The Effects of Moldiness Level on Seed Selection by Dipodomys spectabilis

Desert rodents of the family Heteromyidae are mainly seed eaters and some species of kangaroo rats (Dipodomys) store large quantities of seeds in underground caches (Shaw, 1934; Vorhies and Taylor, 1922). Approximately 23 species of molds have been discovered growing in caches of D. spectabilis (Reichman et al., 1985), about half of which produce a variety of mycotoxins (Wyllie and Morehouse, 1978). Subterranean fungi are included in diets of a variety of mammals including mice, voles, rats, lemmings (Muridae); chipmunks and squirrels (Sciuridae); and rabbits (Leporidae; Fogel and Trappe, 1978); some aquatic insect larvae eat slightly moldy leaves (Arsuffi and Suberkropp, 1984). In all of these, however, the fungal species involved are unlike those found in the caches of D. spectabilis in that they do not produce mycotoxins and most have a symbiotic relationship with the animals that ingest them; the molds produce specific fruiting bodies that the animals ingest, and through feeding the animals disperse fungal spores. Previous studies of diet choice conducted with pocket mice (Perognathus intermedius) and kangaroo rats (D. spectabilis) suggest that the order selected with respect to moldiness is: slightly moldy > nonmoldy > heavily moldy (Rebar and Reichman, 1983; Reichman and Rebar, 1985). Slightly moldy seeds, as defined by the authors, are those at the stage of fungal colonization where only hyphae are present, whereas heavily moldy seeds are extensively covered with both conidia and hyphae (Reichman, pers. comm.). When toxic fungi reach the stage of conidial production, they also begin to produce mycotoxins (Wyllie and Morehouse, 1978), and heavily moldy seeds contain mycotoxins (Reichman and Rebar, 1985). Reichman and Rebar (1985) suggested that heteromyids might select slightly moldy seeds because these seeds may possess beneficial features associated with fungal colonization (e.g., increased nutrition or digestibility) not found in nonmoldy seeds, but they do not contain the mycotoxins produced by heavily moldy seeds. The authors indicated, however, that seed choices observed in most of their experiments may have been influenced in part by differences in moisture content of seeds. In their experiments, seeds of different moldiness levels were produced by inoculating barley seeds with fungal spores and incubating the seeds at 100% relative humidity for various lengths of time. Seeds kept in high humidities gradually imbibe water over a period of days (Christian and Lederle, 1984; Morton and MacMillen, 1982). Experiments in which husked barley seeds were incubated at 100% relative humidity indicate that the moldy seeds produced by Reichman and Rebar (1985) may have contained as much as three times as much water as nonmoldy seeds used (Frank, 1988). Seeds presented to the rodents, consequently, differed greatly in water content as well as moldiness, except in a final experiment performed by the authors in which moisture levels in seeds were controlled. Heteromyid rodents do not drink water, but rely upon preformed water in their diet and metabolic water produced by the oxidation of food (Schmidt-Nielsen, 1964, 1972). Feeding trials with D. merriami (Frank, 1988) demonstrated that kangaroo rats can detect differences in moisture content in seeds as small as 10% and that they select seeds that contain the most water. Therefore, the slightly moldy seeds may have been selected only because they were more moist than nonmoldy seeds, but not yet moldy enough to be toxic. Kangaroo-rat burrows and caches in the field usually are more humid than the external environment (Kay and Whitford, 1978; Schmidt-Nielsen and Schmidt-Nielsen, 1950). Humid conditions within rodent burrows are ideal for fungal colonization of seeds because fungi require high humidities to grow (Martin and Gilman, 1976), thus seeds in kangaroo rat caches often may be both moldy and moist. Laboratory experiments suggest that D. spectabilis caches nonmoldy seeds preferentially in areas of high relative humidity, but when they become slightly moldy, they are moved to low humidities that inhibit further mold growth (Reichman et al., 1986). The rodents may be moving their caches to different humidities to increase water content and to control moldiness of seeds. To better understand the influence of moldiness level on