Interpopulation Differences In Tolerance To Creosote Bush Resin In Desert Woodrats - Neotoma Lepida - Statistical Data Included

Ecology, August, 2000 by Antonio M. Mangione, M. Denise Dearing, William H. Karasov

ANTONIO M. MANGIONE [1]

M. DENISE DEARING [2]

Abstract. Plant secondary metabolites (PSMs) can affect survival, reproduction, and distribution of herbivores. Individuals with a high capacity to tolerate PSMs will experience fewer and smaller adverse effects than less tolerant individuals. Theoretically, the capacity to tolerate PSMs can be acquired during development, modulated during adulthood, or genetically fixed. We studied tolerance to phenolic resin from creosote bush (Larrea tridentata) in two populations of desert woodrats as a first step in understanding phenotypic habituation and genetic adaptation of this species to creosote resin. One population was from Mojave desert habitat where woodrats eat creosote bush, and the other from the Great Basin desert, where creosote bush is not present and woodrats consume mainly juniper (Juniperus osteosperma). For [greater than] 1 mo in the laboratory, woodrats from both populations were fed rabbit chow with increasing amounts of phenolic resin extracted from creosote bush until they lost body mass or show ed any sign of sickness. Woodrats from the Mojave population maintained body mass at higher concentrations of resin and remained in the experiment longer. There were no differences between populations in food intake across all resin levels; however, maximum resin intake was 25% higher for the Mojave population. Food intake decreased with increasing resin intake. Glucuronic acid excretion in urine, one indicator of detoxification capacity, did not differ between populations. Water consumption increased with increased levels of creosote resin in the diet in woodrats from both populations. The results are consistent with the idea of differential tolerance to creosote bush phenolic resin in desert woodrat populations. Woodrats appear to be a promising natural system to study the developmental or genetic factors underlying vertebrate adaptation to plant secondary metabolites.

Key words: creosote bush; desert woodrats; detoxification; glucuronic acid; Great Basin; Mojave Desert; Larrea tridentata; Neotoma lepida; phenolic resin; plant secondary metabolites; tolerance.

INTRODUCTION

The ability to cope with or tolerate PSMs (plant secondary metabolites) has profound implications for animal population ecology by influencing diet selection (Freeland and Janzen 1974, Belovsky and Schmitz 1991), mortality, and hence population dynamics (Haukioja 1980, Bryant et al. 1991). Tolerance to a PSM can be measured as the highest intake of the compound (as mass per unit time or as percentage of diet) that permits survival, ability to maintain body mass, or normal growth. In insects tolerance to PSMs differs between populations within species (Fox and Morrow 1981, Futuyma and Peterson 1985, Ayres and Scriber 1994). Intraspecific tolerance to secondary compounds has not been investigated in mammals, and the desert woodrat (Neotoma lepida) is a good species to study potential intraspecific differences in tolerance to PSMs. Woodrats of this species are widely distributed, in all North American deserts except the Chihuahuan. Neotoma lepida occurs in many habitat types, i.e., creosote bush, pinyon-juniper woodland, chaparral, oak woodland, and coastal scrub (Cameron and Rainey 1972). Populations in these habitats have diets dominated by different plant species with different secondary metabolite composition. Opuntia spp. are rich in oxalates (Shirley and Schmidt-Nielsen 1967, Justice 1985), Juniper spp. are rich in terpenes (Schwartz et al. 1980, Adams et al. 1981), and Larrea tridentata (creosote bush) is rich in phenolics. Leaves of creosote bush contain 10-25% dry mass of a phenolic resin. The resin is composed of 40% dry mass of NDGA (nordihydroguaiaretic acid) and the remainder of the resin is a complex mixture of partially o-methylated flavones and flavonols (Mabry et al. 1977, Rhoades and Cates 1976).

There are few species of animals that feed on creosote bush (Meyer and Karasov 1991). Creosote bush phenolic resin is known to deter feeding by arthropods and to complex with protein in vitro (Rhoades and Cates 1976). Laboratory rats fed NDGA at 0.5, 1, or 3% of food dry mass, produced cysts in the kidney and vacuolation of kidney tubular epithelium (Grice et at. 1968, Goodman et al. 1970). Animals that naturally feed on creosote bush are very selective regarding the age and part of the plant upon which they feed. For example, jackrabbits (Lepus californicus) and N. lepida prefer the mature over the young leaves presumably because phenolic resin levels are lower in the mature ones (Hayden 1966, Meyer and Karasov 1989, Ernest 1994).

We focused our study of differential tolerance to PSMs on two particular populations of desert woodrats: (1) individuals from three sites in the Mojave Desert (hereafter called Mojave woodrats) and (2) individuals from two sites in the Great Basin desert (hereafter called Great Basin woodrats). The composition of plant species in both habitats and consequently the diets of these two populations of desert woodrats differed greatly between the two habitats. Mojave woodrats eat creosote bush, whereas Great Basin woodrats rely mostly on juniper (Juniperus osteosperma) (A. M. Mangione, personal observation). We measured tolerance of woodrats as defined by maintenance of mass balance when ingesting creosote bush resin and/or the lack of any signs of adverse effects.