Oecologia (2000) 125:218–228 DOI 10.1007/s004420000444 Ahnya M. Redman · J. Mark Scriber Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids Received: 29 November 1999 / Accepted: 14 April 2000 / Published online: 21 June 2000 © Springer-Verlag 2000 Abstract The gypsy moth, Lymantria dispar, and the Key words Competition · Tritrophic interactions · northern tiger swallowtail, Papilio canadensis, overlap Papilo canadensis · Lymantria dispar · Gypsy moth geographically as well as in their host ranges. Adult fe- male swallowtails are incapable of distinguishing be- tween damaged and undamaged leaves, and the opportu- Introduction nities for competition between these two species are nu- merous. We designed field and laboratory experiments to In 1960, Hairston and co-workers asserted that herbi- look for evidence of indirect competition between P. vores could not possibly be limited by food given the canadensis and L. dispar larvae. Swallowtail caterpillars overwhelming abundance of green plants on earth; defo- were reared in the laboratory on leaves from gypsy- liation, after all, seemed a relatively rare event (Hairston moth-defoliated and undefoliated trees to explore host- et al. 1960). Due in part to this influential paper, the plant effects. We tested for pathogen-mediated interac- importance of competition among herbivorous insects tions by rearing swallowtail larvae on both sterilized and was for many years largely overlooked (McClure 1983; unsterilized leaves from defoliated and undefoliated Denno et al. 1995) or discounted entirely (Lawton and sources. In addition, we measured the effects of known Strong 1981). Moreover, most documented instances gypsy moth pathogens, as well as gypsy moth body flu- of competition between herbivorous species can be clas- ids, on the growth and survival of swallowtail larvae. sified as “asymmetrical competition”, in which only Field experiments were designed to detect the presence one species is affected negatively, leading Lawton and of parasitoid-mediated competition, as well: we recorded Hassell (1981) to argue that such interactions would take parasitism of swallowtail caterpillars placed in the field place only during insect outbreaks and thus occur so either where there were no gypsy moth larvae present, or rarely as to be ecologically unimportant. where we had artificially created dense gypsy moth pop- Many plant-herbivore ecologists have recently begun ulations. We found evidence that swallowtails were neg- to reexamine interspecific competition among insect her- atively affected by gypsy moths in several ways: defolia- bivores, which now appears to be far more common than tion by gypsy moths depressed swallowtail growth rate once thought (Denno et al. 1995). However, it may yet, and survival, whether leaves were sterilized or not; ster- as Lawton and Hassell (1981) suggested, tend to be asso- ilization significantly reduced the effect of defoliation, ciated with introduced pests, free from their natural ene- and gypsy moth body fluids proved lethal; and swallow- mies and capable of devouring enormous amounts of tail caterpillars suffered significantly increased rates of vegetation (DeBach and Sundby 1963; Denno et al. parasitism when they were placed in the field near gypsy 1995). Further, it probably involves indirect, or “appar- moth infestations. ent”, competition more frequently than direct battles over food (Faeth 1985; Hawkins 1988; Karban et al. 1994; Denno et al. 1995). Typically, indirect competition between species occurs when the activity of one species A.M. Redman · J.M. Scriber induces a chemical response in its host plant, affecting Department of Entomology, Michigan State University, other species feeding on the same plant (Niemela et East Lansing, MI 48824, USA al. 1984; Faeth 1985, 1986; West 1985; Harrison and Present address: Karban 1986; Gibberd et al. 1988; Neuvonen et al. 1988; A.M. Redman, Department of Entomology, The Pennsylvania State University, University Park, Hunter 1990; Dankert et al. 1997). PA 16802, USA, Examples of indirect competition mediated by patho- e-mail: [email protected], Fax: +1-814-8653048 gens have been reported for a great many species, in- 219 cluding humans (Price et al. 1986), but not, as far as we ize salicaceous plants, which abound in northern lati- know, for herbivorous insects. Few cases have been doc- tudes (Lindroth and Scriber 1988; Scriber et al. 1989). P. umented, but predators and parasitoids may also mediate canadensis is polyphagous, but it typically exhibits a indirect competition (McClure 1981; Karban et al. strong preference for quaking aspen, Populus tremulo- 1994). The attraction of polyphagous natural enemies to ides (Salicaceae) (Scriber et al. 1991). Females of the visual cues (Faeth 1990) or unknown factors associated univoltine Papilio canadensis generally oviposit on new- with primary hosts (Settle and Wilson 1990) or host ly expanded leaves during the first few weeks of June, damage (Faeth 1986) can negatively affect neighboring and larvae grow throughout the summer, pupating in herbivores. Environmental factors, in certain cases, may mid- to late August. also change the outcome of competition: wind and rain Quaking aspen, which supports a large number of her- (McClure and Price 1975, 1976), or temperature (Waloff bivores, is defended primarily by the phenolic glycosides 1968; Valle et al. 1989) may differentially affect herbi- salicortin and tremulacin, and secondarily by tannins vore species that vary in their tolerance of such factors, (Clausen et al. 1989; Lindroth 1992). It grows indetermi- thus conferring an advantage on one competitor. A novel nately throughout the summer, even in the absence of de- example of environmentally mediated competition oc- foliation, and increases its rate of growth when leaf tis- curs on oak trees, where an early-season leaf-chewer cre- sue is removed (Hodson 1981). In some cases, refolia- ates such large holes in leaves that a late-season leaf- tion replaces nearly 90% of damaged foliage (Heichel rolling species is rendered incapable of creating struc- and Turner 1976) with leaves that tend to be rich in phe- tures airtight enough to maintain adequate humidity nolic glycosides (Clausen et al. 1989). Damaged leaves (Hunter and Willmer 1989). themselves also tend to contain elevated levels of these As awareness of interspecific competition among in- compounds (Mattson and Palmer 1987). sects increases, so does interest in its impact on the popu- The European gypsy moth, Lymantria dispar (L.) lation dynamics, host use, and community organization of (Lepidoptera: Lymantriidae) was brought to Massachu- insect folivores. There is experimental evidence suggest- setts from France in 1868, and has since radiated steadily ing that the population dynamics of certain herbivore spe- to the north, south, and west, taking over most of the cies can be driven both by changes in plant chemistry in- eastern United States (Liebhold et al. 1997; Sharov et al. duced by competing species feeding on the same host, and 1998). In the East, it prefers to feed on white oak and by natural enemies associated with competitors. Karban chestnut oak, and, in the Midwest, Populus species such (1986), for one, showed that competition between Phil- as quaking aspen are favored (Wallner 1988). Gypsy aenus spumarius (Homoptera: Cercopidae) and Platyptilia moth outbreaks are ecologically dramatic events, and it williamsii (Lepidoptera: Pterophoridae), presumably me- is difficult to imagine that many species remain unaffect- diated in part by plant chemistry, negatively affected the ed by the presence of such a voracious defoliator. During abundance of P. spumarius on Erigeron glaucus (Compo- peak outbreak years, levels of stand defoliation by gypsy sitae). Several years later, Karban et al. (1994) found that moths can reach nearly 100% in some areas (Cameron populations of the herbivorous Tetranychus pacificus (Ac- 1986; Hart 1990), opening the tree canopy and causing ari: Tetranychidae) fluctuated in response to populations profound ecological changes, such as increased preda- of a neighboring herbivore, Eotetranychus willamettei tion on bird nests (Thurber et al. 1994) and a reduction (Acari: Tetranychidae), and its associated predators on in the diversity of lepidopteran fauna (Sample et al. grapevines. 1996). Gypsy moth defoliation affects the chemistry of Further, a few researchers have shown that interspe- primary host plants, such as quaking aspen (Lindroth cific competition plays a part in shaping the host use and 1992; Dankert et al. 1997), and gypsy moth outbreaks the community organization of folivores. For example, are associated with high densities of pathogens, preda- Ritchie and Tilman (1992) found that the relative por- tors, and parasitoids (Elkinton and Liebhold 1990). At tions of dicots and monocots in the diets of polyphagous least some of these natural enemies, e.g., Compsilura co- grasshoppers were altered by the presence of indirect ncinnata (Diptera: Tachinidae), are known to use alterna- competition, and Karban (1989) found experimental evi- tive hosts (Leonard 1981). dence that interspecific competition helped to shape the Both the geographic range and the host range of Papi- community organization of folivores on Erigeron glau- lio canadensis overlap significantly with those of L. dis- cus. par. Therefore, it seemed likely to us that the tri- or We