Evolution of toxicity in Pitohuis: I. effects of homobatrachotoxin on chewing lice (order Phthiraptera)

Auk, The, Oct 1999 by Dumbacher, John P

ABSTRACT.-Birds in the genus Pitohui carry the potent neurotoxin homobatrachotoxin in their skin and feathers. In this study, I tested whether homobatrachotoxin can repel or kill chewing lice (order Phthiraptera). When individual feather lice were offered a choice of two feathers on which to feed or take shelter, the lice preferred nontoxic feathers to feathers of the most toxic pitohui species, Pitohui dichrous. Moreover, the presence of toxic P dichrous feathers significantly shortened the life span of captive feather lice. These results suggest that homobatrachotoxin repels and kills lice and may thus protect pitohuis against lice infestation. Received 10 April 1998, accepted 8 February 1999.

SPECIES IN THE AVIAN GENUS PITOHUI carry a potent alkaloid neurotoxin in their skin and feathers (Dumbacher et al. 1992). Pitohui toxin, known as homobatrachotoxin (homoBTX), is a member of a well-known family of steroidal alkaloids that depolarize nerve and muscle membranes by binding and activating voltage-dependent sodium channels (Albuquerque et al. 1971). In some cases, concentrations of toxin are sufficiently high that merely handling an individual Hooded Pitohui (Pitohui dichrous) can irritate buccal membranes and can cause sneezing and burning, watery eyes (Salvadori 1881, Majnep and Bulmer 1977, Dumbacher et al. 1992). Anthropological evidence suggests that the toxin defends pitohuis from human hunters (Majnep and Bulmer 1977; KocherSchmid 1991, 1993), and other workers have speculated that it also defends pitohuis against natural predators (Diamond 1992) and arthropod ectoparasites (Mouritsen and Madsen 1994, Poulsen 1994). Nevertheless, no studies have directly investigated if the enemies of pitohuis are deterred by homoBTX or how homoBTX deters them.

Arthropod ectoparasites are natural enemies of pitohuis and potential targets for pitohui defensive chemicals. HomoBTX has been shown to affect a wide range of vertebrates and invertebrates (Albuquerque et al. 1971, Daly and Spande 1986, Dwivedy 1988). With the notable exceptions of pitohuis and Phyllobates frogs, nearly every animal that contains voltage-dependent sodium channels is poisoned by batrachotoxins, including distantly related arthropods. Also, bird lice can influence host fitness in several ways. Lice can affect the energetics and survival of hosts (Clayton 1990, Booth et al. 1993, Brown et al. 1995), reduce egg numbers and hatching rates (Derylo 1974, DeVaney 1976), reduce mating success (Hamilton and Zuk 1982, Clayton 1990, Loye and Zuk 1991, Clayton and Tompkins 1995), and transmit pathogens (Marshall 1981, Clayton 1990). Therefore, defense against lice might be under selection. Finally, a high proportion of a pitohui's total toxin is concentrated in the skin and feathers. Because lice live and feed on feathers, skin, and subdermal blood supplies, pitohui toxins could constitute a formidable barrier to these ectoparasites.

HomoBTXs, and toxins in general, could defend birds against lice through several alternative mechanisms. Toxins could (1) reduce louse fecundity (2) reduce louse survival, (3) reduce the influence of lice on host fitness (e.g. by delaying maturation, lengthening the life cycle, or suppressing appetite), and (4) favorably effect louse transmission rates by reducing immigration or inducing emigration. Here, I report experimental studies that examine whether feather lice exhibit an active choice against naturally toxic pitohui feathers and examine whether the presence of natural levels of homoBTX affects the captive life span of these lice.

Because toxin levels vary across pitohui speties, feathers from different pitohuis provide naturally high and low toxicity treatments, and outgroups provide nontoxic control feathers. Individuals from five pitohui species are known to contain some level of homoBTX (Dumbacher 1997), with P dichrous containing the highest concentrations. In some populations, P dichrous feathers contain more than 50 jg of homoBTX per g of tissue, which is more than 15 times the concentration originally reported. Rusty Pitohui (P ferrugineus) feathers have much lower levels, and Crested Pitohui (P cristatus) feathers have nearly undetectable levels of toxin.

METHODS

Studies were conducted at the Biological Research Station, Varirata National Park (927'S, 14721'E; 840 rn elevation), a 400-ha reserve on the Sogeri escarpment approximately 40 km east of Port Moresby, southeastern Papua New Guinea. Birds were trapped in mist nets, measured (wing, tarsus, head and bill length, and body mass), banded, visually inspected for parasite loads, and released.

Lice were removed from host birds using fumigation jars described by Bear (1995) and equipped so industrial-grade CO, could be pumped constantly into the jar. Feathers were blown and ruffled to detach anesthetized lice. The lice revived within 15-30 s of exposure to normal air and then were collected in petri dishes where they were held until they could be placed into experimental arenas, usually within the hour.