Journal of Chemical Ecology, Vol. 25, No. 9, 1999

FIREFLY TOXICOSIS IN LIZARDS1

MICHAEL KNIGHT,2 RICHARD GLOR,3 SCOTT R. SMEDLEY,4

ANDRES GONZALEZ,3 KRAIG ADLER,3 and THOMAS EISNER3,*

2ASPCA, National Animal Poison Control Center1717 South Philo Road, Suite 36

Urbana, Illinois 618013Department of Neurobiology and Behavior

Cornell University, Seeley G. Mudd HallIthaca, New York 14853

4Department of Biology, Trinity CollegeHartford, Connecticut 06106

(Received November 16, 1998; accepted April 18, 1999)

Abstract—Ingestion of fireflies of the genus Photinus (Lampyridae) can belethal to Australian lizards of the genus Pogona (Agamidae), probably becauseof the poisonous steroidal pyrones (lucibufagins) that these fireflies contain.One Photinus may suffice to kill a Pogona. Captive Pogona kept as petsneed to be shielded from firefly ingestion. African chameleons (Chamaeleo;Chamaeleonidae) appear also to be vulnerable to Photinus toxicosis.

Key Words —Pogona, Chamaeleo, Lacerta, Litoria (Pelodryas) Photinus,lucibufagins, cardiotonic agents, pet industry.

INTRODUCTION

Fireflies of the genus Photinus are poisonous. Their bodies contain lucibufagins(Eisner et al., 1978), steroidal pyrones related structurally to such well-knowntoxins as the bufodienolides of toads and the cardenolides of plants (Fieser andFieser, 1949; Budavari et al., 1996) (Figure 1). Not surprisingly, the lucibufaginsprotect Photinus against predation. Spiders (Phidippus spp.) are orally deterredby lucibufagins, as are birds (Hylocichla spp.), which also show reluctance toattack Photinus (Eisner et al., 1978, 1997). In the exceptional case where a

*To whom correspondence should be addressed.1Paper no. 158 of the series Defense Mechanisms of Arthropods; no. 157 is Gonzalez, A., F.Schroeder, J. Meinwald, and T. Eisner, J. Nat. Prod. 62:378-380 (1999).

1981

0098-0331/99/0900-198l$16.00/0 © 1999 Plenum Publishing Corporation

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FIG. 1. Chemical structures of a cardenolide (ouabain), a bufodienolide (bufalin), and alucibufagin.

Hylocichla was noted to ingest a Photinus, the bird reacted in short order byregurgitating it (Eisner et al., 1978). We know of no data on LD50 determinationsfor lucibufagins, but have now learned that ingestion of Photinus can be fatal toAustralian lizards of the genus Pogona, commonly known as bearded dragons.

Pogona lizards are highly tractable and easily maintained in captivity; theyare bred in large numbers in the United States for the pet market (Vosjoli andMailloux, 1996). The two instances in which ingestion of Photinus led to deathof Pogona involved lizards that were maintained as pets. Their case historiesfollow.

METHODS AND MATERIALS

Case 1. The owner of a healthy 8-month-old male P. vitticeps (about 100g body mass) captured a number of fireflies one July evening in the environs ofhis home (Iowa City, Iowa) and offered these to the lizard in its cage (aquar-ium tank). The lizard promptly ingested several of the fireflies. Within about 30min the lizard began exhibiting violent head-shaking movements, followed bypronounced and increasingly frequent oral gaping. The animal seemed intent onvomiting, but no regurgitation was noted. As the gaping intensified, so did thelizard's respiratory effort, and the animal soon showed severe dyspnea. Withinthe next 30 min, it underwent a conspicuous color transformation, its dorsal trunkand nape changing from the usual light tan to black. Within the hour after inges-tion of the fireflies, and before veterinary assistance could be enlisted, the lizarddied.

Postmortem examination showed the animal to have been in good nutri-tional condition. The stomach contained insect remains (mostly Acheta crickets,

a staple food of pet lizards), including body parts of nine Photinus pyralis. Therewere no gross anatomical lesions in stomach, spleen, trachea, heart, lungs, skele-tal muscle, kidneys, or brain.

Case 2. The owner of a 7-month-old male Pogona sp. (probably P. vit-ticeps) caught a single firefly (evening, mid-summer, Bronx, New York) andintroduced it to the lizard's aquarium. The lizard immediately ate the firefly andwithin 60-90 min began showing oral gaping movements. These became morefrequent over the next 30 min, but there was no vomiting. The animal also under-went a color change, from tan to black, in the ventral region of the neck andabdomen, and the back of the tail. In the course of gaping, the lizard tendedto protrude and bite its tongue. It then became quiescent and died. Postmortemexamination revealed no gross internal lesions. The stomach contents were notscrutinized and the ingested firefly remained unidentified.

RESULTS AND DISCUSSION

There seems little doubt that the two Pogona died as a consequence of fire-fly ingestion. Moreover, in case 1, the firefly, P. pyralis, was of a species that weourselves showed to contain lucibufagins (on the order of 90 ug per individual)(Meinwald et al., 1979; Goetz et al., 1981). In case 2, the firefly was in all likeli-hood also a Photinus, since two species of the genus (P. ignitus and P. marginellus),both known to contain lucibufagins (on average 60 ug per individual), are abun-dant in New York State (Eisner et al., 1997). Even if the ingested firefly had beenof another genus, say Photuris (which also occurs in New York State), the Pogonacould still have taken in lucibufagins, since female Photuris routinely acquire thechemicals by feeding on Photinus (Eisner et al., 1997).

Given the lack of detailed information on the toxicity of lucibufagins, littlecan be said about how the chemicals effected their lethal action on Pogona. Car-denolides and bufodienolides are, of course, potently cardiotonic (Budavari et al.,1996), and even at low concentrations they are prone to induce nausea and emesis(Kaiser and Michl, 1958; Kelly and Smith, 1996). Moreover, they can be lethal atremarkably low dosages (ouabain: LD50, intravenous, cat = 0.11 mg/kg; bufalin:LD50, intravenous, cat = 0.14 mg/kg) (Harborne and Baxter, 1993; Kaiser andMichl, 1958). If lucibufagins are comparably toxic and if lizards are as sensitive ascats, a systemic dose of 10-20 ug lucibufagin- less than half the amount in a singlePhotinus — could be lethal to a 100-g Pogona. This estimate may not be out of line.Pharmacological tests (by Schering-Plough Corporation) established that lucibufa-gins induced ventricular arrhythmia in dogs when administered intravenously at adosage of 0.06 mg/kg. The dose equivalent for a 100-g Pogona (assuming againcomparable sensitivities) would be the amount of lucibufagin in one tenth of aPhotinus. Obviously, it would make sense to evaluate the toxicity of lucibufagins

FIREFLY TOXICOSIS 1983

directly, by injecting the chemicals into Pogona, but we are unwilling to undertaketests that risk killing these beautiful animals.

It may seem surprising that Pogona did not reject Photinus on the basis oftaste. In our experience with captive vertebrate predators, including a number ofmice, birds, amphibians, and Anolis lizards, ingestion of potentially lethal insectsoccurs relatively rarely. Insect defenses, after all, are fashioned typically to takeeffect before rather than after ingestion. Interesting in this connection is that lizards(Anolis carolinensis, Sceloporus undulatus, Eumeces laticeps) that are sympatricwith Photinus in southeastern United States reject these insects (Lloyd, 1973; Sex-ton, 1960, 1964; Sydow and Lloyd, 1975). Could Pogona's failure to reject Phot-inus be a consequence of lack of historical coexistence of these lizards, in theirnative Australian habitats, with fireflies, or at least with lucibufagin-containingfireflies? Perhaps Pogona simply have been spared the selective pressure for evolv-ing an oral aversion to (or systemic tolerance of) lucibufagins. To our knowledge,Australian fireflies have not been studied chemically.

Alternatively, it is conceivable that caged Pogona, as a consequence of pro-longed confinement or captive breeding, have become "reckless" in their feed-ing habits. We are disinclined to believe this and feel instead that Pogona arenaturally incautious. In tests with captive P. vitticeps (R. Glor, unpublished),we found these lizards to be aggressively indiscriminate. They readily ate thequinone-spraying cockroach Diploptera punctata (Roth and Alsop, 1978), aswell as the pyrrolizidine alkaloid-laden moth Utetheisa ornatrix (Eisner andMeinwald, 1995). They rejected only bombardier beetles (whose quinonoid sprayis hot) (Aneshansley et al., 1969) when first taking these into the mouth, butthrough persistent assault came to eat even these insects. We used several P. vit-ticeps in these tests and found none to be harmed by ingestion of these insects.

We conclude that Pogona pet owners would do well to exercise supervisionover the insect diet of their pets, lest they risk losing them. Fireflies, of course,should be altogether excluded from the diet, but so probably should the complexof insects that sequester cardenolides from milkweed plants [including, amongothers, the monarch and queen butterflies (Danaus plexippus, D. gillipus), andthe lygaeid bug, Oncopeltus fasciatus] (Blum, 1981).

Also worth noting is that exotic lizards other than Pogona may be susceptibleto Photinus toxicosis as well. We were informed recently by the owner of severalAfrican chameleons (Chamaeleo pardalis) in Peoria, Illinois, that one individual(female) died following ingestion of "five or six" fireflies (unidentified).

POSTSCRIPT

Since writing the above we have learned of a case of firefly toxicosis involv-ing White's tree frog, Litoria (or Pelodryas) caerulea (Hylidae), a native of

1984 KNIGHT ET AL.

northern and eastern Australia. Two juvenile frogs ate about three fireflies atabout 20 : 00 hr that had been collected near Cleveland, Ohio. The insects con-tinued to flash even after ingestion, as could be seen through the frog's bodywall. The frogs were dead the next morning; they did not attempt to regurgitatenor were there signs in the aquarium that they had attempted to do so. Theydid not change color. We are grateful to Lynn and Martin Rosenberg (Depart-ment of Biology, Case Western University, Cleveland, Ohio 44106) for theseobservations.

More recently, we have learned that a healthy adult specimen of Lacertaderjugini (Lacertidae), a native of the Caucasus, died following ingestion of asingle firefly (unidentified) that had been collected on a late June day on LongIsland, New York. Five minutes after eating the firefly, the lizard began to gapeand regurgitated the dead prey; it then rolled on the substrate for 2- 3 min, con-tinued to gape, and was dead within 15 min of consumption. We thank EdwardMariotti (Handex Environmental, Inc., New York) for this information. It seemsthat firefly toxicosis may be a widespread phenomenon.

Acknowledgments—This study was supported in part by grant AI02908 from NIH. We thankDr. Ashit K. Ganguly of Schering-Plough Corporation for sharing with us the data on the toxicityof lucibufagins, Mr. Thomas Adams of Peoria, Illinois, for the information on his pet chameleon,and Dr. Jerrold Meinwald for the chemical formulas. We also thank Dr. Mary J. Hart Weintraub forsending the lizard (case 1) remains containing the P. pyralis, and the University of Illinois Collegeof Veterinary Medicine Diagnostic Laboratory (Drs. Howard B. Gelberg and Roberto E. Guzman),and the Animal Medical Center, New York (Drs. Tracy E. Bartick and Katherine E. Quesenberry)for diagnostic work.

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