Enemy-free space maintains swallowtail butterfly host shift

Abstract

Natural enemies can be significant sources of mortality for herbivorous insects and therefore important agents of natural selection. One might expect selection to favor herbivores that escape from their natural enemies into enemy-free space. Although this is an appealing idea, it has received little empirical support, and no studies have documented enemy-free space as part of a nonagricultural, nonartificial host shift. The Alaskan swallowtail butterfly, Papilio machaon aliaska, uses as host plants a species in the family Apiaceae (Cnidium cnidiifolium) along with two Asteraceae species (Artemisia arctica and Petasites frigidus). I analyzed growth and survival of P. m. aliaska larvae in the field on the three host plants in treatments that either exposed or protected them from predators. I found that, in the presence of predators, larval survival is greater on the novel hosts (Asteraceae) than on the ancestral host (Apiaceae), but that in the absence of predators survival and growth are greater on the ancestral host. These results are a demonstration of enemy-free space as a mechanism for maintaining a naturally occurring host shift.Papilio machaon aliaska ͉ Lepidoptera ͉ predation ͉ Formica podzolica S wallowtail butterflies from the Papilio machaon (Linnaeus) group use plants of the Apiaceae as their primary hosts (1-4). Behavioral and metabolic constraints evidently limit potential opportunities to switch to other co-occurring plant species (5). Apart from the occasional use of plants in the family Rutaceae, an ancestral host family for the genus Papilio (2), P. machaon swallowtails have rarely incorporated nonapiaceous plants into their diet. In Alaska and northwestern Canada, P. m. aliaska Scudder oviposits and feeds not only on the local apiaceous host, Cnidium cnidiifolium (Turczaninow) Schischkin, but also on Artemisia arctica Lessing and Petasites frigidus (Linnaeus) Franchet (6) in the distantly related family Asteraceae. This host-range expansion by P. m. aliaska appears to represent an intermediate step toward a complete host shift. There is at least one example of a species in the P. machaon group that is now restricted to the novel host genus Artemisia (2); Papilio oregonius Edwards, a close relative of P. m. aliaska (2), is monophagous on Artemisia dracunculus Linnaeus (7). It is unclear, however, whether P. m. aliaska and P. oregonius represent a single host shift or two independent host shifts to Artemisia.The P. m. aliaska system presents an ideal opportunity to examine the role of enemy-free space (EFS) in a naturally occurring host shift. Other swallowtail larvae are subject to attack by a range of invertebrate and vertebrate predators (8, 9); my observations over the past 5 years of P. m. aliaska near Fairbanks, AK, suggest that the two most important larval predators are Formica podzolica Francoeur, an ant species that is widely distributed throughout North America (10), and the ichneumonid parasitoid Trogus lapidator panzeri Carlson. Jeffries and Lawton (11) defined EFS as ''ways of living...

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