Model Selection For A Subterranean Trophic Cascad: Root-Feeding Caterpillars And Entomopathogenic Nematodes

Ecology, Dec, 1999 by D. R. Strong, A. V. Whipple, A. L. Child, B. Dennis

D. R. STRONG [1,4]

A. V. WHIPPLE [1]

A. L. CHILD [2]

B. DENNIS [3]

(1.) Bodega Marine Laboratory, Box 247, Bodega Bay, California 94923-0247 USA

(2.) Natural Resource Ecology Laboratory, Colorado State University, Ft. Collins, Colorado 80523 USA

(3.) Department of Fish and Wildlife Resources and Division of Statistics, University of Idaho, Moscow, Idaho 83844-1136 USA

Abstract. Conjecture abounds while evidence is limited concerning indirect protection afforded plants by carnivorous predators in terrestrial ecosystems, apropos of the Hairston-Smith-Slobodkin (HSS) hypothesis. We conducted a field experiment with a suspected trophic cascade. Could an entomopathogenic nematode protect bush lupine by killing rootfeeding ghost moth caterpillars? The experiment measured survival of lupine seedlings as a function of density of hatchling ghost moth caterpillars in rhizospheres with or without the entomopathogenic nematode.

We modeled lupine survival with a hierarchical family of "one-hit dose response" models to interpret the results of the experiment. We obtained maximum likelihood estimates of parameters and selected the best-fitting model using the Schwarz Information Criterion (SIC). The best model fit the data closely, and SIC model selection was consistent with classical likelihood ratio test results of models nested in the one-hit family. A parallel analysis performed upon a logistic family of models yielded results of poorer fit but largely consistent with results of the one-hit analysis. Finally, we compared our model-centered approach with the conventional methods-centered approach of logistic regression in statistical packages. While these packages give correct calculations, the implications of hypothesis tests are ecologically obscure in the absence of the explicit representation of models and their hierarchical relationships. For understanding ecological data, building an explicit statistical model of the process and testing parameters can be more informative than accepting the implicit model and testing variables in canned statistical packages.

The ecological implications were that seedling survival decreased exponentially with increasing densities of root-feeding caterpillars, and the entomopathogenic nematode virtually canceled the negative effect of this herbivore upon seedling survival. However, the significance to the broader community of this trophic cascade remains to be demonstrated. This cascade is a module or vignette within the greater food web, and additional interactions affect its influence: intraguild predation by nematode predators, apparent competition from other herbivores of lupine (each with its own natural enemies), and even more complicated interactions through competing plant species all come into play. As well, genetic variation of both the lupine and ghost moth caterpillars affects these interactions. Evidence does not support the inference that protection from ghost moth caterpillars by the entomopathogenic nematode is key to the "green" world of bush lupine.

Key words: Akaike information criterion; binary data; entomopathogenic nematode; indirect interaction; natural enemy; one-hit dose-response; Schwarz information criterion; statistical models; subterranean herbivory.

INTRODUCTION

With its hallmark "green world" metaphor, indirect, top-down control was a seminal idea of trophic ecology that has remained central to population-based theories of food webs (Oksanen et al. 1981, Hairston and Hairston 1993, 1997; carnivores ("natural enemies") suppress herbivore populations and thereby protect plants (Hairston, Smith, and Slobodkin 1960, "HSS"). Although HSS was originally applied to terrestrial food chains, most compelling examples of carnivores that indirectly protect plants are aquatic (Power 1990, Carpenter and Kitchell 1993, Estes and Duggins 1995, Brett and Goldman 1996). For communities on land, opinion is divided. Some authors advocate that simple HSS food chains determine the character of terrestrial ecosystems (Hairston and Hairston 1993), while others emphasize a more diverse set of food webs on land (Pastor and Naiman 1992, Strong 1992, Polis and Strong 1996, Jefferies 1999). Here we focus on a subterranean food chain that has been cited as evidence of HSS (Hairston and Hairston 1997). Herbivorous insects in the soil are ubiquitous (Brown and Gagne 1990), and very little is known of the significance of natural enemies in suppressing root-feeders. Our experiment concerned the plant protection afforded by an underground natural enemy of root-feeding insects.

Circumstantial evidence of a trophic cascade

Previous correlations suggested that an entomopathogenic nematode, Heterorhabditis hepialus, could indirectly protect bush lupine by killing root-feeding ghost moth caterpillars, which appeared to kill unprotected lupines. Lupinus arboreus, bush lupine, is a rapidly growing, nitrogen-fixing, perennial shrub (Mason and Connors 1996) native to the central California coast. Ghost moth caterpillars of Hepialus californicus (Lepidoptera, Hepialidae) feed upon lupine roots, are univoltine and largely monophagous at the study site at the Bodega Marine Reserve, Sonoma County, California. Ghost moths, also known as "swifts" or "swift moths," are strong flyers and disperse widely. On the wing, a single moth broadcasts upwards of 2000 small (0.5 mm diameter) eggs around and beneath L. arboreus plants (Wagner 1985, Tobi et al. 1993). Hatching within a few weeks, the tiny larvae burrow into the soil and feed upon the exterior of lupine roots. By early summer, larger caterpillars can bore inside to a refuge from natural e nemies. Death rates of mature lupines were correlated in space with densities of large ghost moth caterpillars on lupine roots. Roots of dead plants were girdled or deeply bored, presumably by ghost moth caterpillars (Strong et al. 1995). An entomopathogenic nematode, H. hepialus, killed ghost moth caterpillars in the soil of the study site (Stock et al. 1996). Where nematode prevalence in lupine rhizospheres was highest, densities of ghost moth caterpillars and annual rates of lupine mortality were lowest (Strong et al. 1996). This evidence was suggestive of an HSS chain, but circumstantial, and the field observations did not resolve the interactions of the nematode, young caterpillars (which are numerous but too small to be seen reliably in field surveys), and seedling bush lupine.