Flash Communication in Fireflies

Transcription

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VOLUME 60,
THE
No. 4
DECEMBER
QUARTERLY
REVIEW
of
B IOLOGY
COMMUNICATION
IN INSECTS
I. FLASH COMMUNICATION IN FIREFLIES
ALBERT D.
CARLSON
& Behavior,State Universityof New York,
Department
of Neurobiology
Stony Brook, New York11794
JONATHAN
COPELAND
*
Departmentof Biological Sciences, University of Wisconsin-Milwaukee,
Milwaukee, Wisconsin 53201 USA
ABSTRACT
Thefireflyflash is a signal in a courtshipsystembasedupontimingpatternscontrolled
by
thebrain.Courtshipflash
codessupplybothspeciesandsexidentification
andrelyonprecisetimto preserveinformation.
ing and stereotypy
of oneor a few temporal
parameters
Theflashcontrolsystemis physiologically
complex.It involvesrandom
physiologicalfluctuationsthattendto introduce
andthusto degrade
transvariabilityintocommunication
information
thephysiological
basisofflashcommunication
it is therefore
essentialtoestablish
fer. To understand
thelimitsoffluctuationwithinwhichtheentiresystemmustoperate.Thephysiological
processes
thatareso variableinvolvesensoryreception,
centralintegration,
and theoutputof an unusual
neuroeffector
(thefireflylantern).Forexample,thepatterngenerators
offirefliesmustbeprimed
to operatewith sufficientprecision. Insufficientlyprimed animals produceflashes of abnormal
kinetics and timing. Flashing behaviorof fireflies is greatly affected by the animal's state of
arousal; quiescentfireflies are inducedtoflash with difficulty, whereasexcitedanimals produce
rapid and variedluminescentemissions. Also, thefirefly's visual apparatusis highly specialized
for the receptionoffast transientflashes, and its ability toprocessothertypesof photic information
remainsunknown. Finally, andperhapsmostsignificantly, theflash patterngeneratorsoffireflies
can be entrainedby incomingflashes to produce, in females, responsesof appropriatedelay; and
in males, flash synchrony.
Lloyd (1981b) has proposedthat aggressivemimicry by Photuris femmes fatales has had
a great evolutionaryimpact on theflash codesof preyfirefly species. This mimicrymay represent
a simple entrainmentof Photuris females to a wide arrayofflash patterns. Theprecisionofflash
behaviorshould be measuredin females of known physiological state and previousflash history
in orderto assess the effect of mimicry on firefly courtship behavior.
*
Present address: Dept. of Biology, SwarthmoreCollege, Swarthmore,Pennsylvania 19081 USA.
? 1985 by the Stony Brook Foundation, Inc. All rights reserved.
415
1985
416
THE QUARTERLY REVIEW OF BIOLOGY
INTRODUCTION
HE FLASH of a firefly, a brillant
burst of light lasting fractions of a second, is a signal in a courtship and mating
communication system in which species and
sexual identity are conferred by flash timing
parameters (McDermott, 1910-1917; Buck,
1937; Barber, 1951;Lloyd, 1966a).
The flash code involved in courtship and
mating behavior is both stereotyped and interactive. In the simplest and least ambiguous case, something that rarely occurs in the
field and must usually be achieved through
controlled laboratory or field studies, an isolated pair of individuals produces stereotyped
flash patterns. Male and female thus act as
both sender and receiver in "typical"firefly
flash communication, and little variability in
signaling is to be seen.
Firefly communication, however, does
show some variability, and such variability
(noise) may enter at any stage. Such stages involve sensory reception, central processing of
the photic signals, and motor output to a
highly unusual effector organ, the firefly lantern. This variability may be quantified and
its limits defined.
Additional sources of variability also exist
the recognition of which is critical to an understanding of firefly communication: (1)
small changes or nuances in timing patterns
may occur during the later stages of firefly
courtship; (2) there may be changes in the
central excitatory state of either organism;
and (3) previous flash and mating history result in variability.
The stereotyped nature of firefly flash
communication is thus somewhat illusory.
Fixity of pattern exists to a certain extent in
both laboratory and field, but upon arrival
in the field an observer is struck with the
cacophony of flashes with which a firefly
must contend.
Recently there have developed two approaches to the analysis of variability seen in
the field: an adaptationist approach and a
neuroethological approach. In the adaptationist approach, functions are assigned to all
flashes observed, and the variability seen is
thought to be maintained in the population
by sexual selection (Lloyd, 1969a). Not all
flashes, then, are considered to be courtship
T
[VOLUME
60
flashes, in the simplistic sense indicated
above. Fireflies must also contend with
numerous competing deceitful flash strategies, such as rivalry flashes, designed to win
females in courship competition. Thus, injected flashes (Lloyd, 198 la) and transvestite
flashes (Lloyd, 1984) have been described to
explain some of the variability seen in the
field.
In addition, some flashes seen in the field
are only indirectly involved in sexual selection for they are actually used in predation.
Flash mimicry by both male (Lloyd, 1980)
and female (Lloyd, 1965) fireflies has been
hypothesized to have evolved in obtaining
food or, indirectly, in the search for a mate.
Still other flashes are thought to be involved in behaviors other then courting. For
example, landing flashes are supposed to
light up a landing site (Lloyd, 1968; Papi,
1969); some flashes are said to aid the female
in finding a suitable egg-laying site (Kaufmann, 1965); or aerial predators ("hawkers")
home in on flashing targets (Lloyd and Wing,
1983).
The second, or neuroethological
approach, suggests that (1) the firefly's nervous
system is designed to produce flashes in
stereotyped timing patterns; (2) the variability seen in the field can be largely explained
by definable and measurable physiological
fluctuations; (3) the firefly's state of arousal
and its previous flash history are critically
important in understanding the meaning of
particular flashes; and (4) most flashes involved in communication can be described
and modelled according to certain simple
physiological rules.
Fireflies present a nearly ideal group of insects for neurobiological or behavioral study
of animal communication (Lloyd, 1983), for
a number of reasons. First, not only is firefly
communication dynamic and interactive,
both males and females exchanging information rapidly, but also the signals can be observed and recorded at a distance without affecting the interaction. The observer can,
furthermore, easily participate in the exchange by means of simple equipment such
as a flashlight. In addition, the rationales and
results of the communication paradigm are
usually obvious. Second, the communication
system is amenable to a degree of neu-
1985]
DECEMBER
FLASH COMMUNICATION
417
20 16
_
1st BURST
N=75
12 8-
z 4-)
I1 1I
z
u
I
1 1
A
20-
,
0
oL
0
16-
2nd
12
N=74
BURST
idIL Th4I6
8-
z
r
LU
4
D-
20
3rd BURST
N=59
16_
2
84_
8
12
16
20
24
NUMBER OF SPIKES PER BURST
FIG.
1.
RELATIONSHIP BETWEEN NEURAL ACTIVITY RECORDED IN THE LANTERN TISSUE AND THE
TRIPLE-PULSED COURTSHIP FLASH OF A Photurisversicolor
MALE
(A) Photomultiplieroutput (upper trace) and action potential volleys (lower trace) recorded from the
anterior segment of a lantern during two courtship flashes of a restrained male. The average interval
between the first and second flash pulses was 243.9 + 8.67 (S.D.) msec (N=98); between the second
and third flash pulses it was 236.7 + 9.04 (S.D.) msec (N=86). The bar equals 100 msec.
(B) The variation in number of spikesper burst in the three volleys that trigger the pulses of the courtship flash. No consistent relationship was observed between spike numbers and flash pulse intensities.
Temperature, 210C.
rophysiological analysis, because fireflies of
some species will continue their courtship behavior when restrained or even in dissected
preparations (Fig. 1). Third, each species of
firefly produces a different courtship code
(Lloyd, 1966a), differences that make comparative studies possible. Fourth, the flash
patterns are clearly under the control of the
firefly's brain (Case and Buck, 1963; Buck,
Case, and Hanson, 1963) and therefore rep-
resent patterns of activity that can provide insight into the insect's brain function. All of
these advantages make firefly courtship a
powerful communication system that lends
itself to the precise analysis of behavior.
In this review we first provide a brief
description of the natural history of fireflies.
To demonstrate the potential complexity of
courtship communication, the courtship of
Photinusmacdermottifireflies is described in de-
418
tail. Next, the physiological basis of flash
control is described. This section included a
description of lantern anatomy and innervation, of flash production, of the sensory
reception of flashes, of the central programming of flash behavior, and of synchronous
flashing as an example of the role of pacemakers in flash timing, and an analysis of
flash entrainment by Photuris versicolor females. This section is completed by summary
of the physiological processes that influence
and control flash behavior. In the next section, this physiological background is used to
analyze predatory mimicry by female Photuris
fireflies. The importance of understanding
the physiological limits inherent in firefly
flash communication before assigning putative functions to flash behaviors observed in
the field is discussed.
THE
NORTH
NATURAL
HISTORY
AMERICAN
OF
FIREFLIES
Fireflies are luminescent beetles of the
family Lampyridae (McDermott, 1964). The
description that follows is confined to the two
principal genera of north American fireflies:
the yellow-green-flashing Photinus, the taxonomy of which has been studied by Green
(1956) and by Lloyd (1966a, b, 1969b); and
the green-flashing Photuris, the taxonomy of
which is less well known (Barber, 195 1;
Lloyd, 1969b).
The life cycle of a firefly is typical of a
coleopteran. It begins with the egg stage, followed by an overwintering larval stage of a
number of instars, then by pupation in the
spring, and eventual eclosion as an adult,
usually in June or July. Photinus larvae are
only rarely found on the surface, as they
spend most of their lives under the leaf litter
or in the soil. Photurislarvae, in contrast, are
found in large numbers at night on the surface of the ground, in moist areas in late
spring and early autumn. They apparently
require two years for development (Williams, 1917; Hess, 1922; McDermott, 1958;
McLean, Buck and Hanson, 1972). This larval life stage is carnivorous. The larvae feed
on other insect larvae, worms, and molluscs,
which they immobilize by injecting poison
into them through their curved mandibles
(Fabre, 1919; Schwalb, 1961; Copeland,
1980).
[VOLUME
60
The larval firefly possesses tiny, paired
lanterns on the sternite of the eighth abdominal segment. These lanterns differ significantly in structure (Buck, 1948; Peterson,
1970) and in biochemistry (Strause and
DeLuca, 1981) from the adult's lantern,
which occupies all or a portion of the sixth
and seventh abdominal sternites. The larval
lantern is incapable of producing a flash. Instead, the insect produces a glow that waxes
and wanes over a period of seconds.
The role of the larval lantern has been the
object of considerable speculation (Sivinski, 1981). One possible function is as an
aposematic signal to warn nocturnal predators of the insect's unpalatability (Carlson
and Copeland, 1978). This interpretation is
suggested by two observations: (1) that Photuris larvae luminescence immediately upon
being touched or handled; and (2) that they
exude a liquid which appears to be noxious
to mammals such as mice (Carlson and
Copeland, 1978). Finally, the fact that adult
fireflies are unpalatable to a number of
potential predators (Lloyd, 1973a; Vernon,
1983) also suggests aposematic signalling.
Many vertebrates, such as thrushes (Eisner,
Wiemer, Haynes, and Meinwald, 1978) and
the big brown bat (Vernon, 1983), reject
adult fireflies promptly or avoid them entirely. Adults of some species exude a liquid
that appears to be noxious to ants and lizards
(Williams, 1917; Blum and Sannasi, 1974).
Their unpalatability is due, in part, to lucibufagins (Eisner et al. 1978), so-called because these substances resemble bufodienolides, the cardiotonic agents present in
toad skin.
The Photuris larva overwinters within a
pupal cell constructed of mudballs (Hess,
1920; McLean, Buck, and Hanson, 1972).
In the second spring it pupates and develops
the adult lantern on the sixth and seventh abdominal sternites. Initially, the lantern can
only produce a glow, which eventually can be
quenched in scattered areas of the lantern.
Slowly the ability to produce a flash arises
(Carlson, 1969), the process being still incomplete after the eclosion and emergence of
the adult (Strause, DeLuca, and Case,
1979). During this period the larval lanterns
usually degenerate and disappear. Harvey
and Hall (1929) excised the larval lanterns
DECEMBER
FLASH COMMUNICATION
1985]
without any effect on development of the
adult lantern, and thus established that the
former is not a precursor of the latter.
THE
COURTSHIP
OF
Potinus macdermottiFIREFLIES
The Nearctic Photinus fireflies include
several dozen species (Green, 1956; Lloyd,
1966a). They communicate by one of two basic flash codes. The simplest code is typified
by P. pyralis, the most widespread American
firefly. It involves a series of consecutive
flashes emitted by the male at intervals of
about 6 seconds at 23?C and a single flash answer by the female approximately 2 seconds
after each male flash (Buck, 1937). The other
courtship flash code is emitted by P. consanguineus, P. greeni, and P. macdermottifireflies,
members of the so-called consanguineus
group (Lloyd, 1966a). In these, the male
emits courtship flashes in pairs, with a fixed
interval between the two flashes of the courtship pair, and a variable period between the
pairs. The female responds after the second
flash of each pair, twisting her lantern in the
male's direction. The courtship of P. greeni
has been studied intensively by Buck and
Buck (1972).
All flash-timing parameters, including
flash duration and frequency, are affected by
temperature (Buck, 1937; Edmunds, 1963;
Carlson, Copeland, Raderman, and Bulloch, 1976; Carlson, 1981). Unless otherwise
specified here, flash periods and latencies are
given for approximately 20?C.
Photinus macdermottimales emit a pair of
courtship flashes of approximately a 2.3second period and receive answers from the
perched female about 1.5 second after the
second flash (Lloyd, 1966b, 1969b; Carlson
et al., 1976, 1977). If a male approaches a female through the grass, he will climb a blade,
stop, emit a pair of flashes, and receive an answer from the stationary female. He will then
move to the top of another blade of grass before emitting his next courtship pair of
flashes. If a male approaches a female from
the air, he will hover in flight in front of the
female and will fly upward between his courtship flashes. Upon receiving an answer, he
will dip and climb again while flashing.
These courtship flashes become extremely
dim as courtship proceeds, so that the possi-
419
bility of detection by other males is reduced.
This behavior is similar to that found in orthopteran males, in which pair-forming signals are loud, but those emitted by males
near females are characteristically muted
(Otte, 1972).
Flying Photinus macdermottimales who have
not located a female produce strings of rhythmically repeated flashes approximately onehalf second longer in flash period (i.e., 2.6
sec.) than courtship flashes (Carlson et al.,
1976). This seemingly insignificant difference in timing produces a change in female
behavior. The longer interval between these
flashes induces females to respond after each
flash instead of answering every alternate
flash, like females replying to flashes in the
courtship rhythm. Perhaps, by receiving answers to consecutive flashes, the flying male
can obtain information from the female more
rapidly, and this signal enables him to locate
her more precisely. The paired courtship
flashes, emitted once the male has located a
female, are apparently designed, in part, to
establish that the answers are coming from a
conspecific female.
A courting male might be expected to ignore flashes that arrive between his first and
second courtship flashes because such answers are not appropriate to the basic firefly
code. However, experiments with courting
males have revealed that this assumption is
1978).
wrong (Carlson and Copeland,
Flashes that arrive within one second after
the first courtship flash cause the male to delay his second courtship flash by up to 300
msec. Perhaps the male interprets the premature answer of the female as a flash from another male and, by delaying his second flash,
attempts to synchronize more closely with
the intruding male's second flash. If the intruding flash arrives between 1 and 1.5 seconds after the first flash, the courting male
cancels his second flash and initiates another
pair of courtship flashes. He may interpret
this flash as coming from the female because
it is properly timed, even though it follows
the wrong flash. Flashes that arrive later than
1.5 seconds after the courting male's first
flash usually have no effect on his second
flash, probably because the male is already
committed to emit that flash.
A rival male that happens upon a court-
420
ship in progress adopts one of two behaviors
designed to compete for the female's attention. He attempts either to synchronize his
flash with the courting maie's second flash, or
he flashes within a second after the female's
response (Lloyd, 1981a,b; Carlson and
Copeland, 1983). By synchronizing with the
courting male's second flash, the rival male
does not mis-time the 2-second courtship
flash interval so essential to obtain a female's
response. Furthermore, he can induce the female to aim her answer in his direction (Carlson and Copeland, 1983, and unpub.). Frequently the female does answer toward the
rival male. The function of the flash sometimes emitted by the rival male after the female's response, the "transvestite flash" of
Lloyd (1984), is unknown. Experiments reveal that it is timed from the courting male's
second flash and represents a repetition of the
courting rhythm. It appears, then, that the
rival male has timed incorrectly from the
original courting male's second flash instead
of from his first flash. This is an example of
the kind of perceptual miscue that plagues
firefly courtship. Although this competing
flash does not normally induce another response from the female, she will often reorient her subsequent answers toward the intruding male (Carlson and Copeland, 1983,
and unpub.)
The type of flash activity just described
portrays "normal" behavior at the peak of the
nightly activity period. However, both males
and females require a preliminary period of
flashing before they are capable of the stereotyped flash periods and flash responses of
normal dialogue. For example, we have
observed that following a period of flash
quiescence, many Photinus macdermottimales
emit a series of flash pairs of variable but increasing period before they attain the normal
and
flashes (Carlson
period between
Copeland, unpub.). One such male produced a series of paired courtship flashes of
increasing interval beginning at intervals of
1625 msec, and finally stabilized at a 2000
msec interval after eleven flash pairs. This
same male, when attempting to compete with
another courting male during this period,
first appeared to interject flashes 1450 and
1600 msec after the courting male's first
courtship flash. Eventually, he synchronized
[VOLUME
60
his competing flash with the courting male's
second flash when his own courtship flashes
attained the 2000 msec interval.
If exposed to a long quiescent period with
no flashing, Photinus macdermottifemales will
normally answer any flash, even that of a
lighted match or lightning. Additionally, many
females when beginning the evening courtship, answer consistently after both the first
and second male flashes. In one case, the female answered 5 of the first 15 counterfeit
courtship flash pairs after both the first and
second flashes, but she answered after both
flashes only once in the next 41 courtship
pairs (Carlson and Copeland, unpub.).
Thus, either the female's ability to discriminate the flash interval or her ability to
respond is strongly affected by a previous
photic input. Carlson et al. (1977) observed
that females routinely responded to the first
flash pair of an inappropriate period following a number of pairs of proper period, all of
which she had answered. Alternatively,
when subjected to a series of inappropriate
flash pairs, the female failed to respond to the
first pair of the proper period. This observation suggests, then, that both the firefly's
state of arousal and past history are important in assessing flash behavior.
From computer analysis of the responses
of Photinusmacdermottifemales to a wide range
of counterfeit flash patterns, Soucek and
Carlson (1975) developed a model to explain
female flash-response behavior. The model
involves an alternating series of excitatory
and inhibitory periods initiated by the incoming male flash. This response function,
combined with a short-term memory of
previous flashes and background noise, determines the probability of particular female
responses. The actual responses of females to
counterfeit flash sequences show good agreement with those predicted by the model
(Carlson and Soucek, 1975).
The courtship protocol of P. macdermotti
fireflies is one of the most complex described
for a Photinus species. It is not clear whether
the complexity is unique to this species or
simply reflects the greater attention investigators have paid to P. macdermotti.The behavioral nuances that this species exhibits,
such as (1) males changing the flash interval
between patrolling and courting, (2) the abil-
DECEMBER
FLASH COMMUNICATION
1985]
ity of rival males to synchronize, (3) the
changes in flash response by females when
presented with different male flash patterns,
and particularly (4) the effect of previous
flash history on flash behavior, are likely to
have counterparts in some or all other Photinus species. With this in mind, it is essential
that the courtship flash protocols of firefly
species be examined under carefully controlled conditions so that the firefly's entire
courtship repertoire is well understood. Only
then is it possible to assess the functions of the
various flash behaviors observed.
ROLE
IN
OF
FIREFLY
THE
NERVOUS
FLASH
SYSTEM
COMMUNICATION
Our description of the physiological
processes that underlie the receiving and
sending of flashes by fireflies is not meant to
be exhaustive. An understanding of the physiology is necessary, however, to allow an assessment of the capabilities, limitations, and
variations of firefly flash behavior. For a
detailed historical review of research on firefly flash control the reader is directed to Buck
(1948), and for more recent information to
Case and Strause (1978).
Anatomical Organizationof the
Adult Lantern and Its Innervation
The ultrastructure of the male Photurislantern has been described by Beams and Anderson (1955), Kluss (1958), and Smith
(1963). It is organized into a ventral photogenic layer and a dorsal reflector layer. Uniformly spaced tracheae and nerves penetrate
ventrally into the photogenic layer and form
vertical "cylinders" around which are arranged rosettes of photocytes. Tracheal
processes, enclosed in tracheolar cells, project horizontally away from the tracheal
cylinders, pass through mitochondria-filled
tracheal end cells, and run between the photocytes. Axons leave their surrounding
sheath cells and terminate in pad-like endings between the tracheal end cells and the
tracheolar cells (Smith, 1963). The nerve
endings contain both small electron-clear
vesicles and large, electron-dense vesicles.
Synaptic specializations appear between the
nerve endings and the tracheolar cells, and
the latter cells therefore appear to be the elements that couple neural activity to photo-
421
cyte response and may be capable of generating propagated potentials themselves (Case
and Strause, 1978).
The photocytes are highly structured.
They have a clear, outer, differentiated zone
and an interior filled with photogenic granules believed to have peroxidase activity
(Hanna, Hopkins, and Buck, 1976). These
granules contain internal tubular processes
(Smith, 1963) and the light-emitting molecule, luciferin (Hopkins and Hanna, 1972;
Smalley, Tarwater, and Davidson, 1980),
and luciferase (Neuwirth, 1981). By the use
of image-intensified cinematographics, Hanson, Miller, and Reynolds (1969) have determined that the smallest functional luminescent unit in the lantern is a "microsource"
composed of three photocytes.
The light-emitting reaction involves the
interaction of reduced luciferin (LH2), luciferase (E), Mg++ and ATP to form an activated (LH2-E-AMP) complex and pyrophosphate (McElroy and DeLuca, 1978, 1981).
This complex is oxidized by oxygen to form
an oxidized complex (L-E-AMP), with the
emission of light. In the light-emitting reaction, one quantum of light is emitted for every luciferin molecule oxidized (Seliger and
McElroy, 1960).
Seven dorsal unpaired median (DUM)
neurons, which reside in the sixth and seventh abdominal ganglia, represent the final
common motor pathway from the central
nervous system (CNS) to the lantern
(Christensen and Carlson, 1981). These
cells, three in the sixth and four in the seventh abdominal ganglia, have a structure
that is characteristic of DUM neurons identified in other insects (Hoyle, Dagan,
Moberly, and Colquhoun, 1974). Projecting
dorsally from each large soma is a neurite,
which bifurcates into two bilateral axons that
leave the ganglion and ramify extensively
throughout the photogenic tissue (Christensen and Carlson, 1981). This arrangement is
capable of synchronizing the excitation of
thousands of photocytes to produce the coordinated flash of the male.
Motor (Neural and Pharmacological)
Controlof the Flash
The adult firefly's lantern has the characteristics of a true neuroeffector similar to
422
muscle (Chang, 1956; Buck and Case, 1961).
It responds to direct electrical stimulation
analogously to muscle, and shows facilitation, summation, constant stimulus-response latency, tetanus, treppe, adaptation,
and fatigue (Buck and Case, 1961). The
topographical organization of the lantern's
luminescence closely follows its gross neural
organization (Hanson, 1962). Direct electrical stimulation of the photogenic tissue
produces two kinds of flash responses depending upon the voltage of the stimulus
(Buck, Case, and Hanson, 1963). At lowstimulus voltages, a flash of 70 msec. latency
appears; at high voltages there is a "quick"
flash of 18 msec. latency. In the former case,
the lantern appears to be activated by way of
its nerves, but the quick flash is presumably
caused by a more direct activation of the photogenic tissue that bypasses the nerves.
Initial studies of the pharmacology of the
adult lantern implicated an adrenergic transmitter (Smalley, 1965; Carlson, 1968a), but
in the larval lantern the monophenolic
amines, synephrine and octopamine, were
found to be even more potent (Carlson,
1968b). The photomotor neurons, like the
DUM neurons of other insects (Hoyle, 1975;
Evans and O'Shea, 1977) are now believed to
contain octopamine as a neurotr ansmitter
(Robertson and Carlson, 1976; Copeland
and Robertson, 1982). This concept has been
strengthened by the demonstration that octopamine is not only found in the larval lantern, but also in the lantern ganglion (8th abdominal) and in the photomotor neurons
themselves (Christensen, Sherman, McCaman, and Carlson, 1983). An octopaminesensitive adenylate cyclase has been found in
the larval lantern (Oertel and Case, 1976).
Exogenously applied octopamine stimulates
the production of enormous quantities of cyclic AMP (Nathanson, 1979); Nathanson
and Hunnicutt, 1979), which is believed to
act as a second messenger in the induction of
luminescence. The remaining steps in the
chain of events from neural input to luminescence are unknown. Complicating the search
is the fact that any manipulation of the adult
lantern that admits oxygen induces an uncontrollable glow.
Oxygen control, therefore, appears to play
a major role in the ability of the adult lantern
[VOLUME
60
to make a rapid, brilliant burst of luminescence.
Favoring this interpretation,
Ghiradella (1977, 1978, 1983) had reported
that the lantern tracheoles contain unusual
strengthening structures that may insure an
access of oxygen to the photogenic tissue by
resisting collapse when fluid is absorbed from
the tracheoles. DeLuca and McElroy (1974)
reported that mixtures of luciferase and substrate, allowed to form the active complex,
reach peak luminescence in only 60 msec. following injection of oxygen. Several hundred
milliseconds are needed if the reaction is initiated by combining luciferin with luciferase
and cofactors in the presence of oxygen.
Although we do not understand the final
coupling mechanisms, the knowledge that
the brain, operating via the photomotor neurons, can precisely control the flash of the
firefly, is sufficient to identify flash behavior
as a true reflection of the output of timing circuits (pattern generators) residing inrthe firefly brain.
SensoryReceptionof the Flash
The firefly's flash is a signal that must be
clearly distinguished from visual interference
by ambient light. Flashing activity, therefore, is restricted to periods of low illumination. For example, Dreisig (1975) has shown
that the peak of flashing activity by fireflies
in different geographic areas does not begin
before the environmental illumination levels
have dropped below 1 lux.
The firefly's compound eye is apparently
also tuned to the emission spectrum of its
own species' flash. The luminescence spectra
of North American fireflies have maxima in
the yellow-green spectral band (Seliger,
Buck, Fastie, and McElroy, 1964; Biggley,
Lloyd, and Seliger, 1967). By means of the
electroretinogram two sensitivity peaks were
found in the eyes of Photinus pyralis (Lall,
Chapman, Trouth, and Holloway, 1980)
and Photinus macdermotti(Lall, pers. commun.). One peak is in the near ultraviolet,
the other in the longer wavelengths close to
the emission peak (565 nm) of the flash of
those species. The longer-wavelength sensitivity peak in the eye of Photuris versicoloralso
corresponds to the emission peak of its green
(552 nm) flash (Lall, 1981). Lall, Seliger,
Biggley, and Lloyd (1980) demonstrated a
DECEMBER
1985]
FLASH COMMUNICATION
correlation between the firefly's emission
spectrum and the light level during courtship
activity. Yellow-flashing fireflies tended to be
active only at dusk while green-flashing species did not become fully active until full
darkness. Seliger, Lall, Lloyd, and Biggley
(1982a, b) pointed out that at dusk there is a
large amount of reflected green light from
vegetation and that consequently flashes in
or approaching the yellow region of the spectrum will stand out in contrast to this reflected
green color.
The firefly eye itself contains further
specializations that increase its sensitivity.
The ommatidia are constructed to sum light
from several facets while also preserving
some directional information from the source
(Horridge, 1969). Not only are the eyes and
facets of luminescent lampyrids generally
larger than those of non-luminescent species,
but the eyes and facets of dark-active fireflies
are larger than those of dusk or active forms
(Case, 1984). The brain of the firefly shows
specializations for processing luminescent
signals: in Phausis splendidulathe optic lobe of
the brain reflects the large size of the eyes
(Ohly, 1975).
The incoming flash that is transduced by
the eye can be complex in form and timing
(see Fig. 1), and some of the timing
parameters may be important in flash codes.
However, such features of the flash as its
color, intensity, or movement have been
shown to be unimportant (Lloyd, 1966a). In
Photinus fireflies, Lloyd (1966a) conclusively
demonstrated that timing parameters (the
male's flash interval and duration and the female's flash duration and response latency)
play important roles in species recognition
and sexual recognition. The neural correlates of most of these stimulus features have
not yet been studied.
Many male courtship flashes contain characteristic intensity modulations (see Figure
1). Lloyd (1973b) had pointed out that although absolute flash intensity is of little use,
since it varies with distance, the fixed relative
intensities of bimodal courtship flashes, for
example in Southeast Asian fireflies, would
be preserved over distance and therefore
serve as excellent parameters for flash recognition. As other examples, the Luciola lusitanica female triggers her responses from the on-
423
set of the rapidly brightening male flash
(Papi, 1969), and Photuris lucicrescensfemales
trigger their responses from the slowly rising
intensity of the male crescendo flash (Carlson, Copeland, and Shaskan, 1982). Unmated P versicolorfemales require at least two
interpulse intervals of less than 300 msec before responding to a male's courtship flash.
ANALYSIS
OF
OF
THE
THE
CENTRAL
FLASH
PROCESSING
INPUT
Studies made of the courtship flash patterns of North American lampyrids by
McDermott (1910-1917), Buck (1937), Green
(1956), Buck and Buck (1972), Lloyd (1966a),
and others, of a European firefly, Luciola lusitanica by Papi (1969), and of Japanese fireflies by Ohba (1983), among others, have revealed the stereotyped nature of photic
communication systems. Barber (1951), in his
study of Photuris fireflies in the Baltimore
area, emphasized this fact by means of a concept that he termed a "physiological species."
This concept recognizes that the dialogue
flash pattern is as useful a taxonomic tool as
are morphological characters. However, the
complexities of the Photuris flash code make
the use of flash behavior as a taxonomic tool
difficult (Lloyd, 1969a).
The studies of Buck, Case and Hanson,
reviewed by Carlson (1969), have revealed
that the firefly flash provides a window into
the insect's brain activity. Case and Buck
(1963) were able to monitor the neural input
to the lantern by means of electrodes inserted
into the lantern. They found that the overall
pattern of luminescence
intensity corresponded rather well to the structure of the
incoming neural burst. The correspondence
of the burst with the flash is not exact, however, because the recording electrodes in the
lantern sample only a small portion of the
neural input, whereas the phototube records
the luminescence produced by the entire lantern (see Fig. 1).
Case and Buck (1963) also found that the
overall luminescent activity of an individual
closely mirrored the firefly's excitatory state.
Refractory animals could be made to flash
only with difficulty. Initially, the lantern
glowed and scintillated with unstructured luminescence. Animals in this state were characterized by very high electrical thresholds,
424
dim induced luminescence, a lack of spontaneous flashing and lethargic behavior. Responsiveness could be restored by handling
the firefly or by other irritation. Arousal had
to precede decapitation, however, a fact suggesting that the level of brain excitability determines the responsiveness of the entire excitation pathway. Case and Buck (1963)
speculated that prior to flashing, the Photuris
lantern requires neural priming before wellshaped courtship flashes can be produced.
Once both male and female Photuris fireflies
become aroused, they could flash spontaneously for hours.
Excited Photuris versicolormales often emit
simple, rhythmic flashes that are unlike their
rapidly modulated courtship flashes. These
simple flashes do not elicit responses from
conspecific females. P versicolorfemales are
often observed flashing spontaneously as they
walk through the underbrush, and these females do not respond to flash signals of any
kind (Barber, 1951). Luminescence, therefore, is to be observed in non-courtship situations during which the animal is agitated or
is actively moving.
Although males of most American Photinus
fireflies produce flashes of a relatively simple
time course, the courtship flashes of Photuris
males can be intensity-modulated. The crescendo flash of Photuris lucicrescens,a slowly
brightening glow culminating in a brilliant
burst of light, is shaped by a long, continuous
neural burst, probably of increasing spike frequency (Carlson, Copeland, and Shaskan,
1982). The courtship flash of P versicolor
(Carlson, 1981) is composed of three pulses,
usually of descending intensity, and is shaped
by three neural bursts of descending spike
number (see Fig. 1). As is illustrated in Fig.
1, the flash-generating center in the brain of
P versicolormale fireflies is capable of producing a stereotyped pattern of neural bursts in
which spike number, spike frequency, and
burst period are relatively constant. Fluctuations in these neural parameters do occur,
however, as is also shown in Fig. 1. Not only
do individual bursts vary in spike number,
but single courtship flashes also can vary
from two to many pulses. The consequence of
these inherent fluctuations for the effectivness of communication can only be determined by an analysis of courtships under
controlled conditions.
[VOLUME
60
In the absence of the central nervous system, the lanterns of some fireflies of the genus
Photurisrespond differently to direct electrical
stimulation. In deganglionated lanterns of
P lucicrescensmales, it is possible to alter the
time course of luminescence by changing the
frequency of electrical stimulation (Carlson,
Copeland, and Shaskan, 1982). Deganglionated P versicolorlanterns respond only with
short flash pulses of approximately 100 msec
duration, no matter what stimulus parameters are used. For example, a 500-msec
stimulus train composed of 1-msec stimuli of
100 Hz frequency results in a triple-pulsed
flash of descending pulse intensity. This flash
differs from the courtship flash only in having
shorter interpulse intervals. Stimulation for
longer periods simply produces paroxysms of
flash pulses, but no glowing (Carlson, 1981).
The lanterns of these two species also differ
in their response to solutions in which sodium is replaced by potassium: P versicolor
lanterns scintillate vigorously in such a solution (Carlson, 1967) whereas those of P lIuczcrescensrespond only with a glow (Carlson,
unpub.).
In intact Luciola lusitanica males, Buonamici and Magni (1967) observed two responses
to direct electrical stimulation with single, 10msec stimuli. A flash of 100 to 160 msec
latency that was kinetically identical to the
spontaneous flash was followed by a flash of
variable latency (220-750 msec) and variable
contour. The latter response could not be induced in decapitated males, however, and it
was attributed to reflex activity elicited by
stimulation of some afferent pathway. Magni
(1967) reported that spontaneous flashing
could be depressed by photic stimulation of
high intensity and could be facilitated by low
levels of illumination. Flashes evoked by direct stimulation of the lantern could also be
inhibited by strong photic stimulation, and
this effect was mimicked in decapitated males
by low-frequency stimulation of the ventral
nerve cord.
Brunelli, Buonamici, and Magni (1968a)
demonstrated that illumination of the eyes of
one male could depress the intensity and rate
of flashing of a second firefly when their body
cavities were connected by a saline bridge.
Ablation of the gonads eliminated this inhibitory effect induced by illumination and by
low-frequency ventral nerve cord stimulation
DECEMBER
1985]
FLASH COMMUNICATION
(Brunelli, Buonamici, and Magni, 1968b).
Perfusion of the body cavities of fireflies with
a homogenate of gonads reestablished the inhibition (Brunelli, Buonamici, Magni, and
Viola-Magni, 1970). The inhibitory substance was located in granules derived from
the cortex of the male gonad. Cortical granule number was reduced in illuminated
males, and isolated granules produced the
same inhibitory effect as whole-gonad extracts. Noradrenaline, which is present in
large amounts in the gonadal granules, induced flash inhibition and was postulated to
be the active, inhibitory substance (Bagnoli,
Brunelli, Magni, and Viola, 1972).
By using restrained preparations, some
properties of the central processing system
have been revealed via electrical or photic
stimuli delivered to the firefly's eye. Electrical
stimulation of the eye of a Photurismale with
simulated photic input could inhibit or enhance flashing, depending upon the relative
intensities of eye and brain stimulation (Case
and Buck, 1963). In Photurisfemales this photic inhibition caused by photic stimulation
peaked at about 300 msec, then changed into
a period of increased excitation manifested as
a lowered threshold to brain stimulation
(Case and Trinkle, 1968; Carlson and
Copeland, 1972). In Luciola lusitanica photic
stimulation of the eyes of both males and females induced not inhibition, but a flash response of 250 msec latency (Papi, 1969;
Brunelli, Magni, and Pellegrino, 1977), and
direct electrical stimulation of the eye mimicked this response in females (Papi, 1969).
Brunelli, Magni, and Pellegrino (1977) found
that weak photic stimuli induced a later response of 600 msec latency in males, and they
concluded that each photic stimulus exerts a
dual action on the photomotor centers of the
protocerebrum. They suggested that the neural mechanisms underlying reflex flashing
are identical in both sexes.
In one of the most extensive studies of central control, Bagnoli, Brunelli, Magni, and
Musumeci (1976) investigated the neural
mechanisms underlying flashing in Luciola lusitanica by using localized electrolytic lesions
and electrical stimulations. Electrical stimulation of the median protocerebral neuropil
induced fully formed flashes, whereas lesions
to this area abolished spontaneous flashing.
Separation of the protocerebrum from the
425
optic lobes stopped rhythmic flashing, which
was replaced by a continuous dull luminescence. Concomitantly, the flash-inducing
photic nerve volleys in the lantern nerves
were replaced by an asynchronous, lowfrequency discharge of these nerves. Ablation
of the retina-lamina ganglionaris complex
resulted in a marked increase of flash frequency, and stimulation of the more central
optic ganglion, the medulla, facilitated flashing. From these and other findings these investigators concluded that the rhythmic activity of the central photic neurons, located in
the deep protocerebral neuropil of the firefly's brain, results from an oscillator located
in the optic lobes. The retina-lamina complex
exerts a tonic inhibitory influence on flashing, whereas the medulla induces a phasic
facilitatory influence.
To explain the response patterns of predatory Photuris versicolorfemales, Soucek and
Carlson (unpub.) have developed a quantitative model based upon generation of a sequence of time windows. Using a similar approach to their earlier model for Photinus
macdermotti(Soucek and Carlson, 1975), this
model can predict the female's response patterns with considerable precision. The model
proposes that the response patterns of these
females are the result of the entrainment of
brain oscillatory circuits that have fixed
periods, but can be influenced by the female's
previous flash history.
Fireflies, then, probably have brain circuits
that produce flashes patterned in the domain
of time. The synchronously flashing fireflies
of Southeast Asia represent an excellent example of the e-volution of precision in such firefly timing circuits. They have provided ideal
material for the analysis of flash control by
the nervous system (Buck, Buck, Hanson,
Mets, and Atta, 1981). The analysis of flash
synchrony in fireflies will be described next.
The Analysis of CentralProcessingin
SynchronouslyFlashing Fireflies
Nothing emphasizes the importance of
timing patterns and oscillators in firefly flash
codes as well as synchronous flashing does.
While both Photinuspyralis and Photinus macdermottimales show some propensity for synchronous flashing during courtship, Southeast Asian fireflies of the genera Pteroptyxand
Luciola have carried this behavior to a spec-
426
tacular extreme, when entire trees containing
a swarm of males pulsate rhythmically with
light.
As described by Buck and Buck (1966,
1968, 1976, and 1978), males congregate in
large numbers in trees along river banks and
flash at frequencies of 1 to 4 hz, depending on
the species, but in total synchrony. In Malaysia and Thailand, synchronizing males of
Pteroptyxmalaccaeappear to be evenly spaced
within the mangrove trees and exhibit a flash
period of 500 to 600 msec. Photomultiplier
recordings of their double-pulsed flashes
show such complete coincidence that the
shape of the individual male's flash is easily
discerned within the massed display.
In another Malaysian species, Pteroptyx
tener, which synchronizes at about 3.7 Hz
(Case, 1980), the males may recognize females by means of the latter's nonsynchronized flashes, which should stand out
from the background display. Prior to attempting copulation, the male mounts the female, twists its lantern over her head, and
flashes in synchrony with other males,
directly into her eyes.
In his comparative studies of such firefly
pacemakers, Hanson (1978) has suggested
that at least two different mechanisms exist to
attain synchrony. It could be attained either
by a cycle-by-cycle phase shift of a stable oscillator or by a change of the underlying period
of a variable oscillator. The synchronously
flashing New Guinea firefly, Pteroptyxcribellata, is an example of a species using the first
mechanism (Hanson, Case, Buck, and Buck,
1971; Buck, Buck, Case, and Hanson, 1981).
It emits free-run flashes at nearly 1 Hz. A
flash from another male seen within a critical
period after flashing resets the first male's
next flash cycle to the beginning. If the two
males' flash periods are very similar, the reset
flash by the follower male coincides with the
next flash fromi the pacemaker male, and synchrony results (Hanson, Case, and Barnes,
1972; Hanson, 1978). P malaccaeand P tener
use a different mechanism to achieve synchrony. They can synchronize with an out-ofphase pacer flash by slightly shortening or
lengthening their flashing periods so that
coincidence develops over the course of
several cycles (Hanson, 1978). These males
are continually resetting their flashes to
achieve more precise synchrony. This ten-
[VOLUME
60
dency to synchronize is so strong that males
will continue to flash in synchrony with their
conspecifics even during flight or while
mating.
Photinuspyralis males can synchronize their
courtship flashes emitted every six seconds,
particularly if they are densely aggregated
(Buck, 1935; Buck, Hanson, Buck, and Case,
1982). In this case, however, the resetting
male pacemaker flash triggers a flash from
the synchronizing male within less than 400
msec. Since the P pyralis flash normally lasts
600 msec, both flashes overlap and appear to
synchronize. This is a different mechanism
from that of New Guinea Pteroptyxmales, in
which the pacemaker flash resets the nextflash
period of the follower male.
Sychrony is probably necessary to preserve
the timing patterns essential for sexual and
species recognition in an environment
crowded with many individuals (Otte, 1980).
Although males and females can direct their
flashes by twisting their lanterns toward flash
sources and therefore have some directional
sense, they apparently cannot discriminate
between spatially separate light sources that
occur simultaneously. Therefore, flashes entering one eye can easily destroy the timing
pattern of flashes entering the other eye. Case
(1984) has shown that in Pteroptyxtenermales
synchrony can be established to two spatially
separated light generators 1800 out of phase
at half the required frequency, summing to
make the required frequency. An analogous
situation occurs in Photinus greeni females
(courtship code similar to Photinus macdermotti) (Case, 1984). The interval between the
P greenimale's courtship flash pair is about 1.2
seconds, and the female answers 600 to 800
msec after the second flash. If the female
receives two properly timed flashes from one
source in one eye and receives a flash from a
different source in the other eye during the
period between those flashes, she does not respond to either. If she receives two properly
timed flashes from two different sources, one
in each eye, she responds toward the flash that
arrived second.
The female's response can be manipulated
even after she has received a correctly timed
flash pair. A third flash timed to arrive in one
eye slightly after two properly timed flashes
delivered to the other eye causes the female to
respond in the direction of the third flash and
1985]
DECEMBER
8
2
_
6
_
16
FLASH COMMUNICATION
24
32
40
48
10 _
ir
14 -
m
18 _
z
-
22
-
26 _
I
34 _
_
30 _
38
-
1
42
-
w
46
-
o
50
cn
_
at the proper latency following that flash, that
is, at a slightly longer latency than might be
expected to follow the normal pair (Case,
1984).
Because the eye of the firefly is designed to
collect light over a wide area and because of
the animal's inability to attend and respond
to localized points of light to the exclusion of
other light sources, flash communication in
dense aggregations is very difficult. In this
situation, flash synchrony becomes an extremely useful tool for extracting the timing
relationships of male and female flashes.
Analysis of CentralProcessing.
Flash Entrainment
-
54
-
58
-
62
-_
66
-
Additional insight into the operation of
central processing is obtained by an examination of a mating-induced change in flash behavior seen in Photuris versicolorfemales (Nelson, Carlson, and Copeland, 1975). Prior to
mating, these females respond only to a con16
8
24
32
(FFA)
LATENCY
To
OF RESPONSES
48
OF Afemmefatale
PAIRS OF COUNTERFEIT
VARYING
40
x 100)
TIME (milliseconds
FIG. 2.
427
FLASHES
A
OF
INTERVALS
The first counterfeit flash is placed at 0 on the
abscissa and the second counterfeit flash at the beginning of each horizontal line. Flash pairs were
separated by intervals of at least 10 seconds. The
first ten counterfeit flashes of 300 msec period induced female responses averaging 2900 msec
latency, measured from the second counterfeit
flash. Most counterfeit flash pairs induced female
responses of 800 to 1100 msec latency (measured
from the second counterfeit flash). Response
latency to counterfeit flash pairs of greater than
1500 msec was significantly longer. Flash pairs 62
to 64 show a typical response of afemmefatale to abrupt changes in flash parameters. The period of
flash pair 63 was longer than 1500 msec, but the
femmefatale exhibited a short latency (1040 msec)
response, characteristic of answers to flash periods
of less than 1500 msec.
The counterfeit flash period and female flash
latency were measured from the onset of each
flash. The females included in these tests and in
Fig. 3 and Tables 2 and 3 were each maintained
in a terrarium in the field. Counterfeit flashes were
produced by a stimulator-driven flashlight and female responses were detected by a photomultiplier, the output of which was fed to an FM tape
recorder. Tape recorder records were transferred
to a Beckman Dynagraph pen recorder (Fig. 3),
and the measurements were made from the
records. Temperature, 21?C.
D
Is
FIG.
3.
EXAMPLES OF ENTRAINMENT OFfemme
fatale C's (FFC) (SEE TABLE 3) RESPONSES TO
MULTIPLE
COUNTERFEIT
FLASHES
The female'sresponses are marked with circles.
Counterfeit flash period in msec is as follows: (A)
500, 520, 312. (B) 1280, 1240, 1250, 1332, 1400.
(C) 420, female latency 640 msec to 3rd, 4th, and
5th counterfeit flashes. (D) 560, female latency 750
msec to 2nd, 3rd, 4th, and 5th counterfeit flashes.
Note the characteristicintensity pattern of female
responses. Time scale: 1 second. Temperature,
22?C. Counterfeit flashes of 150 msec duration
have been cut at the top by the recorder. Experimental protocol, as described for Fig. 2.
428
TABLE 1
Responselatency(RL) of femme fatale B (FFB) to
stimulusflashes (SF)
SF Interval
SF
RL after Last SF
(msec)
(msec)
number
(x)
(S. D.)
(n)
420
440
516
1100
1600
2168
1400*
2
3-5
2
2
2
2
1
3022
715
836
770
899
2286
1027
37.3
51.8
12.9
46.2
45.0
190.8
68.3
7
45
8
29
5
11
12
* Rhythmically repeated flashes.
Interval between paired and multiple flash sets was
over 5 seconds. Paired flashes as illustrated in Fig. 3A,
rhythmicallyrepeated flashes as in Fig. 3B, and multiple
flashes as in Figs. 3C and D. See Fig. 2 for description
of experimental protocol. Temperature, 21?C.
specific male's triple-pulsed courtship flash,
by answering approximately 1 second after
the end of the flash. In this unmated state, the
stationary female answers male courtship
flashes from a hunched posture, while twisting her lantern toward the male flash. Within
three days after mating, the female responds
very infrequently to a conspecific male's
courtship flash, but she does respond to a
wide range of other flash patterns. In this behavioral mode the female adopts an upright,
prey-capture posture and is highly mobile.
With appropriate flash responses these voracious insects are capable of attracting heterospecific males, then capturing and devouring
them. In this predatory state, mated females
that respond to flashes of heterospecific males
have been called femmesfatales (Lloyd, 1965)
and their behavior has been proposed as an
example of aggressive mimicry (Wickler,
1968).
The attractiveness of Photuris females in
these two mated states is illustrated by observations of a femmefatale and an unmated female placed in adjacent terraria in the field.
At one time, nine conspecific males were observed on the unmated female's terrarium,
whereas the femmefatale did not attract a single male all evening (Carlson and Copeland,
unpub.).
Barber (1951) observed Photuris females
walking through the underbrush and flashing
spontaneously, apparently oblivious to exog-
[VOLUME
60
enous flashes. He suggested that these females had already mated. We have found that
such females, oblivious to flashes at first, become femmesfatales when tested again one to
three days after capture. Zorn and Carlson
(1978) observed that unmated females, mated
to sterile males, remain in the courtship posture but no longer respond at all to flashes.
These unfertilized females did not become
femmesfatales. Zorn and Carlson (1978) speculated that mating causes the females to stop
answering conspecific male courtship flashes,
but something transferred by the male, such
as sperm, is required to induce predatory
mimic behavior.
It appears that the flash-control circuits of
femmesfatales can be triggered by a wide array
of flash patterns. Femmesfatalesof Photuris versicolor tested in the field or in the laboratory
show highly stereotyped and precise response
patterns (Figs. 2 and 3, Tables 1 and 2). They
respond to rhythmically repeated flashes
(flash trains) with a fixed latency to each of
the flashes. Within certain limits, femmefatale
flash latency can clearly be triggered by
paired flashes at certain interflash intervals.
The response behaviors offemmesfatales A
(see Fig. 2), B (see Table 1), and C (see Table
2 and Fig. 3) were similar to that shown by
12 other females tested. The responses to
stimulus flashes of different patterns and
periods can be summarized as follows:
(1) At the extremes of the sign.al pair interval (short intervals of less than 320 msec and
long periods over 1500 msec) female response
latency changes abruptly, but consistently.
As might be expected, however, the exact
break point is affected by temperature. FFA
(see Fig. 2) and FFB (see Table 1) were tested
near 21?C, whereas FFC (see Fig. 3 and Table 2) was tested between 220 and 23.3?C.
This difference may explain why FFC
responded to paired flashes of a 320-420
msec period differently than did FFA or FFB.
(2) Single flashes more than 5 seconds apart
elicited responses of approximately 3 seconds
latency (see FFC, Table 2, Part B).
(3) The Photuris versicolor triple-pulsed
courtship flash has pulse periods ranging
from 220 to 270 msec at temperatures of 23?
and 20?C respectively (Carlson, 1981), and
the unmated female requires at least two
periods (three flashes) before she will respond
DECEMBER
1985]
FLASH COMMUNICATION
429
TABLE 2
Responselatency(RL) of femme fatale C (FFC) to stimulusflashes (SF)
A.
RESPONSES
TO PAIRED
FLASHES
741
666
665
756
775
729
802
988
320
420
560
620
900
1100
1620
1620*
27.1
26.5
40.0
12.8
33.3
24.6
5.4
67.2
17
6
14
27
13
10
5
5
FirstSF of flashpair
B.
SF Interval
(msec.)
5000
940
1050
1450
1600
1900
RESPONSES
TO SINGLE
FLASHES
FLASHES (FIG. 3B)
Response Latency to Stimulus
Flashes (msec.)
(x)
(S.D.)
(n)
AND REPEATED
Type
2858
786
773
795
879
904
Single
Trains
t
it
t
it
C.
SF Period
(msec.)
420
520
746
3A)
Response Latency after Stimulus
Flashes (msec)
(x)
(S.D.)
(n)
SF Interval
(msec)
*
(FIG.
RESPONSES
SF 2
738
746
TO MULTIPLE
FLASHES
(FIG.
74.1
39.2
61.7
54.0
37.2
40.4
3C AND D)
Response Latency to Stimultis Flashes (msec.)*
SF 4
SF 5
SF 3
640
706
757
643
735
760
11
17
52
96
6
21
647
SF
6
646
760
*
Rangeof standarddeviations10.4-19.0.
Restperiodbetweenpresentations
of pairedandmultipleflashsetswas5 secondsorlonger.SeeFig. 2 fordescription of experimentalprotocol.Temperature,
22.0?-23.30C.
(Zorn and Carlson, 1978). Femmesfatales appeared unable to resolve periods that short
(see FFA, Fig. 2; FFC, Table 2). They respond to double and triple-pulsed flashes of
less than 420 msec interflash interval in identical fashion to single flashes, with response
latencies of about 3 seconds measured from
the onset of the second stimulus flash. It is
possible thatfemmesfatales cannot resolve flash
pairs 400 msec or less apart and therefore respond as if they were observing single flashes.
(4) Paired flashes 500 to 1400 msec apart
induced responses of 650 to 900 msec latency
(see FFA. Fig. 2; and FFB and FFC, Tables
1 and 2). Flash trains with periods in the
same range induced responses in the
650-1000 msec latency range (see FFB, Table
1; FFC, Table 2 and Fig 3). In this timing
range the latency of responses remained relatively constant with increasing period.
(5) With stimulus flashes of 1500 msec or
more apart, individual females abruptly and
consistenly changed their response patterns
and latencies. FAA (see Fig. 2) abruptly increased her latency from 700 to 2700 msec to
the second flash of pairs more than 1500 msec
apart. FCC (see Table 2) responded after
both flashes of a pair 1620 msec apart. FFB
(see Table 1) responded to paired stimulus
flashes 2168 msec apart with a latency to the
second of over 2 seconds. The courtship flash
pairs of Photinus macdermotti males are
430
reported as being approximately every 2150
msec at 21?C. Having a female response
latency of over 2 seconds, FFC would attract
but few P macdermottimales, for the conspecific female answers with a latency of 1.5
seconds.
(6) Femmesfatales are entrained to successive flashes at short intervals (400-800 msec)
with latencies of considerable precision, as
shown by the small S.D.s of FFC, Table 2,
part C.
(7) As illustrated in Fig. 2, the response behavior of Photurisversicolorfemales is strongly
affected by the animal's previous flash history, an effect previously observed in Photinus
macdermottifemales (Carlson et al., 1977).
FFA usually responded to flashes more than
1500 msec apart with response latencies of
over 2 seconds. At flash pair 63, an abrupt interval change occurred from 1360 msec to
over 1600 msec, but FFA responded to the
longer interval with a latency of only 1
second.
Summary. PhysiologicalProcesses(Motor,
Sensory, Central)that ControlFirefly Flashing
The picture that emerges from the physiological observations on the control of flash behavior is as follows:
(1) The courtship flash behaviors of fireflies
are controled by neural pattern generators
that produce stereotyped flash communication patterns of minimum ambiguity. These
pattern generators have been perpetuated by
selection and result in unique flash codes that
contribute to the reproductive isolation of
each species. In some species, these pattern
generators can be activated directly by electrical stimulation of the firefly's brain (Bagnoli et al., 1976, in Luciola lusitanica;Case and
Trinkle, 1968, and Carlson and Copeland,
1972, in Photuris).
(2) Fireflies may be programmed to produce only one or a very few flash patterns.
Photinusmacdermottimales are capable of emitting two different flash patterns during different stages of courtship, either rhythmic
flashes during searching or paired flashes
during courtship (Lloyd, 1969b; Carlson et
al., 1976).
(3) Neural priming of flash-pattern generators must occur for the system to operate with
precision. Male fireflies must undergo a
[VOLUME
60
period of neural warmup before properly
shaped flashes (Case and Buck, 1963) and
properly timed flashes (see Table 1) can be
produced. Even in suitably primed males,
random fluctuations at each step in the chain
of flash-excitation processes may degrade the
timing of the signal (see Fig. 1). Furthermore,
female fireflies must be primed to respond to
the correct courtship pattern with the appropriate latency. The level of priming can fluctuate so that behavior is strongly influenced
by the immediately previous flash history
(Carlson et al., 1977, in Photinus macdermotti
females). This effect is most apparent when
females are subjected to sudden changes of
flash pattern (Carlson and Soucek, 1975, for
Photinusmacdermotti;see Fig. 2, for Photurisversicolor).
(4) The ability of fireflies to flash is greatly
influenced by their state of arousal. At low
levels of arousal (flash quiescence during daytime), it is difficult to induce a normal courtship flash (Case and Buck, 1963). We have
observed in addition that highly excited fireflies produce paroxysms of flashes that have
no apparent communicative significance. In
Photuris fireflies, the flash-generating center
appears to be easily activated by noncourtship interference caused by movement
of the animal (Barber, 1951, reported that females flash spontaneously as they are observed walking through the underbrush) or
by undergoing physical manipulation (fireflies flash vigorously when trapped in spider
webs or when handled or restrained, Case
and Buck, 1963).
(5) The firefly's visual apparatus is adapted
to receive and to process flash signals (Lall,
1981; Horridge, 1969). The eyes collect light
through wide visual angles, and the spectral
sensitivity of the firefly's eye closely approximates the emission spectrum of its flash.
(6) The neural pattern generators of some
male and of all female fireflies can be activated by light flashes, so as to result in female
responses of proper latency (Soucek and
Carlson, 1975, in Photinusmacdermotti;Soucek
and Carlson, unpub., in Photuris versicolor)
and in flash synchrony in rival males (Buck,
Buck, Hanson, Mets, and Atta, 1981, in
Pteroptyx;Buck et al., 1982, in Photinuspyralis;
Carlson and Copeland, 1983, in Photinusmacdermottz).Femmesfatalesof Photurisversicolorre-
DECEMBER
1985]
FLASH COMMUNICATION
spond consistently to a wide array of flash
patterns (see Figs. 2 and 3, Tables 1 and 2).
Their response patterns can be interpreted on
the basis of a series of neural time windows
that are susceptible to the memory of previous flashes (Soucek and Carlson, unpub.).
431
criteria. The courtship flashes of Photinus
pyralis and Photinus macdermottimales differ
significantly from the triple-pulsed flash of
Photuris versicolor males. The responses of
femmes fatales to the flashes of heterospecific
males appear more frequently and consistently than purely random flashes (Nelson,
MIMICRY
IN FIREFLIES
Carlson, and Copeland, 1975). However, the
precision of the response latency of femmes
The conversion of females from unmated
to mated (femmefatale)behavior (luminescent,
fatales is questionable (Carlson and Copepostural, and locomotory) by means of an ir- land, unpub.). As illustrated by FFC (see Tareversible mating-induced switch (Nelson,
ble 2), single flashes repeated less often than
once in 5 seconds can induce response latenCarlson, and Copeland, 1975) has been described previously. The mating of females of cies of about 3 seconds. In the field, however,
some Photuris species apparently renders femmesfatales appear to answer at this latency
them no longer responsive to courtship, con(3 sec) less often, and usually respond with a
trary to the effect in Photinusfemales, who will
latency of approximately 1 sec to P pyralis
mate and court on successive evenings (Carlmales (J. Buck, pers. commun.). Responses
son and Copeland, unpub.). Further, Photuris to Photinus macdermotticourtship flashes are
versicolorfemales in the field are eitherfemmes
sometimes emitted correctly after the second
fatales or are simply unresponsive to flashes of courtship flash, but at 20?C such responses
any kind; virtually none are unmated (Zorn
are at highly variable latencies rather than at
and Carlson, 1978). Only by raising females
the 1500 msec characteristic of P macdermotti
from larvae in the laboratory (McLean,
females. As shown in Fig. 2, the latency of reBuck, and Hanson, 1972) could unmated fesponse of FFA to flash intervals longer than
males be obtained that would participate in
1500 msec varied between 2.0 to 2.8 seconds.
courtship with a conspecific male (P ver- FFB (see Table 1) responded with latencies
sicolor,Nelson, Carlson, and Copeland, 1975; longer than 2 seconds to paired flashes that
P lucicrescens, Carlson,
Copeland,
and
mimic the courtship flash period of P macderShaskan, 1982). These laboratory-raised femotti males. In the only direct assessment of
males were tested in both the field and the
the efficiency of Photuris predation, Lloyd
laboratory.
(1979) reported that of 119 Photinus collustrans
What then is female aggressive mimicry in males he followed, none closely approached
fireflies? We feel that to be considered mimor were captured by the many femmesfatales,
icry, the flash responses of Photuris females
but two conspecific females were quickly apshould fulfill at least three criteria. (1) They
proached and mated.
A strong case for aggressive mimicry has
should be produced in response to male
flashes significantly different from those of been made for only three species of Photuris
their own males. This criterion would exfireflies. They are P versicolor(Lloyd, 1965;
clude the apparent mimicry produced by the
Nelson, Carlson, and Copeland, 1975),
P jamaicensis (Farnworth, 1973), and P fairserendipitous overlap of conspecific and hetchildi (Buschman, 1974). The flashes of
erospecific (mimic) courtship codes. While
P pennsylvanica and P lucicrescens males,
the latter might represent a form of mimicry,
whose females are not known to be aggressive
it is not what is usually meant when the conmimics, are of long duration and simple in
cept of aggressive mimicry is discussed
shape, whereas the males of the known ag(Wickler, 1968). (2) The responses should be
produced often enough to be more-than rangressive mimics emit flickering or pulsed
flashes. The P versicolor, P jamaicensis and
dom, spontaneous flashes of unknown comP fairchildi females must, therefore, be able to
municative significance. (3) The responses
should be timed so precisely that they can at- analyze rapid light fluctuations. Perhaps, aftract the heterospecific male.
ter mating, a change within the brain renders
To date, the flash responses of Photuris ver- these fireflies incapable of responding to consicolor femmes fatales fulfill the first two
specific males, but still able to entrain to the
432
simpler flash patterns of heterospecific males.
This, of course, is pure speculation, but it
does point up the importance of rigorously
establishing the response parameters of any
suspected or known aggressive mimic. Until
this is done, the evolutinary implications of
aggressive mimicry for firefly flash codes
must remain uncertain.
SUMMARY
AND
CONCLUSIONS
In summary, firefly communication depends on signal systems coded for timing patterns of flashes. These timing patterns are
produced by insects with relatively simple
sensory and neural equipment that must be
primed in order to function with sufficient
precision. For lack of a better term, we may
say that the firefly's state of arousal must be
sufficiently elevated to enable it to produce
the proper flash patterns.
It is difficult to underestimate the importance of this concept of state of arousal because it is seen in nearly every aspect of firefly
flash behavior. The lanterns of both quiescent
Photuris and Photinus males require considerable neural input before their courtship
flashes can be correctly produced. Much
neural priming is required before Photuris
males can emit their characteristic intensitymodulated courtship flashes and Photinus
males can achieve the correct timing patterns
of their courtship flashes. Photinus females
may be unresponsive or may respond incorrectly during the initial stages of courtship,
but when they become sufficiently aroused
they may become highly discriminating.
The central flash triggering circuits of the
firefly's brain appear to be highly susceptible
to activation during periods of high excitability, and the result is often the production of
flashes of unknown communicative function.
Photuris females, presumably mated, are often seen flashing spontaneously as they walk
through the foliage (Barber, 1951). Fireflies
that are handled, that crash in flight, or that
fly into spider webs flash vigorously.
The timing circuits (pattern generators
and pacemakers) of the firefly's brain have
been studied in a wide array of species. By
means of electrical or photic stimulation, firefly brain circuits have been activated to produce the flash patterns observed in the field
(Luciola lusitanica males, Bagnoli et al., 1976;
[VOLUME
60
Photurisfemales, Case and Trinkle, 1968, and
Carlson and Copeland, 1972). By analyzing
the responses of fireflies to natural or artificial flash patterns, models have been developed that predict firefly flash behavior with
considerable accuracy (synchronously flashing Pteroptyxmales -Buck,
Buck, Case, and
Hanson, 1981; and Photinus macdermottifemales-Soucek and Carlson, 1975). Essential
to the success of these studies has been rigid
experimental control combined with a knowledge of the previous flash history of each animal. All of these considerations point to the
difficulty of analyzing the flashes of fireflies in
the field in situations where these experimental requirements cannot be met.
Given our present understanding of the
physiological control of firefly flash behavior,
questions may be raised concerning the responses of Photurisfemmesfatalesto the flashes
of heterospecific males: do they truly represent mimicry? The responses of these predatory females may simply be too inaccurate to
meet the criteria of mimicry. Flashes presumed to be mimicking may actually reflect
entrainment of neural oscillatory circuits of
femmesfatales to a wide array of different flash
patterns, and the flash responses that result
may have only a superficial resemblance to
the response patterns of other species. The
prey-capturing ability of these flashes of
femmesfatales, such as it is, may therefore only
reflect the wide timing variations in the flash
dialogues of the prey species. The choice between two such possible explanations offemme
fatale behavior can only be made after rigorous experimental examination in which the
response latencies of predatory females to
different flash patterns have been measured
under conditions in which the previous flash
history of each female is known.
The firefly's flash communication system,
in short, is designed to emit pulsed signals in
precise timing patterns that convey courtship
information. The variation observed in these
patterns is the result of normal fluctuations
found in any physiological system. It is possible to misinterpret this variation as being of
functional significance if the observations of
flash behavior are not performed under controlled conditions. Without a knowledge of
the firefly's central excitatory state and previous flash history, it is very difficult to inter-
DECEMBER
1985]
FLASH COMMUNICATION
pret the precise function of the flash behavior
observed.
We think that the study of flash communication in fireflies is really the study of flash
entrainment. Male fireflies entrain to the
flashes of others, so as to produce synchronous flashing by means of different
mechanisms in Photinus macdermottirivalry,
Photinus pyralis rivalry, and Pteroptyx communal flash displays. Photinus macdermottifemales entrain to the rhythmic flashes of Photi-
433
nus macdermottimales. Femmesfatalesof Photuris
versicolorcan entrain to a wide range of counterfeit flash patterns. The study of firefly flash
communication, then, is a study of entrainment, a physiological process. By precisely
defining the limits of the proximal (physiological) mechanisms, we hope eventually to
define the characteristics of the ultimate
(evolutionary) processes: courtship rivalry,
communal flashing, and aggressive mimicry.
REFERENCES
BAGNOLI, P., M. BRUNELLI, F. MAGNI, and D.
MUSUMECI. 1976. Neural mechanisms
under-
lying spontaneous flashing and its modulation
in the firefly Luciola lusitanica.j Comp. Physiol.,
108: 133-156.
BAGNOLI, P., M. BRUNELLI, F. MAGNI and M.
VIOLA. 1972. The identification of a flashinhibiting substance from the male gonads of
Luciola lusitanica (Charp.). Arch. Ital. Biol., 110:
16-34.
BARBER, H. S. 1951. North American fireflies of
the genus Photuris. SmithsonianMisc. Collns., 117:
1-58.
BEAMS, H. W., and E. ANDERSON. 1955. Light and
electron microscope studies on the light organ
of the firefly (Photinus pyralis). Biol. Bull., 109:
375-393.
BIGGLEY, W. H., J. E. LLOYD, and H. H.
SELIGER. 1967. The spectral distribution
of
firefly light. j Gen. Physiol., 50: 1681-1692.
BLUM, M. S., and A. SANNASI. 1974. Reflex bleeding in the lampyrid Photinus pyralis: Defensive
function. j Insect Physiol., 20: 451-460.
BRUNELLI, M., M. BUONAMICI, and F. MAGNI.
1968a. Mechanisms for photic inhibition of
flashing in fireflies. Arch. Ital. Biol., 106: 85-99.
and
. 1968b. Effects of castration
on the inhibition of flashing in fireflies. Arch.
Ital. Biol., 106: 100-112.
BRUNELLI, M., M. BUONAMICI, F. MAGNI and M.
VIOLA-MAGNI. 1970. The role of the male
gonads in the peripheral inhibition of flashing
in Luciola lusitanica. Arch. Ital. Biol., 108: 1-20.
BRUNELLI, M., F. MAGNI, and M. PELLEGRINO.
1977. Excitatory and inhibitory events elicited
by brief photic stimuli on flashing of the firefly
Luciola lusitanica(Charp.). j Comp. Physiol., 119:
15-35.
BUCK, J. B. 1935. Synchronous flashing of fireflies
experimentally induced. Science, 81: 339-340.
. 1937. Studies on the firefly. II. The signal
system and color vision in Photinuspyralis. Physiol. Zool., 10: 412-419.
. 1948. The anatomy and physiology of the
light organ in fireflies. Ann. NY Acad. Sci., 49:
397-482.
BUCK, J., and E. BUCK.
1966. Biology of synchronous flashing of fireflies. Nature, 211:
562-564.
, and
. 1968. Mechanisms of rhythmic
synchronous flashing of fireflies. Science, 159:
1319-1327.
. 1972. Photic signaling in the fire, and
fly, Photinus greeni. Biol. Bull., 142: 195-205.
. 1976. Synchronous fireflies. Sci.
, and
Am., 234: 74-85.
. 1978. Toward a functional in, and
terpretation of synchronous flashing by fireflies. Am. Nat., 112: 471-492.
BUCK, J., E. BUCK,J.
F. CASE, and F. E. HANSON.
1981. Control of flashing in fireflies. V.
Pacemaker synchronization in Pteroptyxcribellata. J Comp. Physiol., 144: 287-298.
BUCK, J., E. BUCK, F. E. HANSON, L. METS, and
G. J. ATTA. 1981. Control of flashing in fireflies. IV. Free run pacemaking in a synchronic
Pteroptyx.J Comp. Physiol., 144: 277-286.
andJ. F. CASE. 1961. Control of flashing
BUCK,J.,
in fireflies. I. The lantern as a neuroeffector organ. Biol. Bull., 121: 234-256.
BUCK, J., J. F. CASE, and F. E. HANSON, JR. 1963.
Control of flashing in fireflies. III. Peripheral
excitation. Biol. Bull., 125: 251-269.
E. BUCK, and J. CASE.
BUCK, J., F. E. HANSON,
1982. Mechanism and function of synchronous
flashing in the firefly Photinuspyralis. Biol. Bull.,
163: 398.
BUONAMICI,
M., and F. MAGNI. 1967. Nervous
control of flashing in the firefly Luciola italica.
Arch. Ital. Biol., 105: 323-338.
L. L. 1974. Flash behavior of a Nova
BUSCHMAN,
Scotian firefly, Photurisfairchildi Barber, during
courtship and aggressive mimicry (Coleoptera,
Lampyridae). Coleopts. Bull., 28: 27-31.
CARLSON, A. D. 1967. Induction of scintillation in
the firefly. J Insect Physiol., 13: 1031-1038.
434
[VOLUME
60
MCCAMAN, and A. D. CARLSON.1983. Pres. 1968a. Effect of adrenergic drugs on the lanence of octopamine in firefly photomotor neutern of the larval Photuris firefly. j. Exp. Biol.,
rons. Neuroscience,9: 183-189.
48: 381-387.
of prey cap. 1968b. Effect of drugs on luminescence in
COPELAND, J. 1980. Neuroethology
ture by larval fireflies: Inhibitory effects of firelarval fireflies. J Exp. Biol., 49: 195-199.
. 1969. Neural control of firefly luminescence.
fly extracts on cardiac function in terrestrial
Adv. Insect Physiol., 6: 51-96.
slug. Neurosci. Abstr., 6: 75.
. 1981. Neural control of the male Photuris ver- COPELAND, J., and H. A. ROBERTSON. 1982. Octopamine as the transmitter at the firefly lansicolor firefly flash. J Exp. Biol., 92: 165-172.
CARLSON, A. D., and J. COPELAND. 1972. Photic
tern: Presence of an octopamine-sensitive and
a dopamine-sensitive adenylate cyclase. Comp.
inhibition of brain stimulated firefly flashes.
Biochem. Physiol., 72C: 125-127.
Am. Zool., 12: 479-487.
. 1978. Behavioral plasticity in the
DELuCA, M., and W. D. McELROY. 1974. Ki, and
netics of firefly luciferase catalysed reactions.
flash communication systems of fireflies. Am.
Biochemistry,NY, 13: 921-925.
Sci., 66: 340-346.
DREISIG, H. 1975. Environmental control of the
. 1983. Male-male interactions and
, and
daily onset of luminescent activity in glowfemale responses in the firefly Photinus macderworms and fireflies (Coleoptera: Lampyridae).
motti. Am. Zool., 23: 299.
CARLSON,A. D., J. COPELAND,R. RADERMAN,
Oecologia, 18: 85-99.
EDMUNDS,
L. E., JR. 1963. The relation between
and A. G. M. BULLOCH.1976. Role of interflash intervals in a firefly courtship (Photinus
temperature and flashing intervals in adult
male fireflies, Photinuspyralis. Ann. Entomol. Soc.
macdermotti).Anim. Behav., 24: 786-792.
Am., 56: 716-718.
. 1977. Response pat)
,~) ~~, and
EISNERT., D. F. WIEMER,L. W. HAYNES, andJ.
terns of female Photinus macdermottifirefly to arMEINWALD. 1978. Lucibufagins: defensive
tificial flashes. Anim. Behav., 25: 407-413.
CARLSON, A. D., J. COPELAND, and R. SHASKAN.
steroids from the fireflies Photinus ignitus and
1982. Flash communication between the sexes
P marginellus (Coleoptera: Lampyridae). Proc.
of the firefly, Photuris lucicrescens.Physiol. EnNat. Acad. Sci., US.A., 75: 905-908.
EVANS,P. D., and M. O'SHEA. 1977. The identifitomol., 7: 127-132.
CARLSON,A. D., and B. SOUCEK.1975. Computer
cation of an octopaminergic neuron which
simulation of firefly flash sequences. J Theor.
modulates neuromuscular transmission in the
locust. Nature, 270: 257-259.
Biol., 55: 353-370.
CASE, J. F. 1980. Courting behavior in a synFABRE, J. H. 1919. The Glow-wormand OtherBeetles.
chronously flashing, aggregative firefly, PteropDodd, Mead and Company, New York.
E. G. 1973. Flashing behavior, ecolFARNWORTH,
tyx tener.Biol. Bull., 159: 613-625.
. 1984. Vision in mating behavior of fireflies.
ogy and systematics ofJamaican lampyrid fireIn T. Lewis (ed.), Insect Communication, p.
flies. Ph.D. Dissertation,
Univ. Florida,
195-222. Royal Entomological Society of LonGainesville.
H. 1977. Fine structure of the
don, London.
GHIRADELLA,
CASE,J. F., and J. BUCK. 1963. Control of flashing
tracheoles of the lantern of a Photurid firefly.
in fireflies. II. Role of central nervous system.
J. Morphol., 153: 187-204.
Biol. Bull., 125: 234-250.
. 1978. Reinforced tracheoles in three firefly
CASE,J. F., and L. STRAUSE.1978. Neurally conlanterns: Further reflections on specialized
trolled luminescent systems. In P. Herring
tracheoles. j Morphol., 157: 281-300.
(ed.), Bioluminescencein Action, p. 331-366. Aca. 1983. Permeable sites in the firefly lantern
demic Press, New York.
tracheal system: Use of osmium tetroxide vaCASE, J., and M. S. TRINKLE. 1968. Lightpor as a tracer. j Morphol., 177: 145-156.
inhibition of flashing in the firefly, Photuris misGREEN, J. W. 1956. Revision of the nearctic spesouriensis. Biol. Bull., 135: 476-485.
cies of Photinus (Lampyridae: Coleoptera). Proc.
CHANG,J. J. 1956. On the similarity of response
Calif. Acad. Sci., 78: 561-613.
of muscle tissue and of lampyrid light organs.
C. H., T. A. HOPKINS, and J. BUCK.
HANNA,
1976. Peroxisomes of the firefly lantern. J
J Cell. Comp. Physiol., 47: 489-492.
Ultrastr. Res., 57: 150-162.
T. A., and A. D. CARLSON. 1981.
CHRISTENSEN,
HANSON, F. E. 1962. Observations on the gross inSymmetrically organized dorsal unpaired median (DUM) neurones and flash control in the
nervation of the firefly light organ. J Insect
male firefly, Photuris versicolor.J Exp. Biol., 93:
Physiol., 8: 105-111.
133-147.
. 1978. Comparative studies of firefly
T. A., T. G. SHERMAN, R. E.
CHRISTENSEN,
pacemakeres. FederationProc., 37: 2158-2164.
DECEMBER
1985]
FLASH COMMUNICATION
J. F. CASE, and A. T. BARNES.
1972. Mechanism of flash synchrony in Malaysian fireflies. Am. Zool., 12: 682.
HANSON, F. E., J. F. CASE, E. BUCK and J. BUCK.
1971. Synchrony and flash entrainment in a
New Guinea firefly. Science, 174: 161-164.
HANSON, F. E., J. MILLER, and G. T. REYNOLDS.
1969. Subunit coordination in the firefly light
organ. Biol. Bull., 137: 447-464.
HARVEY, E. N., and R. T. HALL. 1929. Will the
adult firefly luminesce if its larval organs are
entirely removed? Science, 69: 253-254.
HESS, W. N. 1920. Notes on the biology of some
common lampyridae. Biol. Bull., 38: 39-76.
. 1922. Origin and development of the lightorgans of PhoturispennsylvanicaDeGeer. J Morphol., 36: 245-277.
HOPKINS, T. A., and C. H. HANNA. 1972. Intracellular localization of the luminescent system
of the firefly. Physiologist, 15: 171.
HORRIDGE, G. A. 1969. The eye of the firefly Photuris. Proc. R. Soc. London, Ser. B, 171: 445-463.
HOYLE, G. 1975. Evidence that insect dorsal unpaired median (DUM)
neurons are octopaminergic. J Exp. Zool., 193: 425-431.
HOYLE, G., D. DAGAN, B. MOBERLY, and W.
COLQUHOUN. 1974. Dorsal unpaired median
insect neurons make neurosecretory endings
on skeletal muscle.J. Exp. Zool., 187: 159-165.
T. 1965. Ecological and biological
KAUFMANN,
studies on the west African firefly Luciola discicollis (Coleoptera: Lampyridae). Ann. Ent. Soc.
Am., 58: 414-426.
KLUSS, B. C. 1958. Light and electron microscope
observations on the photogenic organ of the
firefly, Photurispennyslvanica,with special reference to the innervation. J Morphol., 103:
159-186.
LALL, A. B. 1981. Electroretinogram and the special sensitivity of the compound eyes in the firefly Photuris versicolor (Coleopterea: Lampyridae): A correspondence
between
green
sensitivity and species bioluminescence emission. J Insect Physiol., 27: 461-468.
LALL, A. B., R. M. CHAPMAN, C. 0. TROUTH,
and J. A. HOLLOWAY. 1980. Spectral mechanisms of the compound eye in the firefly Photinus pyralis (Coleoptera: Lampyridae). J Comp.
Physiol., 135: 21-27.
LALL, A. B., H. H. SELIGER, W. H. BIGGLEY, and
J. E. LLOYD. 1980. Ecology of colors of firefly
bioluminescence. Science, 210: 560-562c.
LLOYD, J. E. 1965. Aggressive mimicry in Photuris:
fireflyfemmesfatales. Science, 149: 653-654.
. 1966a. Studies on the flash communication
system in Photinus fireflies. Univ. Michigan Mus.
Zool. Misc. Publ., No. 130: 1-96.
. 1966b. Two cryptic new firefly species in the
HANSON, F. E.,
435
genus Photinus (Coleoptera:
Lampyridae).
Coleopt. Bull., 20: 43-46.
. 1968. Illumination, another function of firefly flashes. Entomol News, 79: 265-268.
. 1969a. Flashes of Photuris fireflies: their
value and use in recognizing species. Fla. Entomol., 52: 29-35.
. 1969b. Flashes, behaviour and additional
species of Nearctic Photinusfireflies (Coleoptera:
Lampyridae). Coleopt. Bull., 23: 29-40.
. 1973a. Firefly parasites and predators.
Coleopt. Bull., 27: 91-106.
. 1973b. Fireflies of Melanesia: Bioluminescence mating behavior, and synchronous flashing. Environ. Entomol., 2: 991-1008.
. 1979. Sexual selection in luminescent beetles. In M. Blum and N. Blum (eds.), Sexual Selection and ReproductiveCompetition in Insects, p.
293-342. Academic Press, New York.
. 1980. Male Photuris fireflies mimic sexual
signals of their females' prey. Science, 210:
669-671.
. 1981a. Firefly mate-rivals mimic their predators and vice versa. Nature, 250: 498-499.
. 1981b. Mimicry in the sexual signals of fireflies. Sci. Am., 245: 138-145.
. 1983. Bioluminescence and communication
in insects. Annu. Rev. Entomol., 28: 131-160.
. 1984. On deception, a way of all flesh, and
firefly signalling and systematics. In OxfordSurveysin EvolutinaryBiology, Vol. 1, 49-84. Oxford
University Press, Oxford.
LLOYD, J. E., and S. R. WING.
1983. Nocturnal
aerial predation of fireflies by light-seeking
fireflies. Science, 222: 634-635.
MAGNI,
F. 1967. Central and peripheral mechanisms in the modulation of flashing in the firefly Luciola lusitanica L. Arch. Ital. Biol., 105:
339-360.
F. A. 1910-1917. Observations on
McDERMOTT,
the light-emission of American Lampyridae.
Can. Entomol., 42: 357-363, 1910; 43: 399-406,
1911; 44: 73, 309-312, 1912; 49: 53-61, 1917.
1958. The Fireflies of Delaware. Society on
Natural History, Wilmington.
. 1964. The taxonomy of the lampyridae
(Coleoptera). Trans.Am. Entomol. Soc., 90: 1-72.
1978. ChemMcELROY, W. D., and M. DELuCA.
istry of firefly luminescence. In P. Herring
(ed.), Bioluminescencein Action, p. 109-127. Academic Press, New York.
. 1981. The chemistry and applications of firefly luminescence. In M. DeLuca and W. D.
McElroy (eds.), Bioluminescenceand Chemiluminescence:Basic Chemistry and Analytical Applications, p. 179-186. Academic Press, New York.
McLEAN,
M., J. BUCK, and F. HANSON. 1972.
Culture and larval behavior of photurid fire-
436
flies. Am. Midl. Nat., 87: 133-145.
J. A. 1979. Octopamine receptors,
adenosine 3', 5'-monophosphate, and neural
control of firefly flashing. Science, 203: 65-68.
NATHANSON, J. A., and E. J. HUNNICUTT. 1979.
Neural control of light emission in Photurislarvae: identification of octopamine-sensitive
adenylate cyclase. J Exp. Zool., 208: 255-262.
NELSON, S., A. D. CARLSON, and J. COPELAND.
1975. Mating induced behavioral switch in female fireflies. Nature, 255: 628-629.
NEUWIRTH, M. 1981. Ultrastructure of granules
and immunocytochemical localization of luciferase in photocytes of fireflies. Tissue Cell.,
13: 599-608.
OERTEL, D., andJ. F. CASE. 1976. Neural excitation of the larval firefly photocyte: slow
depolarization possibly mediated by a cyclic
nucleotide. J Exp. Biol., 65: 213-227.
OHBA, N. 1983. Studies on the communication
system of Japanese fireflies. Sci. Rep. Yokosuka
City Mus., No. 30: 1-62.
OHLY, K. P. 1975. The neurons of the first synaptic region of the optic neuropil of the firefly,
Phausis splendidula, L. (Coleoptera). Cell. Tiss.
Res., 158: 89-109.
OTTE, D. 1972. Simple vs elaborate behavior in
grasshoppers: An analysis of communication in
the genus Syrbula. Behaviour, 42: 291-322.
. 1980. Notes and comments on theories of
flash synchronization in fireflies. Am. Nat., 116:
587-590.
PAPI, F. 1969. Light emission, sex attraction and
male flash dialogues in a firefly, Luciola lusitanica (Charp.). Monitore Zool. Ital., 3: 135-184.
PETERSON, M. K. 1970. The fine structure of the
larval firefly light organ. J Morphol., 131:
103-116.
ROBERTSON, H. A., and A. D. CARLSON. 1976.
Octopamine: presence in firefly lantern suggests a transmitter role. J Exp. Zool., 195:
159-164.
SCHWALB, H. H. 1961. Beitrage zur Biologie der
einheimischen Lampyriden Lampyris noctiluca
Geoff. und Phausis splenidula. Lec., und experimentelle Analyses ihres Beutfang- and Sexualverhaltens. Zool. Jb. Syst., 88: 399-550.
SELIGER, H. H., J. B. BUCK, W. G. FASTIE, and
W. D. McELROY. 1964. The spectral distribution of firefly light. J Gen. Physiol., 48: 95-104.
NATHANSON,
[VOLUME
60
SELIGER, H. H., A. B. LALL, J. E. LLOYD, and
W. H. BIGGLEY. 1982a. The colors of firefly
bioluminescence. I. Optimization model. Photochem. Photobiol., 36: 673-680.
and
. 1982b. The colors of
firefly bioluminescence. II. Experimental evidence for the optimization model. Photochem.
Photobiol., 36: 681-688.
SELIGER, H. H., and W. D. McELROY. 1960.
Spectral emission and quantum yield of firefly
bioluminescence. Arch. Biochem. Biophys., 88:
136-141.
SIVINSKI, J. 1981. The nature and possible functions of luminescence in Coleoptera larvae.
Coleopt. Bull., 35: 167-179.
SMALLEY, K. N. 1965. Adrenergic transmission in
the light organ of the firefly, Photinus pyralis.
Comp. Biochem. Physiol., 16: 467-477.
SMALLEY, K. N., D. E. TARWATER, and T. L.
DAVIDSON. 1980. Localization
of fluorescent
compounds in the firefly light organ. J
Histochem. Cytochem.,28: 323-329.
SMITH, D. S. 1963. The organization and innervation of the luminescent organ in a firefly, Photurispennsylvanica(Coleoptera). J Cell Biol., 16:
323-359.
SOUCEK, B., and A. D. CARLSON. 1975. Flash pattern recognition in fireflies. J Theor. Biol., 55:
339-352.
STRAUSE, L. G., and M. DELuCA. 1981. Characteristics of luciferases from a variety of firefly
species: Evidence for the presence of luciferase
isozymes. Insect Biochem., 11: 417-422.
STRAUSE, L. G., M. DELUCA, and J. F. CASE.
1979. Biochemical and morphological changes
accompanying light organ development in the
firefly, Photuris pennsylvanica. J Insect Physiol.,
25: 339-347.
VERNON, C. L. 1983. The use of vision in prey selection by the big brown bat, Eptesicusfuscus.M.
S. Thesis, University of Wisconsin-Milwaukee.
WICKLER, W. 1968. Mimicry in Plants and Animals.
World University Library, McGraw-Hill Book
Co., New York.
WILLIAMS, F. X. 1917. Notes on the life history of
some North American Lampyridae. J N. Y
Entomol. Soc., 25: 11-33.
ZORN, L. P., and A. D. CARLSON. 1978. Effect of
mating on response of female Photuris fireflies.
Anim. Behav., 26: 843-847.

Flash Communication in Fireflies

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