Plant tolerance of gall-insect attack and gall-insect performance

Ecology, March, 1996 by Philip A. Fay, David C. Hartnett, Alan K. Knapp

INTRODUCTION

The ability of plants to tolerate herbivory depends strongly on the environmental conditions surrounding the interaction. For example, tolerance of herbivory is enhanced when light, water, and nutrients are more abundant, and when competition from neighboring plants is less intense (Crawley 1983, Parker and Salzman 1985, Louda et al. 1990, Whitham et al. 1991, McEvoy et al. 1993, Rosenthal and Kotanen 1994). Herbivory tolerance also depends on plant growth rates, post-damage allocation patterns, photosynthetic rates, and reserves of carbohydrates, nutrients, and meristems (Rosenthal and Kotanen 1994). In particular, the ability to reallocate resources to reserve meristems provides developmental plasticity in a variable environment and is necessary for compensatory regrowth after damage (Maschinski and Whitham 1989, Aarsen and Irwin 1991, Paige 1992, Rosenthal and Kotanen 1994).

The factors affecting tolerance of herbivory can also have consequences for herbivores. Host-plant resource availability can affect herbivore attack rates (Horner and Abrahamson 1992, Rossi et al. 1992), survivorship, growth, and sex ratios (Preszler and Price 1988, Waring and Cobb 1989, Craig et al. 1992), and attractiveness to herbivore natural enemies (Fox et al. 1990). Since plant resources have such widespread effects on the plant and on the herbivore, there may be complex feedbacks in their interactions (Haukioja 1990), with uncertain consequences for plant and herbivore population dynamics.

We conducted simultaneous studies of a plant/gall-insect interaction under natural field conditions and in a competition-free experimental garden where nutrient and water availability were manipulated. These experiments examined (1) plant regrowth responses after gall formation on apical meristems, (2) how a plant's growing conditions might affect plant tolerance of gall-insect damage, and (3) how factors affecting plant tolerance might affect gall-insect performance.

Gall-insect/plant interactions are complex and poorly understood. Galls are an integrated part of the plant (Weis et al. 1988, Shorthouse and Rohfritsch 1992) that can alter plant architecture and reproduction (Dennill 1985, Sacchi et al. 1988, Fay and Hartnett 1991, DeClerck-Floate and Price 1994). Galls often play active physiological roles, regulating lateral or adventitious regrowth after gall formation (Weis 1984, Craig et al. 1986, DeClerck-Floate and Price 1994), redirecting resource movement (Jankiewicz et al. 1970, McCrea et al. 1985, Larson and Whitham 1991), and increasing photosynthetic rates (Weis and Kapelinski 1988, Fay et al. 1993). These physiological effects possibly continue for the duration of the metabolically active life of the gall, which is several months in some species. Thus, galls may play a more active role in plant regrowth responses than free-feeding herbivores, which typically "eat and run," leaving the plant to respond based on its own physiological constraints.

These studies focused on the tallgrass prairie perennial forb Silphium integrifolium var. laeve T. and G. (=Silphium speciosum Nutt. Rydberg, Asteraceae; hereafter "rosinweed") and the cynipid gall wasp Antistrophus silphii Gil. (Hymenoptera). A. silphii galls form on shoot apical meristems, causing conflicting effects on shoot growth and physiology. Galls reduce shoot growth, leaf area, and inflorescence development but increase photosynthetic rates and stem water potential (Fay and Hartnett 1991, Fay et al. 1993). Since prairie plants are nitrogen limited (Owensby et al. 1970, Knapp and Seastedt 1986), periodically [TABULAR DATA FOR TABLE 1 OMITTED] [TABULAR DATA FOR TABLE 2 OMITTED] drought stressed, and can be shaded by neighbors (Fay 1992), resource availability should be an important factor in Silphium regrowth responses and gall-insect performance.

Life histories of rosinweed and the gall wasp

Rosinweed grows on sites with deep soils and a history of disturbance (Great Plains Flora Association 1986). A rosinweed plant (genet) usually consists of 20-50 shoots forming a tightly packed clump. Rosinweed's architecture is simple, and typical of many prairie forbs. Each spring new growth emerges from below ground buds set the previous year on a stout, rootstock-like rhizome. During April the buds form a rosette, then in May they rapidly elongate into a 1-2 m tall primary shoot bearing 15-25 pairs of sessile opposite leaves (Fay and Hartnett 1991). Primary shoot growth ends in July when the apical meristem produces a terminal inflorescence of 1-15 flower heads (capitula). Shoots are normally unbranched. As a result, an intact apical meristem is required for sexual reproduction and to grow above the surrounding plant canopy. Deer occasionally browse rosinweed, causing axillary shoot growth and inflorescence production. However, shoot height is reduced and shading by neighbors becomes more severe (P. Fay, personal observation). Achenes mature in August. All aboveground parts die back by the end of October, and are completely replaced the following year.