TWO CASES OF FIREFLY TOXICOSIS IN LIZARDS

TWO CASES OF FIREFLY TOXICOSIS IN LIZARDS

MICHAEL KNIGHT(1), RICHARD GLOR(2), SCOTT R. SMEDLEY(3),
ANDRES GONZALEZ(2), KRAIG ADLER(2), and THOMAS EISNER(2)*

(1) ASPCA, National Animal Poison Control Center, 1717 South Philo Road,
Suite 36, Urbana, IL 61801
(2) Section of Neurobiology and Behavior, Cornell University, Seeley G.
Mudd Hall, Ithaca, NY 14853
(3) Department of Biology, Trinity College, Hartford, CT 06106

* To whom correspondence should be addressed.



Fireflies of the genus Photinus are poisonous. Their bodies contain lucibufagins (Eisner et al. 1978), steroidal pyrones related structurally to such well-known toxins as the bufodienolides of toads and the cardenolides of plants (Fieser and Fieser, 1949; Budavari et al., 1989) (Fig. 1). Not surprisingly, the lucibufagins protect Photinus against predation. Spiders (Phidippus spp.) are orally deterred by lucibufagins, as are birds (Hylocichla spp.), which also show reluctance to attack Photinus (Eisner et al., 1978, 1997). In the exceptional case where a Hylocichla was noted to ingest a Photinus, the bird reacted in short order by regurgitating it (Eisner et al. 1978). We know of no data on LD50 determinations for lucibufagins, but have now learned that ingestion of Photinus can be fatal to Australian lizards of the genus Pogona, commonly known as "bearded dragons".

Pogona lizards are highly tractable and easily maintained in captivity, and are bred in large numbers in the U.S.A. for the pet market (Vosjoli and Mailloux, 1996). The two instances in which ingestion of Photinus led to death of Pogona involved lizards that were maintained as pets. Their case histories follow:

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

Postmortem examination showed the animal to have been in good nutritional condition. The stomach contained insect remains (mostly Achaeta crickets, a staple food of pet lizards), including body parts of 9 Photinus pyralis. There were no gross anatomical lesions in stomach, spleen, trachea, heart, lungs, skeletal muscle, kidneys, or brain.

Case 2. The owner of a 7-month old male Pogona sp. (probably P. vitticeps) caught a single firefly (evening, mid-summer, Bronx, New York) and introduced it to the lizard's aquarium. The lizard immediately ate the firefly and within 60-90 min began showing oral gaping movements. These became more frequent over the next 30 min but there was no vomiting. The animal also underwent a color change, from tan to black, in the ventral region of the neck and abdomen, and the back of the tail. In the course of gaping, the lizard tended to protrude and bite its tongue. It then became quiescent and died. Postmortem examination revealed no gross internal lesions. The stomach contents were not checked and the ingested firefly remained unidentified.

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

Given the lack of detailed information on the toxicity of lucibufagins, little can be said about how precisely the chemicals effected their lethal action on Pogona. Cardenolides and bufodienolides are, of course, potently cardiotonic (Budavari et al., 1996), and even at low concentrations prone to induce nausea and emesis (Kaiser and Michl, 1958; Kelly and Smith, 1996). Moreover, they can be lethal at remarkably low dosages (ouabain: LD50, intravenous, cat=0.11 mg kg-1; bufalin: LD50, intravenous, cat=0.14 mg kg-1) (Harborne and Baxter, 1993; Kaiser and Michl, 1958). If lucibufagins are comparably toxic, and lizards as sensitive as cats, a systemic dose of 10-20 g lucibufagin -- less than half the amount in a single Photinus -- could be lethal to a 100 g Pogona. This estimate may not be out of line. Pharmacological tests (by Schering-Plough Corporation) established that lucibufagins, administered intravenously at a dosage of 0.06 mg kg-1, induced ventricular arrhythmia in dogs. The dose equivalent for a 100 g Pogona (assuming again comparable sensitivities) would be the amount of lucibufagin in one tenth of a Photinus. Obviously, it would have made sense to check on the toxicity of lucibufagins directly, by injecting the chemicals into Pogona, but we were unwilling to undertake tests that risked killing these beautiful animals.

It may seem surprising that Pogona did not reject Photinus on the basis of taste. In our experience with captive vertebrate predators, including a number of mice, birds, amphibians, and Anolis lizards, ingestion of potentially lethal insects occurs relatively rarely. Insect defenses, after all, are fashioned typically to take effect before rather than after ingestion. Interesting in this connection is that lizards (Anolis carolinensis, Sceloporus undulatus, Eumeces laticeps) that are sympatric with Photinus in southeastern United States reject these insects (Lloyd 1973; Sexton 1960, 1964) Sydow and Lloyd 1975). Could Pogona's failure to reject Photinus be a consequence of lack of historical coexistence of these lizards, in their native Australian habitats, with fireflies, or at least with lucibufagin-containing fireflies? In other words, could Pogona simply have lacked a "reason" for evolving 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 prolonged confinement or captive breeding, have become "reckless" in their feeding habits. We are disinclined to believe this and feel instead that Pogona are naturally "incautious". In tests with captive P. vitticeps (R. Glor, unpublished), we found these lizards to be aggressively indiscriminate. They readily ate the quinone-spraying cockroach Diploptera punctata (Roth and Alsop, 1978), as well as the pyrrolizidine alkaloid-laden moth Utetheisa ornatrix (Eisner and Meinwald, 1995). They rejected only bombardier beetles (whose quinonoid spray is hot) (Aneshansley et al., 1969) when first taking these into the mouth, but through persistent assault came to eat even these insects. We used several P. vitticeps 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 supervision over 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 complex of insects that sequester cardenolides from milkweed plants (including, among others, the monarch and queen butterflies [Danaus plexippus, D. gillipus], and the lygaeid bug, Oncopeltus fasciatus) (Blum, 1981).

Also worth noting is that exotic lizards other than Pogona may be susceptible to Photinus toxicosis as well. We were informed recently by the owner of several African chameleons (Chamaeleo pardalis) in Peoria, Illinois, that one individual (female) died following ingestion of "5 or 6" fireflies (unidentified).

Acknowledgements. Study supported in part by grant AI02908 from NIH. We thank Ashit K. Ganguly of Schering-Plough Corporation for sharing with us the data on the toxicity of lucibufagins, Thomas Adams of Peoria, IL, for the information on his pet chameleon, and Jerrold Meinwald for the chemical formulas.

REFERENCES

ANESHANSLEY, D. J., EISNER, T., WIDOM, J. M., and WIDOM, B. 1969. Biochemistry at 100C: explosive secretory discharge of bombardier beetles (Brachinus). Science 165: 61-63.

BLUM, M. S. 1981. Chemical Defenses of Arthropods. Academic press, New York.

BUDAVARI, S., O'NEIL, M. J., SMITH, A. and HECKELMAN, P. E. (eds) 1996. The Merck Index. Merck, Rahway, NJ.

EISNER, T., WIEMER, D. F., HAYNES, L. W., and MEINWALD, J. 1978. Lucibufagins: defensive steroids from the fireflies Photinus ignitus and P. marginellus (Coleoptera: Lampyridae). Proc. Nat. Acad. Sci. USA 75: 905-908.

EISNER, T. and MEINWALD, J. 1995. The chemistry of sexual selection. Proc. Nat. Acad. Sci. USA 92: 50-55.

EISNER, T., GOETZ, M. A., HILL, D. E., SMEDLEY, S. R., and MEINWALD, J. 1997. Firefly "femme fatales" acquire defensive steroids (lucibufagins) from their firefly prey. Proc. Nat. Acad. Sci. USA 94: 9723-9728.

FIESER, L. F. and FIESER, M. 1949. Natural Products Related to Phenanthrene. Reinhold, New York.

GOETZ, M.A., MEINWALD, J. and EISNER, T. 1981. Lucibufagins, IV. New defensive steroids and a pterin from the firefly Photinus pyralis (Coleoptera: Lampyridae). Experientia 37: 679-680.

HARBORNE, J. B. and BAXTER, H. (eds) 1993. Phytochemical Dictionary. Taylor & Francis. Washington, DC.

KAISER, E. and MICHL. H. 1958. Die Biochemie der tierischen Gifte. Franz Deuticke Wien. Vienna, Austria.

KELLY, R. A., and SMITH, T. W. 1996. Pharmacological treatment of heart failure. pp. 809-838 in J. G. Hardman, L. E. Limbird, P. B. Molinoff, R. W. Ruddon and A. G. Gilman (eds). Goodman & Gilman's The Pharmacological Basis of Therapeutics. McGraw Hill, New York.

LLOYD, J. E. 1998. Firefly parasites and predators. Coleopt. Bull. 27: 91-106.

MEINWALD, J., WIEMER, D. F., and EISNER, T. 1979. Lucibufagins. 2. Esters of 12-Oxo-2,5,11a-trihydroxybufalin, the major defensive steroids of the firefly Photinus pyralis (Coleoptera: Lampyridae). J. Am. Chem. Soc. 101: 3055-3060.

ROTH, L. M. and ALSOP, D. W. 1978. Toxins of Blattaria. pp. 465-487, in S. Bettini (ed) Arthropod Venoms. Handbook of Experimental Pharmacology Vol. 48 Springer-Verlag, New York.

SEXTON, O. J. 1960. Experimental studies of artificial Batesian mimics. Behaviour 15: 244-252.

SEXTON, O. J. 1964. Differential predation by the lizard Anolis carolinensis upon unicoloured and polycoloured insects after an interval of no contact. Anim. Behav. 12: 101-110.

SYDOW, S. L. and LLOYD, J. E. 1998. Distasteful fireflies sometimes emetic, but not lethal. Fl. Entomol. 58: 312.

VOSJOLI, P. de and MAILLOUX, R. 1996. Species and morphs of bearded dragons Pogona in U.S. herpetoculture. The Vivarium 7(6): 28-35.

FIGURE LEGEND Fig. 1. Chemical structures of a cardenolide (ouabain), a bufodienolide (bufalin) and a lucibufagin.