvenile hormone (Henrich et al.

Figure 3. The effect of static magnetic field (50 mT) on behaviour of T. obscurus adults. Results are presented as mean � SEM (control: n � 8, N group: n � 6 and S group: n � 8).

Table II. Th e eff ect of static magnetic fi eld (50 mT) on duration (days) of T. obscurus and T. molitor pupa-adult development.

T. obscurus T. molitor

Control 10.38 � 0.26 ( n � 8) 10.57 � 0.36 ( n � 14)N group 10.43 � 0.20 ( n � 7) 11.00 � 0.22 ( n � 19)S group 10.42 � 0.19 ( n � 12) 10.56 � 0.27 ( n � 18)

Results are presented as mean � SEM.

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

48 D. Todorovi ć et al .

changes in the vesicles released from the nurosecretory

neurones may occur. In addition, numerous studies have

shown that static magnetic fi elds can cause changes in the

behaviour (Prato et al. 1996), and bioelectric properties of

neurons (Balaban et al. 1990, Rosen 1992, McLean et al.

1995, Ye et al. 2004, Shen et al. 2007, Nikolic et al. 2008).

It is known that the fi ring properties of neurons and electri-

cal signaling between cells imply specifi c energy demands

(Magistretti 2003) and that energy status of the cell infl u-

ences bioelectrical properties of the membrane (Lara

et al. 1999). Th us, it could be possible that some metabolic

processes, like enzyme modifi cations are involved in medi-

ating the observed response of examined Tenebrio species

to the magnetic fi eld. Nevertheless, in order to prove these

hypotheses it is necessary to carry out additional experi-

ments, particularly on the biochemical level.

According to our experimental results, it is obvious that

static magnetic fi eld (50 mT) shows species- and the mag-

netic pole-specifi c eff ects on motor behaviour in T. obscurus

and T. molitor adults. It has already been revealed that even

very similar species can perform diff erent reactions to the

same environmental infl uences (Gomes et al. 2005, Sisodia

and Singh 2005). Some authors indicated on the genetic

basis of natural variation in motor behaviour (Loer and

Kenyon 1993, Sokolowski 1998, Jordan et al. 2006). Osborne

et al. (1997) reported two genes whose protein products have

major function in control of D. melanogaster larvae behav-

iour. Additionally, variation in the biogenic amines synthesis

represents a factor contributing to natural variation in loco-

motor reactivity (Jordan et al. 2006). Taking into account all

these facts and the data concerning the eff ects of static mag-

netic fi elds on DNA structure and gene expression (Giorgi

et al. 1992, Koana et al. 1997, Takashima et al. 2004), the

assumption of individual reaction of each organism, based

on its unique genetic information, is quite acceptable.

One model of detection of magnetic field by animals

proposes that geomagnetic field is perceived by photo-

chemical mechanism involving blue light photoreceptor

named cryptochrome (Foley et al. 2011). According to this

theory, light-dependent magnetoreception is mediated

by chemical reactions which involve formation of mag-

netically sensitive radical pairs by cryptochrome (Gegear

et al. 2010). Previous work established Drosophila as

a suitable model system for exploring mechanisms of

cryptochrome-based magnetoreception (Hoang et al.

2008, Yoshii et al. 2009, Gegear et al. 2010, Foley et al.

2011). Although cryptochrome of type 1 has been only

identified in Drosophila , it could be expected that other

insects also possess this type of cryptochrome. Accord-

ingly, cryptochrome-based magnetorecpetion could be

the mechanism responsible for the reaction of Tenebrio

toward the magnetic field observed in this study.

Despite the current theories of a unique magnetic fi eld,

living beings still make a distinction between the two

magnetic poles (Krylov and Tarakanova 1960, Blakemore

1975, Blakemore et al. 1980, Lee and Weis 1980, Ru ž ic et al.

1993, Yano et al. 2001, Bertolino et al. 2006). Diff erent eff ects

of the N and S magnetic pole were shown in plants and could

be connected with diverse infl uence of the magnetic poles

on the enzymes activity (Krylov and Tarakanova 1960, Ru ž ic

et al. 1993, Yano et al. 2001). In crabs Uca pungilator and

U. pungnax , limb regeneration in a great manner depends

of the applied magnetic pole, probably due to diff erent infl u-

ence on ion fl uxes (Lee and Weis 1980). Finally, Bertolino

et al. (2006) revealed diff erent speed of healing in Wistar rats

exposed to the N and S magnetic pole. All these data are in

line with our observed fi ndings and point out the importance

of separate investigation the magnetic poles eff ects.

In conclusion, static magnetic fi eld (50 mT) could be con-

sidered as a possible stress factor that does not have infl uence

on pupa-adult development dynamic, but shows diff erent

eff ects on motor behaviour in T. obscurus and T. molitor .

Declaration of interest

Th e authors report no confl icts of interest. Th e authors alone

are responsible for the content and writing of the paper.

Th is study was supported by grant of the Ministry of

Education and Science of the Republic of Serbia (Grant No.

173027).

References

Adamo SA , Linn CE , Hoy RR . 1995 . The role of neurohormonal octopamine during ‘ fight or flight ’ behaviour in the field cricket Gryllus bimaculatus . Journal of Experimental Biology 198 : 1691 – 1700 .

Balaban PM , Bravarenko NI , Kuznetzov AN . 1990 . Infl uence of a stationary magnetic fi eld on bioelectric properties of snail neurons . Bioelectromagnetics 11 : 13 – 25 .

Figure 4. Th e eff ect of static magnetic fi eld (50 mT) on behaviour of T. molitor adults. Results are presented as mean � SEM (control: n � 12, N group: n � 11 and S group: n � 11). * P � 0.05 compared to control group; P � 0.01 and P � 0.001 compared to N group (Kruskal-Wallis ANOVA followed by Mann-Whitney U test).

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

Eff ects of static magnetic fi eld in Tenebrio 49

McLean MJ , Holcomb RR , Wamil AW , Pickett JD , Cavopol AV . 1995 . Blockade of sensory neuron action potentials by a static magnetic fi eld in the 10 mT range . Bioelectromagnetics 16 : 20 – 32 .

N ä ssel DR . 2002 . Neuropeptides in the nervous system of Drosophila and other insects: Multiple roles as neuromodulators and neuro-hormones . Progress in Neurobiology 68 : 1 – 84 .

Nikolic L , Kartelija G , Nedeljkovic M . 2008 . Eff ect of static magnetic fi elds on bioelectric properties of the Br and N1 neurons of snail Helix pomatia . Comparative Biochemistry and Physiology A – Molecular & Integrative Physiology 151 : 657 – 663 .

Osborne RH . 1996 . Insect neurotransmission: Neurotrans mitters and their receptors . Pharmacologyw and Th erapeutics 69 : 117 – 142 .

Osborne KA , Robichon A , Burgess E , Butland S , Shaw RA , Coulthard A , Pereira HS , Greenspan RJ , Sokolowski MB . 1997 . Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila . Science 277 : 834 – 836 .

Pan H , Liu X . 2004 . Apparent biological eff ect of strong magnetic fi eld on mosquito egg hatching . Bioelectromagnetics 25 : 84 – 91 .

Peric-Mataruga V , Prolic Z , Nenadovic V , Mrdakovic M , Vlahovic M . 2006 . Protocerebral mediodorsal A2 ′ neurosecretory neurons in late pupae of yellow mealworm (Tenebrio molitor) after exposure to a static magnetic fi eld . Electromagnetic Biology and Medicine 25 : 127 – 133 .

Peric -Mataruga V , Prolic Z , Nenadovic V , Vlahovic M , Mrdakovic´ M . 2008 . Th e eff ect of a static magnetic fi eld on the morphometric characteristics of neurosecretory neurons and corpora allata in the pupae of yellow mealworm Tenebrio molitor (Tenebrionidae) . International Journal of Radiation Biology 84 : 91 – 98 .

Pfl ü ger HJ , Duch C . 2000 . Th e functional role of octopaminergic neurons in insect motor behaviour . ACTA Biologica Hungarica 51 : 343 – 348 .

Prato FS , Kavaliers M , Carson JJL . 1996 . Behavioral responses to magnetic fi elds by land snails are dependent on both magnetic fi eld direction and light . Proceedings of the Royal Society B: Biological Sciences 263 : 1437 – 1442 .

Prolic Z , Andelkovic M . 1992 . Th e eff ect of a strong magnetic fi eld on the frequency of genetic loads in Drosophila melanogaster . Acta Veterinaria (Belgrade) 42 : 343 – 350 .

Prolic Z , Nenadovic V . 1994 . Th e development of Tenebrio molitor pupae exposed to permanent action of the magnetic fi eld . Archive of Biological Science (Belgrade) 46 : 25P – 26P .

Prolic Z , Nenadovic V . 1995 . Th e infl uence of a permanent magnetic fi eld on the process of adult emergence in Tenebrio molitor . Journal of Insect Physiology 41 : 1113 – 1118 .

Prolic Z , Lazarevic J , Mrdakovic M , Popeskovic D . 2001 . Compara-tive examinations of magnetic fi eld eff ects on pupal development in three holometabolous insect species . Acta Entomologica Serbica 6 : 139 – 142 .

Ramirez E , Monteagudo JL , Garcia-Gracia M , Delgado JM . 1983 . Ovi-position and development of Drosophila modifi ed by magnetic fi elds . Bioelectromagnetics 4 : 315 – 326 .

Rau š S , Todorovic D , Prolic Z . 2009 . Viability of old house borer ( Hylotrupes bajulus ) larvae exposed to a constant magnetic fi eld of 98 mT under laboratory conditions . Archive of Biological Science (Belgrade) 61 : 129 – 134 .

Rosen AD . 1992 . Magnetic fi eld infl uence on acetylcholine release at the neuromuscular junction . American Journal of Physiology 262 : C1418 – 1422 .

Rosen AD . 2003 . Mechanism of action of moderate-intensity static magnetic fi elds on biological systems . Cell Biochemistry and Biophysics 39 : 163 – 173 .

Ru ž i c R , Jerman I , Jeglic A , Fefer D . 1993 . Various eff ects of pulsed and static magnetic fi elds on the developmentof Castanea sativa Mill . in tissue culture . Electro- and Magnetobiology 12 : 165 – 177 .

Saraswati S , Fox LE , Soll DR , Wu CF . 2004 . Tyramine and octopamine have opposite eff ects on the locomotion of Drosophila larvae . Journal of Neurobiology 58 : 425 – 441 .

Savic T , Janac B , Todorovic D , Prolic Z . 2011 . Th e embryonic and post-embryonic development in two Drosophila species exposed to the static magnetic fi eld of 60 mT . Electromagnetic Biology and Medicine 30 : 108 – 114 .

Shen JF , Chao YL , Du L . 2007 . Eff ects of static magnetic fi elds on the voltage-gated potassium channel currents in trigeminal root ganglion neurons . Neuroscience Letters 415 : 164 – 168 .

Sisodia S , Singh BN . 2005 . Behaviour genetics of Drosophila : Non-sexual behaviour . Journal of Genetics 84 : 195 – 216 .

Socha R , Kodr í k D , Zemek R . 2008 . Stimulatory eff ects of bioam-ines norepinephrine and dopamine on locomotion of Pyrrhocoris apterus (L.) : Is the adipokinetic hormone involved? Comparative

Bertolino G , de Freitas Braga A , de Oliveira Lima do Couto Rosa K , de Brito Junior LC , de Araujo JE . 2006 . Macroscopic and histological eff ects of magnetic fi eld exposition in the process of tissue reparation in Wistar rats . Archives of Dermatological Research 298 : 121 – 126 .

Blakemore RP . 1975 . Magnetotactic bacteria . Science 190 : 377 – 379 . Blakemore RP , Frankel RB , Kalmijn ADJ . 1980 . South-seeking

magnetotactic bacteria in the Southern Hemisphere . Nature 286 : 384 – 385 .

Brembs B , Christiansen F , Pfl ü ger HJ , Duch C . 2007 . Flight initiation and maintenance defi cits in fl ies with genetically altered biogenic amine levels . Journal of Neuroscience 27 : 11122 – 11131 .

Dernovici S , Starc T , Dent JA , Ribeiro P . 2007 . Th e serotonin recep-tor SER-1 (5HT2ce) contributes to the regulation of locomotion in Caenorhabditis elegans . Developmental Neurobiology 67 : 189 – 204 .

Foley L , Gegear R , Reppert S . 2011 . Human cryptochrome exhibits light-dependent magnetosensitivity . Nature Communications 2 : 356 .

Fussnecker BL , Smith BH , Mustard JA . 2006 . Octopamine and tyramine infl uence the behavioral profi le of locomotor activity in the honey bee ( Apis mellifera ) . Journal of Insect Physiology 52 : 1083 – 1092 .

Gegear R , Foley L , Casselman A , Reppert S . 2010 . Animal crypto-chromes mediate magnetoreception by an unconventional photo-chemical mechanism . Nature 463 : 804 – 807 .

Gilbert LI , Rybczynski R , Tobe SS . 1996 . Endocrine cascade in insect metamorphosis . In: Gilbert LI , Tata JR , Atkinson BG , editors. Metamorphosis: Postembryonic reprogramming of gene expression in amphibian and insect cells . San Diego, CA: Academic Press . pp. 59 – 107 .

Giorgi G , Guerra D , Pezzoli C , Cavicchi S , Bersani F . 1992 . Genetic eff ects of static magnetic fi elds . Body size increase and lethal muta-tions induced in populations of Drosophila melanogaster after chronic exposure. Genetics Selection Evolution 24 : 393 – 413 .

Gomes L , Sanches MR , Von Zuben CJ . 2005 . Dispersal and burial behav-ior in larvae of Chrysomya megacephala and Chrysomya albiceps (Diptera, Calliphoridae) . Journal of Insect Behaviour 18 : 281 – 292 .

Henrich VC , Rybczynski R , Gilbert LI . 1999 . Peptide hormones, steroid hormones, and puff s: Mechanisms and models in insect develop-ment . Vitamins and Hormones 55 : 73 – 125 .

Ho MW , Stone TA , Jerman I , Bolton J , Bolton H , Goodwin BC , Saunders PT , Robertson F . 1992 . Brief exposures to weak static magnetic fi eld during early embryogenesis cause cuticular pattern abnormalities in Drosophila larvae . Physics in Medicine and Biology (London) 37 : 1171 – 1179 .

Hoang N , Schleicher E , Kacprzak S , Bouly JP , Picot M , Wu W , Berndt A , Wolf E , Bittl R , Ahmad M . 2008 . Human and Drosophila cryptochromes are light activated by fl avin photoreduction in living cells . PLoS Biology 6(7) : e160 .

Hong FT . 1995 . Magnetic fi eld eff ects on biomolecules, cells, and living organisms . Biosystems 36 : 187 – 229 .

Ilijin L , Vlahovic M , Mrdakovic M , Mircic D , Prolic Z , Lazarevic J , Peric-Mataruga V . 2011 . Th e eff ects of acute exposure to magnetic fi elds on morphometric characteristics bombyxin-producing neu-rosecretory neurons in gypsy moth catepilars . International Journal of Radiation Biology 87 : 461 – 471 .

Jordan KW , Morgan TJ , Mackay TF . 2006 . Quantitative trait loci for locomotor behavior in Drosophila melanogaster . Genetics 174 : 271 – 84 .

Kefuss J , M ’ Diaye K , Bounias M , Vanpoucke J , Ecochard J . 1999 . Bio-chemical eff ects of high intensity constant magnetic fi elds on worker honey bees . Bioelectromagnetics 20 : 117 – 122 .

Klotz J , Jander R . 2003 . Magnetic sense. In: Resh VH , Card é RT , editors. Encyclopedia of insects . 1st ed . London: Academic Press. pp. 670 – 672 .

Koana T , Okada MO , Ikehata M , Nakagawa M . 1997 . Increase in the mitotic recombination frequency in Drosophila melanogaster by magnetic fi eld exposure and its suppression by vitamin E supple-ment . Mutation Research 373 : 55 – 60 .

Krylov AV , Tarakanova GA . 1960 . Magnetotropism of plants and its nature . Plant Physiology 7 : 156 – 160 .

Lara J , Acevedo JJ , Onetti CG . 1999 . Large-conductance Ca2 � -activated potassium channels in secretory neurons . Journal of Neurophysiology 82 : 1317 – 1325 .

Lee PH , Weis JS . 1980 . Eff ects of magnetic fi elds on regeneration in fi ddler crabs . Biological Bulletin 159 : 681 – 691 .

Loer CM , Kenyon CJ . 1993 . Serotonin-defi cient mutants and male mating behaviour in the nematode Caenorhabditis elegans . Journal of Neuroscience 13 : 5407 – 5417 .

Magistretti PJ . 2003 . Brain energy metabolism . In: Squire LR , editor. Fundamental neuroscience . Chapter 13. New York: Academic Press . pp. 339 – 360 .

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.

50 D. Todorovi ć et al .

V á cha M . 2007 . Tenebrio beetle pupae show a conditioned behavioural response to pulse rotations of a geomagnetic fi eld . Physiological Entomology 32 : 336 – 342 .

V á cha M , Drstkov á D , Puzov á T . 2008 . Tenebrio beetles use magnetic inclination compass . Naturwissenschaften 95 : 761 – 765 .

Yano A , Hidaka E , Fujiwara K , Iimoto M . 2001 . Induction of primary root curvature in radish seedlings in a static magnetic fi eld . Bioelec-tromagnetics 22 : 194 – 199 .

Ye SR , Yang JW , Chen CM . 2004 . Effect of static magnetic fields on the amplitude of action potential in the lateral giant neu-ron of crayfish . International Journal of Radiation Biology 80 : 699 – 708 .

Yoshii T , Ahmad M , Helfrich-Forster C . 2009 . Cryptochrome mediates light-dependent magnetosensitivity of Drosophila’ s circadian clock . PLoS Biology 7 : 813 – 819 .

Biochemistry and Physiology B: Biochemistry and Molecular Biology 151 : 305 – 310 .

Sokolowski MB . 1998 . Genes for normal behavioral variation: Recent clues from fl ies and worms . Neuron 21 : 463 – 466 .

Takashima Y , Miyakoshi J , Ikehata M , Iwasaka M , Ueno S , Koana T . 2004 . Genotoxic eff ects of strong static magnetic fi elds in DNA-repair defective mutants of Drosophila melanogaster . Journal of Radiation Research 45 : 393 – 397 .

Unoki S , Matsumoto Y , Mizunami M . 2006 . Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning . European Journal of Neuroscience 24 : 2031 – 2038 .

V á cha M . 2006 . Laboratory behavioural assay of insect magneto-re ception: Magnetosensitivity of Periplaneta americana . Journal of Experimental Biology 209 : 3882 – 3886 .

Int J

Rad

iat B

iol D

ownl

oade

d fr

om in

form

ahea

lthca

re.c

om b

y U

nive

rsity

of

Chi

cago

on

09/1

0/13

For

pers

onal

use

onl

y.