© 2004 by The Society for Integrative and Comparative Biology
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Flight Studies on Photic Communication by the Firefly Photinus pyralis1
1 Marine Science Institute, University of California Santa Barbara, Santa Barbara, California 93106-6150
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Flash communication by the firefly Photinus pyralis was studied in a stationary, simulated flight apparatus in which an individual of either sex could be "flown" and its flashing behavior and flight orientation recorded in response to photic stimulation. Males made long "flights" showing many of the characteristics of their natural, female-seeking patrol flights. Males oriented their flight vectors towards light emitting diode (LED) flashes that mimicked the responses of females to their patrol flashes. Females flew and responded to male-emulating LED flashes, making a previously unknown early response followed by the typical 2 sec delayed response characteristic of the dialoging perched female, including abdominal aiming of the flash. Pairs consisting of males, in tethered flight, and females, perched, were run in an integrating sphere photometer, permitting the first determinations of flash intensities of both sexes during courtship dialog. The implications of this work on thought about evolution of photic behavior in fireflies are considered.
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INTRODUCTION |
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This contribution to the symposium honoring John and Elisabeth Buck has relevance if only because its germinal event occurred in their laboratory at the National Institutes of Health. There, working with Frank Hanson and Tamara Frank, a male Photinus pyralis was flown attached to a restraint of John Buck's invention, which was a response to a suggestion by Jonathan Copeland. This pioneering firefly was seen to turn its head in the direction of a LED-generated answer to its patrol flash (Buck, 1990
). The possibilities were immediately apparent. Heretofore inaccessible aspects of firefly dialog communication were thrown open to study in the laboratory, making possible greater precision and experimental scope than is generally attainable in the field (Lloyd, 1997a, p. 190).
Insects, from fruit flies to desert locusts, have been flown in instrumented wind tunnels, in tethered simulation of flight, for study of flight mechanics and energetics, or for investigation of visual and olfactory behavior (Dudley, 2000, p. 84). The technique appears not to have been applied to firefly communication after Buck's initial study of 1990. Therefore, in this report the first priority is to establish the extent to which normal male patrol communication behavior is attainable in our flight simulation apparatus, which evolved from Buck's. Then details of courtship flight orientation as revealed in the apparatus are reported, followed by the discovery and analysis of flight luminescent behavior of the female. Flights of males communicating with females in an integrating sphere allowed the first determination of emission intensities during such behavior. Finally, these observations are related to some aspects of the evolution of firefly communication.
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Experimental organisms
Photinus pyralis fireflies, principally from western Pennsylvania, were studied in July 1997 and 1998. Fireflies were lightly anaesthetized with CO2 gas for approximately two minutes while a balsa wood stub was attached to the broad, head-covering pronotum of each insect with Loktite 447 cyanoacrylic glue. Care was taken not to interfere with a full range of wing or head movement (Fig. 1). The stubs were attachment points for connecting the insect to the pivot of a flight direction encoder and were useful for grasping with forceps while handling the insects.
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Fireflies were housed individually in screw-capped 50 cc plastic tubes and kept in a constant temperature room at 22°C on a 12:12 light cycle. They were given dilute sucrose in water applied to filter paper strips, upon which both sexes fed avidly. Fireflies were exercised daily by letting them run and by lifting them by their stubs for brief flight activity. Insects bearing stubs functioned well, each typically flying in several experiments over about 10 days, but some could still fly at 30 days. There is a large size range in adults of both sexes, from about 12 to 18 mm total length, in our experience, and as reported in detail for P. pyralis from Long Island, New York, by Vencl and Carlson (1998)
. Only insects 14 mm and larger were used in the present experiments to simplify handling. Mite infestations were seen occasionally (Lloyd, 1997b). Infested fireflies were not used although they seemed to fly and communicate well enough. Flight experiments were by far most successful at the beginning of twilight, but day-phase insects performed well after about an hour of artificial twilight. Lifting a firefly into the air by its balsa stub at any time, day or night, nearly always triggered flight accompanied by ejection of a droplet of clear excreta, perhaps a reflex to economize flight weight. Females flew as readily as males, which was surprising because females, often heavily laden with eggs, were rarely seen flying in nature, except occasionally in early twilight as they moved to their display sites (Lindsey, personal communication). Due to the method of collecting it was impossible to know if the females tested were mated or not.
Flight apparatus and general experimental procedures
The flight apparatus was set up on a Newport air table in a temperature and light controlled room (Fig. 2). Minimal diffuse visible light was provided as a necessary flight stimulus. A firefly was attached by its balsa stub to the recording pivot of the flight direction encoder. This pivot was the freely rotating axis of a custom-built variable capacitor for sensing flight direction. After attachment to the pivot, the firefly was given moist filter paper or a balsa stick to manipulate as a flight suppressant before starting an experiment. A LabVIEW (National Instruments) program running on various Macintosh computers controlled most experiments and collected data from the system sensors including: (1) Hamamatsu H5783 photomultipliers (PMT) with integrated power supplies and signal conditioning to monitor firefly flashing and photic stimuli, (2) the firefly heading recorder, (3) wingbeat frequency microphone, (4) Kurz anemometer, and (5) three green LEDs (Zicor 351-5003, 565 nm peak) delivering flashes through glass neutral density filters to the experimental insect. Insects were viewed with an infrared sensitive Sony XC-77/77ce CCD video camera with IR filter removed and equipped with a lens delivering up to 5x magnification. Illumination was from one or more infrared LED strobe arrays, each consisting of a set of 144 Siemens SFH485 IR LEDs firing once per video frame at adjustable durations of between 10 and 30 µs. IR illumination was necessary because sufficient visible light to detect head movements and other behavioral details interfered with communication behavior. Video recordings of flight behavior were time-correlated with the LabVIEW data stream.
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In a typical experiment the male firefly flew spontaneously, or with brief air puff encouragement, and settled immediately into steady flight into the wind. For experimental convenience the wind was adjusted to the least velocity that would cause the firefly to fly upwind unless orienting to a LED stimulus. In the absence of LED stimulation a firefly male intermittently produced trains of patrol flashes. Once a male was flying steadily and making patrol flashes at the temperature dependent interval of 6 to 7 sec, experiments typically began by starting LED-generated female-emulating response flashes at the species specific 2 sec reply delay after the male flash. These were from one or more of the three green LEDs controlled by the system program and positioned at firefly eye height as shown in Figure 2. The female-emulating LED response pulse duration and delay after the male's flash were controlled through the LabVIEW program while the response intensity was regulated by glass neutral density filters. The LED pulse shape was square with virtually instantaneous rise and decay. P. pyralis males and females responded well to square pulses of durations from 0.2 to 3.5 sec, both in the laboratory and in the field.
Experiments on males emphasized reactions to change in the number of female-emulating LEDs active and their response delay, duration, intensity and orientation to the flight axis. With females the response character was dependent on whether or not they were flying. To accommodate to this a polished glass landing platform positioned by a micromanipulator was used to interrupt or initiate flight by precise control of tarsal contact.
Integrating sphere radiometry
To precisely measure light emitted by a non-isotropic emitter such as the nearly flat firefly lantern, measurements were made in a custom-built 26 cm diameter integrating sphere PMT photometer calibrated with a secondary light standard referenced to a National Institute of Standards and Technology standard. Males flew with their stubs attached to a centered post in the integrating sphere and non-flying females were perched in view of them. The sphere PMT was baffled so that light emitted in any direction inside the sphere was recorded indirectly after one or more reflections from the inner sphere surface. Since the females are reluctant to communicate in total darkness (Case and Trinkle, 1968) the sphere interior was illuminated with minimal light sufficient to sustain flashing (Fig. 3), and this was subtracted in data analysis. In experiments now in progress it has been discovered that females will respond normally to LED flashes in the completely dark integrating sphere for somewhat less than half an hour when tested immediately after exposure to an hour of twilight at any time of day. The males were positioned in the sphere facing into a low flow of compressed air from 2 mm diameter tubing to encourage more continuous flying.
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Flight force measurements
The rearward force generated by flying males was compared with the force required to turn the pivot in order to determine if mechanical resistance from the direction indicator pivot might impede changes of flight direction. Male fireflies were flown attached to a Grass Instruments force displacement transducer (FT03) recording to a Grass Polygraph. Females were not tested because they do not change flight heading in the apparatus, spontaneously or in response to a LED flash.
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RESULTS |
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Evidence for normal male flight behavior in the flight apparatus
The force of the propulsive effort along the forward flight axis for 5 males measured from 20 to 30 mg while 2 mg similarly applied to the horizontally oriented direction indicator pivot caused free rotation, indicating that the resistance to turning by the pivot did not impede change of direction in flight (Fig. 4). The same polygraph data on flight restarts by air puffs indicated that about 2 sec was required to develop measurable flight force (Fig. 4, inset). The time constant of the force transducer permitted an estimate of wingbeat frequency at about 65 Hz at 22°C which was comparable with routine measurements by acoustics via the LabView program or by direct display of the microphone signal on a storage oscilloscope. The low frequency tone emitted in flight is plainly audible to the ear and microphonic filtering yielded the wing beat frequency, as Sotavalta (1952)
reliably showed for many insect species.
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Patrol flight posture was ascertained by video and 35 mm still photography (see also, McDermott, 1954
) in the field (Fig. 5) and compared with attitude in the flight apparatus. Leg and antenna positions in the field observations were identical to those seen in the flight apparatus. In flight the antennae were held stiffly forward and all legs were elevated and flexed towards the body, rarely moving until landing. This characteristic posture was required for continuation of an experiment because leg motion and rapid antenna movement seemed to indicate intent to land. While the antennae of experimental insects were in active motion in the apparatus before flight started, as soon as the insect signaled intent to fly by raising the elytra, the antennae extended forward stiffly, the insect dropped its flight inhibiting "pacifier" and began flying. The curious, nearly vertical body orientation of the patrolling male was approximated in the flight apparatus by attaching the insect's balsa stub to the recording pivot at an angle. Presumably this flight posture represents the near-stall flight that might be necessary to remain airborne at the slow, frequently almost hovering, rate of forward movement during patrol flight. This was not measured but was slow enough to permit walking beside the insect and taking photographs as it flew across a lawn.
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Patrol flight flashing typically involves a J-shaped upward swooping flight pattern while the flash is emitted. In the flight apparatus, even though vertical motion is not possible, a male in patrol flight changed wing stroke amplitude in correlation with the patrol flash. As the flash was in progress the wings made only half dorso-ventral strokes that seemed correlated with what in nature would be the climb part of the luminous J (Fig. 6A). Half-strokes did not occur during a second type of male in-flight flashing behavior, the male-male interaction flash, which lacks the upwards swoop in nature as well as half-strokes in tethered flight (Fig. 6C). Thus the half-strokes observed in the flight apparatus suggest that the laboratory tethered firefly was attempting normal patrol flight behavior.
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Patrol flight behavior
Normal patrol flights in nature commence at early dusk while ambient light is easily bright enough for reading. The flight activity period lasts about 45 minutes although perched females continue responding to artificial light flashes for somewhat longer. In one laboratory flight series 25 males flew continuously for a total of 7:52:00 hr (range = 0:06:53 to 0:48:57 hr; average flight duration = 0:18:11 hr). These durations are conservative because some records began after flight was well in progress. The longest flight recorded in both summers of the work was 49 minutes, for one individual among approximately 200 insects that flew for more than a few minutes. Except for this one individual, no fireflies were flown to exhaustion because each could be immediately restarted by an air puff after completing the measured flight. Without receiving any female responses, members of this group of 25 emitted 2,287 flashes of which 997 were considered patrol flashes, that is, sets of at least two flashes separated by 6 sec (Fig. 7).
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Flash intensity during patrol flights in the standard flight apparatus could not reliably be measured so the integrating sphere was brought into play. Successful measurements were obtained from three pairs of insects. Each pair consisted of a male flying on a stub and communicating with a perched female about 10 cm below and 5 cm to one side. This permitted estimation of the interplay of flash intensity during effective communication flights (Fig. 8). While the flash of the female was dimmer than the male's, the nearly ten to one difference in lantern area between the sexes means that the emission per unit area was slightly higher for the female than for the male.
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Flight orientation of the male
A male flying before acquiring a LED respondent frequently turns its head laterally, briefly shifting gaze in a wide arc to each side of the longitudinal body axis, even if not flashing. Its gaze also shifts to observe dark targets passing in front of the insect. When a patrol flash series elicited a first female dialog response (2 sec delay), the male's gaze immediately shifted in one precise movement to the heading of the response within the limits of lateral head movement. The abdomen often twisted to aim the light organ in the response direction before the male's next flash. The second flash of the male to the new source was almost invariably delivered with both head and body aimed at it; thus shifting to the heading of the new respondent by 0 to 90° occurred in less than 4 to 5 sec. A video example of this behavior is available at: http://lifesci.ucsb.edu/~biolum.
Once settled into dialog with the LED source, a male could be shifted to a differently positioned LED source by the first flash falling within the male's receptive timing window. Gaze and usually abdominal redirection accompanied his turn to the new source. After shifting and stabilizing on a new source, he typically turned back at least briefly to the old heading over the next few minutes, even if the LED for that heading remained inactive. While indicating significant short term memory, the occasional return to an old heading might possibly be induced by the fact that the flight apparatus does not cause the new target to loom larger, suggesting relative inaccessibility.
Male-male interaction flashes
In the field, male-male interaction flashes are common, often resulting in a brief and crude synchrony when enough males are in flight for a number of them to be in close proximity during the early sensitive period of the male patrol flash cycle (Case, 1984; Buck 1938, 1988). The male-male reaction time was about 350–400 msec (Fig. 9A) and it was never accompanied by gaze shift or a change in heading. Male-male interactions were readily triggered by a LED flash in the early sensitive period, or at any time if the insect was not spontaneously flashing during the normal period of patrol behavior. Such an exchange has an alerting effect, often causing a previously silent flying male to recommence patrol flashing.
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Female flight behavior
Females flew readily in the apparatus but made shorter flights than the males, rarely exceeding 4 to 5 minutes, though in most cases they could immediately be restarted by an air puff. Females in simulated flight responded to LED-generated male signals with latencies only about 0.12 sec longer than when perched (2.04 sec vs. 1.92 sec) at 25°C. There was never a change in flight direction or gaze. Surprisingly, in flight the female's normal 2 sec delay response was accompanied by the abdominal aiming shift characteristic of a responding perched female.
Most remarkably, nearly every tested flying female commonly emitted early response flashes of about 400 msec latency from the rise of the male LED flash and without significant effect on the normal-latency response flash (Fig. 9B). These early flashes have never been seen in females, flying or perched. Typically the complete simulated flight response of females involved both the early and normal delay flashes accompanied by an abdominal twist. A video example of this behavior can be found at http://lifesci.ucsb.edu/~biolum.
The early response stopped immediately when flight was arrested by touching the feet of the female to a micromanipulator-positioned glass slide. However, a dialog in progress could continue with an unbroken series of normal 2 sec delay responses in spite of the immediate cessation of early responses. If flight was then induced by lowering the glass slide to break tarsal contact, the early flash could resume while the normal 2 sec delay flashes, responsive to the unbroken series of male LED patrol flashes, continued without interruption.
In one instance a female was landed with the glass platform accidentally tilted, causing her to attempt to walk up the incline instead of standing quietly. The early responses, as usual, stopped immediately when flight ceased and the 2 sec responses continued without interruption. This female continued walking in place but halted just before a patrol flash was due, replied to it with an aimed flash, and then resumed walking. This behavior continued for 11 exchanges. While these data are meager, the implication is worth pursuing, namely that a female engaged in dialog might be measuring time accurately enough to be on the alert for the next flash in an ongoing dialog with a specific individual and might even reply to it preferentially with respect to other males in the vicinity.
Photic "noise" and the female response
While the perched and even the flying female tended to aim her response in the general direction of the male's flash, in both response modes the female was easily dissuaded from responding by even one secondary flash from a radically different vector so long as it was not nearly simultaneous with the primary male signal. In nature, this behavior in the presence of competing non-synchronized males must frequently interrupt communication with the female and has been offered as favoring evolution of male-male synchrony (Buck, 1935).
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Adequacy of the flight apparatus
Lack of an interactive visual surround limits the value of the flight simulation apparatus. An attempt was made to provide this with a display of contrasting shapes on a flat CRT scrolled at controlled rates in any direction. There was no perceptible reaction to this display when presented either below or to one side of the flier, perhaps because it occupied less than half of the visual field, the remainder of which was unvaried and necessarily visible to the firefly owing to the twilight requirement for optimal communication behavior. There could be no improvement on this with the existing setup, thereby denying access to important aspects of flight orientation. Among these, because it patrols exclusively at dusk, it seems probable that the P. pyralis male, with its huge eyes with screening and visual pigments optimized to dusk (Cronin et al., 2000
; Lall et al., 1980a, b), exploits its still well-illuminated visual surround in flight orientation. It would seem a waste of sensory resources for the orienting male to simply aim for the last female response seen without correcting flight heading continuously on the basis of change in the surrounding scene. This same consideration impacts other experiments conducted in this study because the orienting male was likely to be aware from the fixed visual surround that headway was not being made towards the target LED. Presumably the firefly CNS is sufficient to cope with such unproductive behavior, but still it is surprising how long males did tend to persist on a particular heading after female responses were deliberately abolished in the flight simulation apparatus. On one occasion flight persisted 47 minutes with only small changes in heading and with the male making patrol flashes only rarely throughout. Such behavior seems counterproductive because even rudimentary optimal search logic suggests that after losing communication with a female the male would search back over its recent course, where a female had been demonstrably present, rather than flying on into unknown territory. This adherence to a specific and unproductive course seems the more strange because, even in the experimental setup there is a tendency of males actively engaged in communicating with a LED to return to a previous productive heading, particularly after unsuccessfully conducting a long dialog in which the female LED grew no closer. In experiments not presented here males favored the brighter of two simultaneously presented targets.
Visual searching
A question as to why head-scanning visual search before acquiring a female flash response is necessary emerges from the fact that the eye of the male is large relative to body size and is virtually spherical. It has a surface area of 8.9 mm2 (avg. of 5 large specimens) based on the greatest diameter measurable in the intact insect. Thus each eye potentially views a significantly duplicate volume ahead and has a large monocular field of view laterally. Because of the curvature of the eyes and their close juxtaposition, anterio-medial blockage by the head is small. Therefore, the question about head scanning might be answered if the shifting gaze search implies vision specialized for distance, possibly even binocular, distance resolving viewing, in the anterior central portion of each eye. While such an adaptation might not facilitate directly ranging on a punctate flash, it should aid navigation through the surrounding vegetation and other obstacles to reach her. This speculation is open to the criticism that in nature the male frequently has difficulty navigating the last few centimeters to reach the female. If he alights on the wrong blade of grass even in plain sight of the targeted female on another, the problem often seems insurmountable. None the less, the idea that the size of the eye of the male is an adaptation to navigation and distance search is bolstered by the small surface area of the eye of the female (2.64 mm2 avg. of 5 large females), because females rarely fly and have only to aim their replies in the general direction of the male flash.
Abdominal aiming of the light organ
Abdominal aiming or torsion during male orientation in the flight apparatus might well be an artifact of the pivot mounting which restricts movement to the horizontal plane, thus inhibiting banking turns and perhaps resulting in attempts to compensate by shifting the center of balance with abdominal movement. However, abdominal aiming is known in males of other firefly species. For example, perched displaying males of the synchronous flashing Pteroptyx tener and the aggregative and probably loosely synchronous Pt. valida (Case, personal observations) rotate the abdomen outwards from the display, presumably to maximize the attraction of the communal display to nearby females. In the extreme of such photic persuasion the male P. tener, perched on the back of the female, contorts his abdomen to project its light directly into the eyes of the female immediately before copulating (Case, 1980).
Abdominal aiming of flashes by the flying female of P. pyralis is most curious and its directional precision cannot be determined from existing data. The timing of the 2 sec delay flash in the flying female is delayed about 100 msec by her early flash (Buck and Case, 2001). Dissociation of twitch and flash occurs with twitches occurring without flashes, indicating, as one would expect, separate neural pathways for light organ and somatic muscle control.
Photic "noise"
Abolishment of 2 sec delay responses to male signals by perched or flying females caused by non-simultaneous flashes from radically different directions suggests that the visual system of the female firefly is organized to emphasize light sensing at the expense of spatial visual acuity. Similar behavior is seen in Photinus greeni (Buck and Case, 1986) and Pteroptyx tener (Case, 1984, p. 216). While there is no direct physiological evidence on this matter in fireflies, the idea is plausible since the communicating task of the female P. pyralis requires only minimal spatial discrimination. She needs only to detect a structureless point of light, aim her reply in 2 sec in its general direction and await further developments. The aim of her reply is basically right or left of her midline with no gradation beyond that. However, she does reply to simultaneous flashes from left and right with preference to the flash on a vector closest to straight ahead (Case, unpublished). Somewhat the same is true of the male P. tener that must only maintain synchrony with nearby and usually surrounding males and interact with females only when they approach closely (Case, 1980).
Moiseff (2003) presents an interesting case in Photinus carolinus, a North American synchronizer, in which synchrony failed when two pacemaking LEDS went out of synchrony. This was taken to be evidence of "jamming."
While evidence from fireflies is sparse, there is some physiological evidence bearing on this matter in the deep ocean where organisms see bioluminescence typically at a distance against a featureless background. In that unforgiving environment detection of luminescence at the maximum possible distance, even at the expense of detailed visual spatial resolution, is argued to have survival value. In most instances the luminescence has no structural detail of importance and quite probably is generated by a predator-prey encounter because spontaneous luminescence in the deep-sea is rare (Widder, 2002). The luminescent mysid shrimp Gnathophausia ingens falls into this category because its visual fields mapped from single units in the eyestalk are quite large, and, in common with many other deep-sea forms, its eyes are so light sensitive as to be damaged by brief exposure to surface moonlight (Moeller and Case, 1994).
Evolutionary significance
Buck (1990) intended to "examine the speculation that duplicate circuits in conspecific male and female fireflies hark back to a stage in dialog evolution in which both sexes flashed alike"(p. 94). The matter remains of interest, at least in some quarters (Buck and Case, 2002), and this report adds another example to this speculation in the form of the in-flight, early response of the P. pyralis female. The latency of this response is close to the male-male excitation flash delay and both are probably virtually indistinguishable from the minimum brain to light organ conduction time. This further addition to early flashes in both sexes argues for the possibility that the most plausible ancestral firefly flashing behavior was alarm flashing in all life stages, giving way to, or including later, a similarly timed aggregation signal shared by both sexes, and expressed in both larva and adult. The CNS circuitry basic to this short latency signal in the adult might also serve by repetition in silent time-counting cycles to build up a more temporally complex communication mode (Buck and Case, 2001).
A cladistic analysis of distribution of larval and adult luminescence in modern members of the family Lampyridae and related luminescent cantharoids counters this line of thought, maintaining that firefly luminescence first arose in larvae (Branham and Wenzel, 2001, 2003). Biochemical and physiological considerations raise the possibility that there are useful clues to understanding evolutionary origins of bioluminescence that are revealed by distributional patterns of well-expressed larval and adult luminescent systems in existing species. A connection between these modern species and the earliest stages of luminescent systems in unknown firefly ancestors is suggested by several arguments. First, Seliger (1975) proposed that the likely antecedent of the modern firefly luminescent system lies in the ubiquitous mixed function oxidases, some of which are capable of weak luminescence. Enzymes of this class are widely distributed in many tissues of the organism. More recently Ward (1995) argued for evolution of firefly luciferase from coenzyme A synthetases. Thus it seems necessary to postulate that the most primitive form of bioluminescence in the firefly lineage would be generalized, whole body luminescence produced by an oxygen requiring luciferase, and appearing most likely simultaneously in all life stages. For such a development to have early adaptive value an aposematic role has been proposed (De Cock and Matthysen, 1999) or rapid attainment of neural control of light generation, or both, would be an early requirement for survival of the trait. To achieve a CNS controlled luminescent system from such an anatomically disperse beginning, most probably in virtually all tissues, larval and adult, one possibility is general, organism-wide tissue oxygen regulation by way of the tracheal system. Late evolution of the Coleoptera among the insects ensures that tracheal respiration was already undoubtedly in existence. Spiracular valve gating of respiratory gas exchange by discontinuous respiration is a well known water conservation mechanism in many insects (Buck, 1962) and this process could as well limit oxygen access to disperse primitive luciferases throughout the organism and render the insect both inactive and dark, so as to escape notice more easily. An alarm flash function might evolve under such circumstances because an attack would precipitate escape behavior and renewed tissue oxygenation with concomitant luminescence. The whole organism pupal glow (Strause et al., 1978) might be a model of the early stages of such a system. In modern insects there is support for this route of evolution of a control mechanism because of the involvement of the median nervous system in both spiracular valve muscle control (Case, 1957) and light organ control (Christiansen and Carlson, 1982). A further obvious step towards light organ evolution could have been consolidation of luminescent tissues in the abdomen as an adaptation to the competing necessity of maintaining a high level of oxygen in the thorax to support respiration of the locomotor musculature.
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ACKNOWLEDGMENTS |
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For ideas and valuable criticism, for instrument development and maintenance, and for help conducting experiments, I am indebted in alphabetical order to: Anna Bass, Marc A. Branham, Elisabeth Buck, John Buck, Albert D. Carlson, Jonathan Copeland, Steven S. H. D. Haddock, Christen Herren, Robert Harper, Maura Jess, Donata Oertel, Cristina Orrico, Cyril Johnson, and Carrie McDougall. Frank Hanson provided important comments on the manuscript. James Lindsey supplied most of the fireflies. I thank The Office of Naval Research for support of the UCSB Marine Bioluminescence Laboratory and the University of California for Faculty Research Grants for firefly research. Support of the FBN Fund is gratefully acknowledged.
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FOOTNOTES |
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1 From the Symposium Flash Communication: Fireflies at Fifty presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
2 E-mail: case{at}lifesci.ucsb.edu
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References |
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