In recent years, various animal observation instruments have been developed to support long-term measurement and analysis of animal behaviors. This study proposes an automatic observation instrument that specializes for turning behaviors of pill bugs and aims to obtain new knowledge in the field of ethology. Pill bugs strongly tend to turn in the opposite direction of a preceding turn. This alternation of turning is called turn alternation reaction. However, a repetition of turns in the same direction is called turn repetition reaction and has been considered a malfunction of turn alternation. In this research, the authors developed an automatic turntable-type multiple T-maze device and observed the turning behavior of 34 pill bugs for 6 h to investigate whether turn repetition is a malfunction. As a result, most of the pill bug movements were categorized into three groups: sub-diffusion, Brownian motion, and Lévy walk. This result suggests that pill bugs do not continue turn alternation mechanically but elicit turn repetition moderately, which results in various movement patterns. In organisms with relatively simple nervous systems such as pill bugs, stereotypical behaviors such as turn alternation have been considered mechanical reactions and variant behaviors such as turn repetition have been considered malfunctions. However, our results suggest that a moderate generation of turn repetition is involved in the generation of various movement patterns. This study is expected to provide a new perspective on the conventional view of the behaviors of simple organisms.

1.
A. I.
Dell
,
J. A.
Bender
,
K.
Branson
,
I. D.
Couzin
,
G. G.
de Polavieja
,
L. P. J. J.
Noldus
,
A.
Pérez-Escudero
,
P.
Perona
,
A. D.
Straw
,
M.
Wikelski
, and
U.
Brose
, “
Automated image-based tracking and its application in ecology
,”
Trends Ecol. Evol.
29
,
417
428
(
2014
).
2.
K.
Branson
,
A. A.
Robie
,
J.
Bender
,
P.
Perona
, and
M. H.
Dickinson
, “
High-throughput ethomics in large groups of drosophila
,”
Nat. Methods
6
,
451
457
(
2009
).
3.
A.
Pérez-Escudero
,
J.
Vicente-Page
,
R. C.
Hinz
,
S.
Arganda
, and
G. G.
de Polavieja
, “
idTracker: Tracking individuals in a group by automatic identification of unmarked animals
,”
Nat. Methods
11
,
743
748
(
2014
).
4.
Y.-J.
Chen
,
Y.-C.
Li
,
K.-N.
Huang
,
S.-L.
Jen
, and
M.-S.
Young
, “
Video tracking algorithm of long-term experiment using stand-alone recording system
,”
Rev. Sci. Instrum.
79
,
085108
(
2008
).
5.
A.
Gomez-Marin
,
N.
Partoune
,
G. J.
Stephens
, and
M.
Louis
, “
Automated tracking of animal posture and movement during exploration and sensory orientation behaviors
,”
PLoS One
7
,
e41642
(
2012
).
6.
A.
Strandburg-Peshkin
,
C. R.
Twomey
,
N. W. F.
Bode
,
A. B.
Kao
,
Y.
Katz
,
C. C.
Ioannou
,
S. B.
Rosenthal
,
C. J.
Torney
,
H. S.
Wu
,
S. A.
Levin
, and
I. D.
Couzin
, “
Visual sensory networks and effective information transfer in animal groups
,”
Curr. Biol.
23
,
R709
R711
(
2013
).
7.
A.
Berdahl
,
C. J.
Torney
,
C. C.
Ioannou
,
J. J.
Faria
, and
I. D.
Couzin
, “
Emergent sensing of complex environments by mobile animal groups
,”
Science
339
,
574
576
(
2013
).
8.
S.
Hayona
,
O.
Avni
,
A. L.
Taylor
,
P.
Perona
, and
S. R.
Egnor
, “
Automated multi-day tracking of marked mice for the analysis of social behaviour
,”
J. Neurosci. Methods
219
,
10
19
(
2013
).
9.
N.
Correll
,
G.
Sempo
,
Y. L.
de Meneses
,
J.
Halloy
,
J.-L.
Deneubourg
, and
A.
Martinoli
, “
SwisTrack: A tracking tool for multi-unit robotic and biological systems
,” in
IEEE/RSJ International Conference on Intelligent Robots and Systems
(
IEEE
,
2006
).
10.
A. D.
Straw
,
K.
Branson
,
T. R.
Neumann
, and
M. H.
Dickinson
, “
Multi-camera real-time three-dimensional tracking of multiple flying animals
,”
J. R. Soc. Interface
8
,
395
409
(
2011
).
11.
N. A.
Swierczek
,
A. C.
Giles
,
C. H.
Rankin
, and
R. A.
Kerr
, “
High-throughput behavioral analysis in C. elegans
,”
Nat. Methods
8
,
592
598
(
2011
).
12.
D. J.
Brady
,
M. E.
Gehm
,
R. A.
Stack
,
D. L.
Marks
,
D. S.
Kittle
, and
D. R.
Golish
, “
Multiscale gigapixel photography
,”
Nature
486
,
386
389
(
2012
).
13.
H. S.
Kühl
and
T.
Burghardt
, “
Animal biometrics: Quantifying and detecting phenotypic appearance
,”
Trends Ecol. Evol.
28
,
432
411
(
2013
).
14.
M.
Betke
,
D.
Hirsh
,
A.
Bagchi
,
N.
Hristov
,
N.
Makris
, and
T.
Kunz
, “
Tracking large variable numbers of objects in clutter
,” in
2007 IEEE Conference on Computer Vision and Pattern Recognition
(
IEEE
,
2007
), Vol. 1, pp.
1
8
.
15.
A.
Attanasi
,
A.
Cavagna
,
L.
Del Castello
,
I.
Giardina
,
T. S.
Grigera
,
A.
Jelić
,
S.
Melillo
,
L.
Parisi
,
O.
Pohl
,
E.
Shen
, and
M.
Viale
, “
Superfluid transport of information in turning flocks of starlings
,”
Nat. Phys.
10
,
691
696
(
2014
).
16.
Y.-J.
Chen
,
Y.-C.
Li
,
K.-N.
Huang
,
S.-L.
Jen
, and
M.-S.
Young
, “
Stand-alone video-based animal tracking system for noiseless application
,”
Instrum. Sci. Technol.
37
,
366
378
(
2009
).
17.
A.
Serrano-Muñoz
,
S.
Frayle-Pérez
,
A.
Reyes
,
Y.
Almeida
,
E.
Altshuler
, and
G.
Viera-López
, “
An autonomous robot for continuous tracking of millimetric-sized walkers
,”
Rev. Sci. Instrum.
90
,
014102
(
2019
).
18.
T. A.
Ofstad
,
C. S.
Zuker
, and
M. B.
Reiser
, “
Visual place learning in drosophila melanogaster
,”
Nature
474
,
204
207
(
2011
).
19.
J.
Sakakibara
,
J.
Kita
, and
N.
Osato
, “
Note: High-speed optical tracking of a flying insect
,”
Rev. Sci. Instrum.
83
,
036103
(
2012
).
20.
H.
Wang
,
L.
Zeng
, and
C.
Yin
, “
A video tracking system for measuring the position and body deformation of a swimming fish
,”
Rev. Sci. Instrum.
73
,
4381
4384
(
2002
).
21.
K.
Drescher
,
K. C.
Leptos
, and
R. E.
Goldstein
, “
How to track protists in three dimensions
,”
Rev. Sci. Instrum.
80
,
014301
(
2009
).
22.
S. T.
Hsieh
, “
Three-axis optical force plate for studies in small animal locomotor mechanics
,”
Rev. Sci. Instrum.
77
,
054303
(
2006
).
23.
J. E.
Gould
,
Concise Handbook of Experimental Methods for the Behavioral and Biological Sciences
(
CRC Press
,
Florida
,
2001
).
24.
S.
Streif
,
W. F.
Staudinger
,
D.
Oesterhelt
, and
W.
Marwan
, “
Quantitative analysis of signal transduction in motile and phototactic cells by computerized light stimulation and model based tracking
,”
Rev. Sci. Instrum.
80
,
023709
(
2009
).
25.
W. M.
Lepley
and
G. E.
Rice
, “
Behavior variability in paramecia as a function of guided act sequences
,”
Comput. Physiol. Psychol.
45
,
283
286
(
1952
).
26.
H.
Dingle
, “
Correcting behavior in boxelder bugs
,”
Ecology
42
,
207
211
(
1961
).
27.
D. W.
Dember
and
C. L.
Richman
,
Spontaneous Alternation Behavior
(
Springer
,
New York
,
1989
).
28.
J. L.
Pate
and
G. L.
Bell
, “
Alternation behavior of children in a cross-maze
,”
Psychon. Sci.
23
,
431
432
(
1971
).
29.
W. N.
Dember
and
R. W.
Earl
, “
Analysis of exploratory, manipulatory and curiosity behaviors
,”
Psychol. Rev.
64
,
91
96
(
1957
).
30.
W. K.
Estates
and
M. S.
Schoeffler
, “
Analysis of variables influencing alteration after forced trials
,”
J. Comput. Physiol.
48
,
357
362
(
1955
).
31.
P. A.
Ramey
,
E.
Teichman
,
J.
Oleksiak
, and
F.
Balci
, “
Spontaneous alternation in marine crabs: Invasive versus native species
,”
Behav. Process.
82
,
51
55
(
2009
).
32.
J.
Tuck
and
M.
Hassall
, “
Foraging behaviour of Armadillidium vulgare (isopoda: oniscidea) in heterogeneous environments
,”
Behaviour
141
,
233
244
(
2004
).
33.
J.
Klafter
,
A.
Blumen
,
G.
Zumofen
, and
M. F.
Shlesingerd
, “
Turn alternation in the pill bug (Armadillidium vulgare)
,”
Anim. Behav.
14
,
68
72
(
1966
).
34.
M.
Watanabe
and
K. S.
Iwata
, “
Alternative turning response of Armadillidium vulgare
,”
Annu. Anim. Psychol.
6
,
75
82
(
1956
).
35.
G. D.
Carbines
,
R. M.
Dennis
, and
R. R.
Jackson
, “
Increased turn alternation by woodlice (Porcellio scaber) in response to a predatory spider, Dysdera crocata
,”
Int. J. Comput. Psychol.
5
,
138
144
(
1992
).
36.
Y.
Hayashi
, “
The mechanism of turn alternation in pill bugs
,”
Tsukuba J. Biol.
12
,
TJB201307YH
(
2013
).
37.
K. G.
Hegarty
and
S. L.
Kight
, “
Do predator cues influence turn alternation behavior in terrestrial isopods Porcellio laevis latreille and Armadillidium vulgare latreille?
,”
Behav. Process.
106
,
168
171
(
2014
).
38.
K.
Houghtaling
and
S. L.
Kight
, “
Turn alternation in response to substrate vibration by terrestrial isopods, Porcellio laevis (isopoda: oniscidea) from rural and urban habitats in New Jersey, USA
,”
Entomol. News
117
,
149
154
(
2006
).
39.
R. N.
Hughes
, “
Turn alternation in woodlice (Porcellio scaber)
,”
Anim. Behav.
15
,
282
286
(
1967
).
40.
R. N.
Hughes
, “
Effects of blinding, antennectomy, food deprivation, and simulated natural conditions on alternation in woodlice (Porcellio scaber)
,”
J. Biol. Psychol.
20
,
35
40
(
1978
).
41.
R. N.
Hughes
, “
Mechanisms for turn alternation in woodlice (Porcellio scaber): The role of bilaterally asymmetrical leg movements
,”
Learn. Behav.
13
,
253
260
(
1985
).
42.
R. N.
Hughes
, “
Mechanisms for turn alternation in four invertebrate species
,”
Behav. Process.
14
,
89
103
(
1987
).
43.
R. N.
Hughes
, “
Tactile cues, bilaterally asymmetrical leg movements, and body distortion in isopod turn alternation
,”
Int. J. Comput. Psychol.
2
,
231
244
(
1989
).
44.
R. N.
Hughes
, “
Directional influences of the sixth leg in turn alternation of the terrestrial isopod, Porcellio scaber
,”
Biol. Behav.
15
,
169
182
(
1990
).
45.
R. N.
Hughes
, “
Effects of substrate brightness differences on isopod (Porcellio scaber) turning and turn alternation
,”
Behav. Process.
27
,
95
100
(
1992
).
46.
R. N.
Hughes
, “
An intra-species demonstration of the independence of distance and time in turn alternation of the terrestrial isopod, Porcellio scaber
,”
Behav. Process.
78
,
38
43
(
2008
).
47.
K.
Iwata
and
M.
Watanabe
, “
Alternate turning response in Armadillidium vulgare: 2. Straight moving and turning
,”
Annu. Anim. Psychol.
6
,
53
56
(
1957
).
48.
K.
Iwata
and
M.
Watanabe
, “
Alternate turning response in Armadillidium vulgare: 3. Effect of preceding turn
,”
Annu. Anim. Psychol.
7
,
57
60
(
1957
).
49.
K.
Iwata
and
M.
Watanabe
, “
Alternate turning response in Armadillidium vulgare: 4. Tracks in maze
,”
Zool. Mag.
66
,
464
467
(
1957
).
50.
K.
Iwata
and
M.
Watanabe
, “
Alternate turning response in Armadillidium vulgare: 5. Sense organ functioning in the response
,”
Zool. Mag.
66
,
468
471
(
1957
).
51.
T.
Kawai
, “
Turn alternation in pill bugs (Armadillidium vulgare): Effect of pathlength, orientation, and the number of forced turns
,”
Humanit. Rev.
60
,
113
125
(
2010
).
52.
T.
Moriyama
, “
Decision-making and turn alternation in pill bugs (Armadillidium vulgare)
,”
Int. J. Comput. Psychol.
12
,
153
170
(
1999
).
53.
T.
Moriyama
,
M.
Migita
, and
M.
Mitsuishi
, “
Self-corrective behavior for turn alternation in pill bugs (Armadillidium vulgare)
,”
Behav. Process.
122
,
98
103
(
2016
).
54.
T.
Ono
and
Y.
Takagi
, “
Turn alternation of the pill bug Armadillidium vulgare and its adaptive significance
,”
Jpn. J. Appl. Entomol. Zool.
50
,
325
330
(
2006
).
55.
T.
Moriyama
, “
Anticipatory behavior in animals
,”
AIP Conf. Proc.
465
,
121
129
(
1999
).
56.
T.
Moriyama
and
M.
Migita
, “
Decision-making and anticipation in pill bugs
,”
AIP Conf. Proc.
718
,
459
464
(
2004
).
57.
J.
Murano
,
M.
Mitsuishi
, and
T.
Moriyama
, “
Behavioral pattern of pill bugs revealed in virtually infinite multiple T-maze
,”
Artif. Life Rob.
23
,
444
448
(
2018
).
58.
M. F.
Shlesinger
,
G. M.
Zaslavsky
, and
J.
Klafter
, “
Strange kinetics
,”
Nature
363
,
31
37
(
1993
).
59.
M. F.
Shlesinger
and
J.
Klafter
, “
Lévy walks versus Lévy flights
,” in
On Growth and Form: Fractal and Non-Fractal Patterns in Physics
, edited by
H. E.
Stanley
and
N.
Ostrowsky
(
Martinus Nijhoff
,
Boston
,
1986
).
60.
J.
Klafter
,
A.
Blumen
,
G.
Zumofen
, and
M. F.
Shlesinger
, “
Lévy walk approach to anomalous diffusion
,”
Physica A
168
,
637
645
(
1990
).
61.
A.
Maye
,
C.-h.
Hsieh
,
G.
Sugihara
, and
B.
Brembs
, “
Order in spontaneous behavior
,”
PLoS One
2
,
e443
(
2007
).
62.
A. M.
Reynolds
,
A. D.
Smith
,
R.
Menzel
,
U.
Greggers
,
D. R.
Reynolds
, and
J. R.
Riley
, “
Displaced honeybees perform optimal scale-free search flights
,”
Ecology
88
,
1955
1961
(
2007
).
63.
S.
Bazazi
,
F.
Bartumeus
,
J. J.
Hale
, and
I. D.
Couzin
, “
Intermittent motion in desert locusts: Behavioural complexity in simple environments
,”
PLoS Comput. Biol.
8
,
e1002498
(
2012
).
64.
G. C.
Hays
 et al., “
High activity and lévy searches: Jellyfish can search the water column like fish
,”
Proc. R. Soc. B
279
,
465
473
(
2012
).
65.
D. W.
Sims
,
E. J.
Southall
,
N. E.
Humphries
,
G. C.
Hays
,
C. J. A.
Bradshaw
,
J. W.
Pitchford
,
A.
James
,
M. Z.
Ahmed
,
A. S.
Brierley
,
M. A.
Hindell
 et al., “
Scaling laws of marine predator search behaviour
,”
Nature
451
,
1098
1102
(
2008
).
66.
D. W.
Sims
,
N. E.
Humphries
,
W. B.
Russell
, and
B. D.
Bruce
, “
Lévy flight and Brownian search patterns of a free-ranging predator reflect different prey field characteristics
,”
J. Anim. Ecol.
81
,
432
442
(
2012
).
67.
N. E.
Humphries
,
N.
Queiroz
,
J. R. M.
Dyer
,
N. G.
Pade
,
M. K.
Musyl
,
K. M.
Schaefer
,
D. W.
Fuller
,
J. M.
Brunnschweiler
,
T. K.
Doyle
,
J. D. R.
Houghton
,
G. C.
Hays
,
C. S.
Jones
,
L. R.
Noble
,
V. J.
Wearmouth
,
E. J.
Southall
, and
D. W.
Sims
, “
Environmental context explains Lévy and Brownian movement patterns of marine predators
,”
Nature
465
,
1066
1069
(
2010
).
68.
N. E.
Humphries
,
H.
Weimerskirch
,
N.
Queiroz
,
E. J.
Southall
, and
D. W.
Sims
, “
Foraging success of biological Lévy fights recorded in situ
,”
Proc. Natl. Acad. Sci. U. S. A.
109
,
7169
7174
(
2012
).
69.
E.
Korobkova
,
T.
Emonet
,
J. M. G.
Vilar
,
T. S.
Shimizu
, and
P.
Cluzel
, “
From molecular noise to behavioural variability in a single bacterium
,”
Nature
428
,
574
578
(
2004
).
70.
N.
Nagaya
,
N.
Mizumoto
,
M. S.
Abe
,
S.
Dobata
,
R.
Sato
, and
R.
Fujisawa
, “
Anomalous diffusion on the servosphere: A potential tool for detecting inherent organismal movement patterns
,”
PLoS One
12
,
e0177480
(
2017
).
71.
S.
Petrovskii
,
A.
Mashanova
, and
V. A. A.
Jansen
, “
Variation in individual walking behavior creates the impression of a Lévy flight
,”
Proc. Natl. Acad. Sci. U. S. A.
108
,
8704
8707
(
2011
).
72.
T.
Shokaku
and
K.
Morioka
, “
Development of a behavioral analysis system based on a long-term automatic observation of pill bugs
,” in
Proceedings of SI2018
(
SICE, Tokyo
,
2018
), Vol. 3, pp.
2347
2350
(in Japanese).
73.
K.-N.
Huang
,
Y.-S.
Yeh
,
S.-L.
Jen
, and
Y.-C.
Li
, “
A simple webcam to record animal behavior
,”
Instrum. Sci. Technol.
41
,
619
637
(
2013
).
74.
M. M.
Magdalena
and
N.
Antoni
, “
Comparison of tracking methods in respect of automation of an animal behavioral test
,”
Metrol. Meas. Syst.
18
,
91
104
(
2011
).
75.
K.
Shoji
, “
Individual activity level and mobility patterns of ants within nest site
,” in
International Conference on Swarm Intelligence
(
Springer, New York
,
2018
), pp.
378
384
.
76.
T.
Shokaku
, “
Development of a long-term automatic observation device for pill bugs and the measurement and analysis of their navigation
,” M.S. thesis,
Meiji University
,
Japan
,
2020
(in Japanese).
77.
K.
Branson
and
S.
Belongie
, “
Tracking multiple mouse contours (without too many samples)
,” in
2005 IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR’05)
(
IEEE
,
2005
), p.
1
.
78.
D.
Frenkel
and
B.
Smit
,
Understanding Molecular Simulation: From Algorithms to Applications
(
Academic Press
,
New York
,
2001
).
79.
T. O.
Kvalseth
, “
Cautionary note about R2
,”
Am. Stat.
39
,
279
285
(
1985
).
80.
R.
Metzler
,
J.-H.
Jeon
,
A. G.
Cherstvy
, and
E.
Barkai
, “
Anomalous diffusion models and their properties: Non-stationarity, non-ergodicity, and ageing at the centenary of single particle tracking
,”
Phys. Chem. Chem. Phys.
16
,
24128
24164
(
2014
).
81.
M. F.
Shlesinger
,
J.
Klafter
, and
Y. M.
Wong
, “
Random walks with infinite spatial and temporal moments
,”
J. Stat. Phys.
27
,
499
512
(
1982
).
82.
V.
Zaburdaev
,
S.
Denisov
, and
J.
Klafter
, “
Lévy walks
,”
Rev. Mod. Phys.
87
,
483
(
2015
).
83.
F.
Bartumeus
,
M. G. E.
da Luz
,
G. M.
Viswanathan
, and
J.
Catalan
, “
Animal search strategies: A quantitative random-walk analysis
,”
Ecology
86
,
3078
3087
(
2005
).
84.
O.
Bénichou
,
C.
Loverdo
, and
M.
Moreau
, “
Intermittent search strategies
,”
Rev. Mod. Phys.
83
,
81
(
2011
).
85.
S.
Focardi
,
P.
Montanaro
, and
E.
Pecchioli
, “
Adaptive Lévy walk in foraging fallow deer
,”
PLoS One
4
,
e6587
(
2009
).
86.
H.
Akaike
, “
Information theory and an extension of the maximum likelihood principle
,” in
Proceedings of the 2nd International Symposium on Information Theory
(
Akadémiai Kiadó, Budapest
,
1973
), Vol. 1, pp.
267
281
.
87.
K. P.
Burnham
and
D. R.
Anderson
,
Model Selection and Multimodel Inference
(
Springer
,
New York
,
2002
).
88.
A. M.
Reynolds
, “
Extending Lévy search theory from one to higher dimensions: Lévy walking favours the blind
,”
Proc. R. Soc. A
471
,
20150123
(
2015
).
89.
E. P.
Raposo
,
S. V.
Buldyrev
,
M. G. E.
da Luz
,
G. M.
Viswanathan
, and
H. E.
Stanley
, “
Lévy flights and random searches
,”
Phys. A: Math. Theor.
42
,
434003
(
2009
).
90.
H.
Murakami
,
C.
Feliciani
, and
K.
Nishinari
, “
Lévy walk process in self-organization of pedestrian crowds
,”
J. R. Soc. Interface
16
,
20180939
(
2019
).
91.
G. M.
Viswanathan
,
S. V.
Buldyrev
,
S.
Havlin
,
M. G. E.
da Luz
,
E. P.
Raposo
, and
H. E.
Stanley
, “
Optimizing the success of random searches
,”
Nature
401
,
911
914
(
1999
).
92.
G.
Ramos-Fernandez
,
J. L.
Mateos
,
O.
Miramontes
,
G.
Cocho
,
H.
Larralde
, and
B.
Ayala-Orozco
, “
Lévy walk patterns in the foraging movements of spider monkeys (Ateles geoffroyi)
,”
Behavioral Ecology and Sociobiology
55
,
223
230
(
2004
).
93.
D. A.
Raichlen
,
B. M.
Wood
,
A. D.
Gordon
,
A. Z. P.
Mabulla
,
F. W.
Marlowe
, and
H.
Pontzer
, “
Evidence of Lévy walk foraging patterns in human hunter-gatherers
,”
Proc. Natl. Acad. Sci. U. S. A.
111
,
728
733
(
2014
).
94.
T. H.
Harris
,
E. J.
Banigan
,
D. A.
Christian
,
C.
Konradt
,
E. D.
Tait Wojno
,
K.
Norose
,
E. H.
Wilson
,
B.
John
,
W.
Weninger
, and
A. D.
Luster
, “
Generalized Lévy walks and the role of chemokines in migration of effector CD8+ T cells
,”
Nature
486
,
545
548
(
2012
).
95.
A.
Reynolds
, “
Liberating Lévy walk research from the shackles of optimal foraging
,”
Phys. Life Rev.
14
,
59
83
(
2015
).
96.
A. M.
Reynolds
, “
Current status and future directions of Lévy walk research
,”
Biol. Open
7
,
bio030106
(
2018
).
You do not currently have access to this content.