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Sleep is a well-studied biological process in vertebrates, particularly birds and mammals. Less is know about sleep in solitary and social invertebrates, particularly the ants. This paper reports a study of light/dark periods on worker activity as well as sleep location, posture and the wake/sleep cycles of fire ant workers and queens located in an artificial nest chamber. Workers slept in one of three locations: on the ceiling, against the chamber wall or in the center of the chamber floor. Workers on the ceiling or against the chamber wall slept for longer periods than those at the center of the chamber floor where most grooming and feeding activity occurred. When sleeping, queens huddled together. Their close contact generated synchronized wake/sleep cycles with each other. Sleep posture was distinctly different than wake posture. During deep sleep, queens and workers folded their antennae and were non-responsive to contact by other ants. Another indicator of deep sleep was rapid antennal movement (RAM sleep). Sleep episodes were polyphasic. Queens averaged ~92 sleep episodes per day, each episode lasting ~6min, for a total of ~9.4h of sleep per day. Workers averaged ~253 sleep episodes lasting 1.1min each for a total of ~4.8h of sleep per day. Activity episodes were unaffected by light/dark periods. Workers were hypervigilant with an average of 80% of the labor force completing grooming, feeding or excavation tasks at any given time. These findings reinforce the parental exploitation hypothesis—sterile workers are a caste of disposable, short-lived helpers whose vigilance and hyperactivty increases the queen’s fitness by buffering her and her fertile offspring from environmental stresses.
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Polyphasic Wake/Sleep Episodes in the Fire Ant,
Solenopsis Invicta
Deby L. Cassill & Skye Brown & Devon Swick &
George Yanev
Revised: 26 November 2008 / Accepted: 20 February 2009 /
Published online: 17 March 2009
#
Springer Science + Business Media, LLC 2009
Abstract Sleep is a well-studied biological process in vertebrates, particularly birds
and mammals. Less is know about sleep in solitary and social invertebrates,
particularly the ants. This paper reports a study of light/dark periods on worker
activity as well as sleep location, posture and the wake/sleep cycles of fire ant
workers and queens located in an artificial nest chamber. Workers slept in one of
three locations: on the ceiling, against the chamber wall or in the center of the
chamber floor. Workers on the ceiling or against the chamber wall slept for longer
periods than those at the center of the chamber floor where most grooming and
feeding activity occurred. When sleeping, queens huddled together. Their close
contact generated synchronized wake/sleep cycles with each other. Sleep posture
was distinctly different than wake posture. During deep sleep, queens and workers
folded their antennae and were non-responsive to contact by other ants. Another
indicator of deep sleep was rapid antennal movement (RAM sleep). Sleep episodes
were polyphasic. Queens averaged ~92 sleep episodes per day, each episode lasting
~6 min, for a total of ~9.4 h of sleep per day. Workers averaged ~253 sleep episodes
lasting 1.1 min each for a total of ~4.8 h of sleep per day. Activity episodes were
unaffected by light/dark periods. Workers were hypervigilant with an average of
J Insect Behav (2009) 22:313323
DOI 10.1007/s10905-009-9173-4
D. L. Cassill (*)
Biology, USF St. Petersburg, St. Petersburg, FL 33701, USA
e-mail: cassill@stpt.usf.edu
S. Brown
:
D. Swick
USF, Tampa, FL, USA
S. Brown
e-mail: blueskyestars@aol.com
D. Swick
e-mail: dmz890@yahoo.com
G. Yanev
Mathematics, University of Texas, Arlington, TX, USA
e-mail: yanevgp@utpa.edu
80% of the labor force completing grooming, feeding or excavation tasks at any
given time. These findings reinforce the parental exploitation hypothesissterile
workers are a caste of disposable, short-lived helpers whose vigilance and
hyperactivty increases the queens fitness by buffering her and her fertile offspring
from environmental stresses.
Keywords Wake/sleep cycles
.
circadian rhythms
Introduction
The function of sleep remains unknown despite decades of vigorous research
(Greenspan et al. 2001; Stickgold 2005). A number of hypotheses have been
proposed, but none has gained general acceptance. Pioneering research on sleep with
cockroaches uncover ed remarkable similarities to sleep in mammals (Tobler 1983).
Sleep research on the behavior and neural mechanisms of fruit flies extended our
knowledge of sleep in insects. Fruit flies choose a particular place and position to
sleep; they twitch in a manner similar to REM sleep and they are non-responsive to
their surroundings when sleeping (Hendricks et al. 20 00 ; Shaw et al. 2000; Nitz et al.
2002). The genes that influence sleep patterns in fruit flies are similar to those in
mammals (Huber et al. 2004; Hendricks and Sehgal 2004; Cirelli et al. 2005).
Pharmacological products that regulate sleep in mammals, birds and fish have
similar affects on sleep in fruit flie s (Paredes et al. 2006; Roth II et al. 2006,
Zhdanova 2006; Zimmerman et al. 2006). Converging evidence supports the hypoth-
esis that neurons and neural processes are universal across speciesvertebrates and
invertebrates alike (Hildebrand and Shepherd 1997; Griffith and Rosbash 2008;
Vyazovskiy et al. 2008). Thus, behavioral differences among species lie in the
circuitry of the nervous systemhow neurons are wired togetherrather than the
form and function of individual neurons.
Research into the neural mechanisms of sleep in one species can enlighten us on
the neural mechanisms of sleep in other species (Roth II et al. 2006). Studies of sleep
among caste members in the social insects can extend our understanding of intra-
and inter-specific variability of sleep/wake cycles day-to-day and over evolutionary
time. In this respect, social insects, particularly ants with their distinctive caste
system, are excell ent systems of study. This paper reports a study of the affect of
light on worker activity levels as well as a description of sleep location, posture and
wake/sleep episodes for queens and workers in the fire ant, Solenopsis invicta.
The success of ants worldwide is largely a result of the ability of workers to
quickly switch back and forth from individual to group tasks based on need.
Although worker and queen activity has been widely studied (Hölldobler and
Wilson 1990; Tschinkel 2006), little is known about worker or queen inactivity.
Because fire ants are subterranean dwellers and thus irregularly exposed to
photoperiods, we hypothesized that inactivity in individuals would be polyphasic
and asynchronous, depending more on tasks at hand then on light/dark periods. As
hypothesized, worker inactivity cycles were polyphasic and asynchronous. Unex-
pectedly, we found that que en activity/inactivity cycles were synchronous with other
queens.
314 J Insect Behav (2009) 22:313323
Methods
Polygyne Fire Ant Colonies Doze ns of polygy ne fire ant colonies were collected
from sites in Brazos Valley in Texas, U.S.A. Colonies were separated from the soil in
the usual the drip-floatation method (Banks et al. 1981) and transferred to large
plastic bins containing artificial nests. Colonies were maintained in the plastic bins
on shelves in an insectary at 27°C and ~50% relative humidity with a 14:10 h (light:
dark) photoperiod. Colonies were provisioned with water ad libitum and a daily diet
of 25% honey water and yellow mealworms (Tenebrio molitor). These conditions are
standard for successfully maintaining fire ant colonies which grow rapidly regardless
of whether the insectary is light or dark. Ants adjust to changes in light within
seconds (Cassill and Tschinkel 1999).
Sampling For our study on sleep cycles of fire ant workers and queens, a single
colony was selected from the laboratory-maintained colonies. Thi s colony con tained
a large ratio of brood (eggs, larvae and pupae) relative to workers, indicating the
presence of healthy queens. To simulate the small groupings of fire ants found in
field nest chambers (Cassill et al. 2002), 3 queens, 30 workers and 30 large larvae
where placed in one artificial chamber (15 mm × 10 mm × 5 mm deep with an exit
tunnel). A glass cover slip was placed over the chamber and tunnel, allowing us to
videotape the entire group except the occasional scout when it left the chamber to
forage for food. The artificial nest was placed in a small plastic bin 15.0 cm in
diameter and 5.0 cm deep. This colony was video taped continuously for 4.7 days.
Queen Inactivity/Sleep Data on the activity/in activity of the three queens was
collected from the videotapes. A computerized event recorder was used to record
queen activity/in activity. Queens were selected, one at a time, for behavioral
analysis. Active and inactive durations were recorded in seconds along with the time
of the change in behavior. From these data, the frequency, duration and synchrony of
each queens active and inactive periods were analyzed. In addition, the posture and
location of queens was noted every hour over the 4.7 day period (sample size = 113).
Worker Inactivity/Sleep Sleep data for the 30 workers was collected from one
randomly selected 24-hour period of the study. Data was recorded only on workers
Table 1 Proportion of the Time that Zero, One, Two or Three Queens were Inactive at the Same Time
X0123
Prob(X = k) 0.2046 0.4279 0.2982 0.0693
Table 2 Observations of the Three Queens Included 2,291 Activity/Inactivity Configurations
Number active queens 0 1 2 3
Observed frequencies 489 868 653 281
J Insect Behav (2009) 22:313323 315315
who were inactive on the chamber floor or ceiling, not on workers who were active
(sample size = 287 data points).
To determine worker activity levels, one worker was selected randomly and
observed for 8 h (1 videotape). The videotape was paused every 10 min and the
number of contacts made during the 10-minute episode by this worker with queens,
larvae or other workers was recorded (sample size = 48 counts).
To test for photosensitivity of worker activity rhythms, an experiment was
designed with eight treatments: 12
AM-light; 12 AM-dark; 6 AM-light; 6 AM-dark; 12 PM-
light; 12
PM-dark; 6 PM-light and 6 PM-dark. At the designated time, 20 workers were
placed in a clear plastic vial (100 mm × 25 mm) with damp sand. Ants become
stressed when above ground and will immediately excavate a subterranean chamber.
After 6 h, vials were frozen. The following day, the length and width of tunnels
excavated in each vial during the six-hrs by the workers were measured. Workers dig
along the inside edge of clear plastic vials, thus shafts and chambers are visible to the
eye and easily measure with a flexible plastic metric ruler. Five replicates from five
stock colonies were created per treatment for a 5 × 8 experimental design.
Data Analysis Data were su mmarized and analyzed using J MP IN statistical
software (Sall and Lehman 2005). Duration data were not normally distributed;
thus, data were log transformed and analyzed using ANOVA or t-tests. Means were
transformed back to integers for the figures. Frequency of activity per 8-hr period
among queens was normally distributed;
To quantify the obvious synchrony of queen activity, the proportion of inactivity
time for a single queen was estimated by the ratio (inactivity time)/(total time). The
most conservative estimate of inactivity (i.e. the one that yields the highest
probability for a queen to be inactive) was 0.5893. Assuming no synchrony between
the queens, we have the following probability distribution for the number of
simultaneously active queens (Tables 1, 2, 3).
Results
Queen Activity/Inactivity
Indicators of wake-acti ve episodes in queens took three forms: antennal movement,
head movement, or body movement in the form of walking. When walking or
moving their heads, queens extended their antennae with the scape forward of the
eyes and scape and funiculi at an obtuse angle to each other (Fig. 1a). In addition,
the mandibles and glossae (tongue) were parti ally extended. Queens that ingested
fluids from a worker or from a larvas anal slit, held their antennae with the scape
Table 3 Expected Frequency of the Activity/Inactivity Periods of Three Queens
Number active queens 0 1 2 3
Expected frequencies 469 980 683 159
316 J Insect Behav (2009) 22:313323
and funiculi at acute angles and with the scape extended in front of the eyes (Fig. 1b).
The tips of the antennae poked and probed the worker glossae or the larvasanalslit.
The mandibular teeth tips were touching but not overlapping and the glossae were
partially extended. Queens that regurgitated food to a worker or another queen
extended their antennae with the scape in front of the eyes, forming a right angle with
the funiculi (Fig. 1c). Mandibles were open and the glossae fully extended.
Indicators of queen sleep episodes took two forms: deep sleep or dozing.
During deep sleep, antennae (scape and funiculi) where completed retracted as were
glossae and mandibles (Fig. 1d) and queens were unresponsive to contact by
workers. Frequently, during periods of deep sleep, the folded antennae of queens
quivered in a rapid antennal movement (RAM) that might be an analog to the
rapid eye movement (REM) in vertebrates.
Dozing differed from deep sleep in that antennal were partially extended, with the
scape and funiculi at right angles to each other; in addition, mandibles were partially
open such that the tips of the teeth were touching, but not overlapping (Fig. 1e).
Dozing queens were more likely to respond to contact by workers or other queens
with antennal movements.
The duration of wake-active episodes for queens was significantly longer (2.5 times
longer) than the duration of sleep episodes (Wilcoxon Test: Chi-square = 28.6; p<
0.0001). In total, queens slept a mean total of 9.4 h/day and were active the remaining
14.6 h/day.
Queen sleep/activity episodes were synchronized with each other (Fig. 2). The
Chi-square goodness-of-fit test for synchronized cycles of queen acti vity was
significant (Tables 2, 3; Chi-square = 109.29; p<0.001). The mechanism of
synchrony was tactile. Queens huddled together with overlapping body parts when
inactive (Fig. 3). Increased activity of one queen was transmitted through contact
d
““
‘’’ ‘’’‘’’ ‘’’
a c
Deep sleep Dozing
Actively
sensing environment Ingesting food Ingesting food
b
e
””
Fig. 1 Differences in the angles of a queens antennae during active and inactive phases. The geometry of a
fire ants antennae, mandibles and glossae (tongue segments) varied with wake and sleep episodes. During
deep sleep, the antennae, mandibles and glossae where retracted. Frequently, during periods of deep sleep, the
folded antennae of queens quivered continuously in a rapid antennal movement (RAM) resembling rapid
eye movement (REM) in vertebrates. During dozing episodes, the antennal scapes (the first and elongated
segments) were retracted above the eyes, but the funiculi were extended. In addition, mandibles were partially
open such that the tips of the teeth were touching, but not overlapping. During wake episodes, the antennae
were extended such that the scapes and funiculi were low and in front of the eyes. Mandibles and glossae were
partially or fully extended depending on whether the queen was ingesting or donating nutrients.
J Insect Behav (2009) 22:313323 317317
Inactive
Active
Fig. 3 Queen location in chamber during wake and sleep episodes. Queens huddled together during sleep
episodes. When active, queens were close, but not touching each other. Caveat: Queen body size is not
proportional to chamber size.
0 4 8
Hours
Queen 1
Queen 2
Queen 3
Queen 1
Queen 2
Queen 3
Queen 1
Queen 2
Queen 3
Fig. 2 Lines represent wake/sleep episodes for each of three polygyne queens residing in the same
chamber. Sleep episodes were demarcated from high point to low point ( \ ). Wake episodes were
demarcated from low point to high point ( / ). This graphic display comparing wake/sleep episodes of
three queens suggested a high degree of activity synchrony among the queens which was confirmed by
analysis (Friedman test).
318 J Insect Behav (2009) 22:313323
with the other queens, much like a cue ball activating billiard balls, and the queens
moved apart from each other. When queens were active, half (50.4%) of their
interactions involved grooming (Fig. 4). The remaining activities included feeding
and walking about the brood chamber.
Worker Activity/Inactivity Workers averaged 253.0 sleep episodes a day for a total
sleep time of 4.8 h/day. The duration of sleep episodes did not vary significantly
with the time of day (6
AM,2PM,10PM, ANOVA: F
2,140
=0.82; p=0.441. However,
the duration of sleep episodes did vary significantly with worker location in the
chamber (ANOVA: F
2, 140
=40.05, p<0.0001). Workers on the chamber floor were
inactive for a mean 32.8 s; workers on the glass ceiling wer e inactive for a mean
82.1 s; workers on the side of the chamber were inactive for a mean 108.7 s.
On average, 20% of workers were asleep at any given time; stated another way,
80% of the labor force was wake and active at any given time. The number of
sleeping workers varied by time of day (ANOVA: F
2, 284
=26.270; p<0.0001).
Significantly fewer workers were asleep in the hours 6
AM2 PM than in the hours 2
PM10 PM (Tukey-Kramer HSD: q=0.46; p<0.0001). Significantly fewer workers
were asleep in the afternoon than at night (Tukey-Kramer HSD: q=0.01664; p=
0.029). Of the sleeping workers, 53.8% were on the chamber floor; 27.3% were
hanging from the glass ceiling, and 18.9% were huddled against the chamber wall.
Our analysis of one individual worker over an eight-hour period found that its
activity cycles were idiosyncratic with bursts of high activity interspersed with low
activity episodes (Fig. 5). This individual worker contacted other workers significantly
more often than it contacted queens or larvae (ANOVA: F
2,141
=112.02; p<0.001). The
worker was significantly more active during the second 4-hr period than the first 4-hr
period (t-Test: t
46
=18.84; p<0.001) suggesting that activity levels are idiosyncratic
and vary over time because of and apart from group activity.
40
30
20
10
0
Ingesting Self-grooming Q-Q grooming Walking
W-Q grooming- Egg laying/grooming Drinking anal fluids
from 4 instar larvae
th
Fig. 4 Type and frequency of queen activities during a 4.7 day period. When queens were active, 29.0%
of their interactions were feedings by workers; 16.7% of their time was spent grooming workers or being
groomed by workers (11.7% gray bar; 5% black bar respectively); 16.4% of their time was spent self-
grooming; 9.2% of their time was spent in interactions with other queens; 8.1% of their time was spent
laying eggs (black bar) and grooming eggs (gray bar); 4.3% of their time was spent drinking anal fluids
from 4th instar larvae. The remaining 16.3% of their time was spent walking around the brood chamber.
J Insect Behav (2009) 22:313323 319319
Significantly longer tunnels were excavated in lighted versus dark conditions
(ANOVA: F
1,39
=3.28; p=0.002). Time of day had no affect on tunnel length
(ANOVA: F
4,36
=0.96; p=0.424). These data suggest that ants react to local stimuli
rather than innate biorhythms.
Discussion
Our study on sleep in fire ants reinforces the idea that sleep location, sleep posture
and sleep episodes in invertebrates such as cockroaches (Tobler 1983 ), Drosophila
(Hendricks et al. 2000 ; Shaw 2003; van Swinderen et al. 2004), scorpions (Tobler
and Stalder 1987) and the honey bee (Kaiser 2004) share many of the fundamental
components that define mammalian sleep (Campbell and Tobler 1984, 1989), avian
sleep (Amlaner and Ball 1994 ; Paredes et al. 2006) and fish sleep (Tobler and
Borbély 1985; Yokogawa et al. 2007). Fire ant workers slept in one of three
locations, on the ceiling, against the chamber wall or in the center of the chamber
floor. Workers were disturbed more frequently by active workers and slept for
shorter episodes when on the floor near the center of the chamber. During deep
sleep, queens and workers folded their antenn ae and were non-responsive to contact
by other ants. Another indicator of deep sleep was rapid antennal movement (R AM
sleep) which might be analogous to REM sleep in vertebrates, suggesting that deep
sleep is a feature of all organisms, vertebrates and invertebrates, with a central
nervous system (reviewed in Hobson 2005).
The wake/sleep episodes were polyphasic and synchronous for queens. Queens
averaged over 9 h of sleep per day, occurring in dozens of sleep episodes lasting
6 min each. Queens sleep together and moved slightly apart only when they were
active. Wake/sleep episodes were polyphasic and asynchronous in workers. Workers
0
25
50
75
100
125
150
Number of contacts with others
Time
(8 hrs at 10 minute increments)
0 240 480
Workers
Queens
Larvae
Fig. 5 Type and frequency of contact by one worker with other colony members. During one 8-hour
period, this one worker contacted other individuals a total of 4,601 times. This worker contacted other
workers 3,149 times, larvae 610 times and queens 842 times. Two features of this workers activity were
apparent. (1) During any given 10-min period, this workers activity was never zero, supporting the idea of
workers are hyperviligant sentinels protecting the queen. The level of its activity was greater during the
last 4 h than the first 4-hrs of the observation period. These data suggest that, as a group, workers are
vigilant 24 h a day, while individuals have extended periods in which they are less vigilant than at other
times.
320 J Insect Behav (2009) 22:313323
averaged 5 h of sleep per day, occurr ing in hundreds of sleep episodes lasting 1 min
each.
The relatively lengthy live span and sleep time for fire ant queens (6 years; 9 h/day)
relative to their sterile offspring (1 month to 1 year; 5 h/day) complements the findings in
Drosophila in which flies that sleep less die younger (Cirelli et al. 2005). A comparative
study across ant species correlating the relationship between longevity and sleep
between the fertile and sterile castes would extend the findings on Drosophila.
As a result of their arrhythmic, polyphasic wake/sleep episodes, 80% of the
worker labor force was available every hour of every day to complete tasks needing
attention. Experiments investigating the effects of sleep deficits on division of labor
could enlighten us on the importance of power naps for effective decision-making
(Tietzel and Lack 2002).
Workers were polyphasic, excavating sand round the clock regardless of time of
day or light/dark periods. Polyphasic activity is found in the honey bee nest building
and the naked mole rat nest excavation (Toma et al. 2000). Perhaps animals that spend
the majority of their lives in dark habitats lose sensitivity to photoperiods and lack the
circadian rhythm present in their ancient surface-dwelling ancestors (Isha y et al 2005).
Ultimately, from the queens perspective, a hyper-vigilant labor force reduces her
exposure to risk and thus increases her longevity. A hyperactive labor force also
increases a queens reproductive efficiency. With 80% of worker offspring awake at
any given time, no task is ever left untend ed for longer than a few seconds (Cassill
and Tschinkel 1995, 1999). These findings reinforce the parental exploitation
hypothesis for the evolution of sterile offspring (Ghiselin 1974; Cassill 2006).
Workers are a disposable caste (Cassill 2002) that buffer queens from environmental
stresses, increasing the queens survival and ability to produce fertile offspring over
a lifetime that can extend to 45 years (Tschinkel 1988; Höl ldobler and Wilson 1990).
In conclusion, our study on sleep in fire ants provides a basel ine for studying the
function of sleep in a highly social organism with a caste syst em of short-lived and
long-lived siblings. The study was largely descriptive, providing data on sleep
posture and cycles for fire ant queens and workers residing wi thin the same chamber
with a 1:1 ratio of workers to larvae. Future studies under different conditions will
reveal whether age, size or idiosyncratic factors influence the number and duration
of sleep/wake episodes. Experiments measuring changes in the number or duration
of sleep episo des among a fertility caste of queens and workers as they age, and
under various levels of sleep disruption could add to our understanding of the form
and function of sleep (Lima et al. 2005).
Acknowledgements We thank USF St. Petersburg undergraduates Kim Vo, Lieu Huynh and Thomas
Watkins for recording data on individual workers. Lastly, we thank the editor, Thomas Payne, and three
anonymous reviewers for critical improvements to the initial manuscriptvery helpful. The work reported
herein was funded in part by the Texas Fire Ant Research Initiative 19952005.
References
Amlaner CL, Ball NJ (1994) Avian sleep. In: Kryger MH, Roth T, Dement WC (eds) Principles and
practice of sleep medicine, 2nd edn. WB Saunders, Philadelphia, pp 8194
J Insect Behav (2009) 22:313323 321321
Banks WA, Lofgren CS, Jouvenez DP, Stringer CE, Bishop PM, Williams DF, Wojcik DP, Glancey BM
(1981) Techniques for rearing, collecting and handling imported fire ants. USDA and SEA Agric
Technol Southern Ser 21:19
Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neuroscien
Biobehav Rev 8:269300
Cassill DL (2002) Yoyo-bang: a risk-aversion investment strategy by a perennial insect society. Oecologia
132:150158
Cassill DL (2006) Why skew selection, a model of parental exploitation, should replace kin selection. J
Bioecon 8:101119
Cassill DL, Tschinkel WR (1995) Allocation of liquid food to larvae via trophallaxis in colonies of the fire
ant, Solenopsis invicta. Anim Behav 50:801813
Cassill DL, Tschinkel WR (1999) Information flow during social feeding in ant societies. In: Detrain CT,
Pasteels JL (eds) Information processing in social insects. Birkauser Verlag, Basel, Switzerland,
pp 6981
Cassill DL, Tschinkel WR, Vinson SB (2002) Nest complexity, group size and brood rearing in the fire
ant, Solenopsis invicta. Insectes Soc 49:158163
Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G (2005) Reduced sleep in
Drosophila shaker mutants. Nature 434:10871092
Ghiselin M (1974) The economy of nature and the evolution of sex. University of California Press,
Berkeley CA, USA
Greenspan RJ, Tononi G, Cirelli C, Shaw P (2001) Sleep and the fruit fly. Trends Neuroscien 24:142145
Griffith LC, Rosbash M (2008) Sleep: hitting the reset button. Nature Neuroscien 11:123124
Hendricks JC, Sehgal A (2004) Why a fly? Using Drosophila to understand the genetics of circadian
rhythms and sleep. Sleep 27:334342
Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, Sehgal A, Pack AL (2000) Rest in
Drosophila is a sleep-like state. Neuron 25:129138
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for
common principles across phyla. Ann Rev Neuroscien 20:595631
Hobson JA (2005) Sleep is of the brain, by the brain and for the brain. Nature 437:12541256
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge Mass,
USA
Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:7881
Ishay JS, Pertsis V, Levtov E (2005) Duration of hornet sleep induced by ether anesthesia in curtailed by
exposure to sun or UV irradiation. Cell Mol Life Scien 50:737741
Kaiser W (2004) Busy bees need rest, too. J Compar Physiol A 163:565584
Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim
Behav 70:723736
Nitz DA, van Swinderen B, Tononi G, Greenspan RJ (2002) Electrophysiological correlates of rest and
activity in Drosophila melanogaster. 12:19341940
Paredes SD, Cubero J, Valero V, Barriga C, Reiter RJ, Rodriguez AB (2006) Comparative study of the
activity/rest rhythms in young and old ringdove (Streptopelia Risoria): correlation with serum levels
of melatonin and serotonin. Chronobiol Intern 23:779793
Roth II TC, Lesku JA, Amlaner CJ, Lima SL (2006) A phylogenetic analysis of the correlates of sleep in
birds. J Sleep Res 15:395402
Sall J, Lehman A (2005) JMP start statistics: a guide to statistics and data analysis using JMP and JMP IN
software. Duxbury Press, Albany, NY, USA
Shaw P (2003) Awakening to the behavioral analysis of sleep in Drosophila. J Biol Rhythms 18:411
Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila
melanogaster. Science 287:18341837
Stickgold R (2005) Insight review: sleep-dependent memory consolidation. Nature 437:12721278
Tietzel AJ, Lack LC (2002) The recuperative value of brief and ultra-brief naps on alertness and cognitive
performance. J Sleep Research 11:213218
Tobler I (1983) The effect of forced locomotion on the rest activity cycle of the cockroach. Behav Brain
Res 8:351360
Tobler I (1989) Sleep and alertness: Chronobiological, behavioral, and medical aspects of napping. In:
Dinges DF, Broughton RJ (eds) Napping and polyphasic sleep in mammals. Raven, New York, pp 9
30
Tobler I, Borbély AA (1985) Effect of rest deprivation on motor activity of fish. J Comp Physiol A
157:817822
322 J Insect Behav (2009) 22:313323
Tobler I, Stalder J (1987) Rest in the scorpiona sleep-like state? J Comp Physiol A 13:227235
Toma DP, Bloch G, Moore D, Robinson GE (2000) Changes in period mRNA levels in the brain and
division of labor in honey bee colonies. Proc Nat Acad Scien 97:69146919
Tschinkel WR (1988) Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta.
Physiol Entomol 13:327350
Tschinkel WR (2006) The fire ants. Harvard University Press, Cambridge, MA, p 669
van Swinderen B, Nitz DA, Greenspan RJ (2004) Uncoupling of brain activity from movement defines
arousal states in Drosophila. Current Biol 14:8187
Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G (2008) Molecular and
electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nature
Neuroscien 11:200208
Yokogawa T, Marin W, Faraco J, Pézeron G, Appelbaum L, Zhang J, Rosa F, Mourrain P, Mignot E
(2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PloS
5:23792397
Zhdanova IV (2006) Sleep in zebrafish. Zebrafish 3:215226
Zimmerman JE, Rizzo W, Shockley KR, Raizen DM, Naidoo N, Mackiewicz M, Chrichill GA, Pack AI
(2006) Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol Genomics
27:337350
J Insect Behav (2009) 22:313323 323323
... The state of inactivity or deep sleep exhibited by P. striata is similar to one that described by Cassill et al. [46]. Many workers remained motionless in foraging area. ...
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Citation only. Full-text article is available only through licensed access provided by the publisher. Published in Biology and Philosophy, 25 (3), 437-440. DOI 10.1007/s10539-009-9176-8 Members of the USF System may access the full-text of the article through the authenticated link provided below.
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