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Adult foraging Behavior in mearns' grasshopper mouse, Onychomys arenicola (Rodentia: Muridae) is influenced by early olfactory experience.

Abstract. -- Studies were conducted to assess the effects of early exposure to food-borne olfactory cues and subsequent searching behavior and odor preferences in adult males of the grasshopper mouse, Onychomys arenicola. Twenty-day old mice were randomly assigned to 1 of 3 treatment groups: a control group (CG) was fed on crickets (Acheta domesticus) and mealworms (Tenebrio molitor). Another group (EG) received an enriched diet of crickets, mealworms, roaches (Periplaneta americana), and commercial dog and cat chow. The IG group received an impoverished diet consisting only of crickets. These feeding regimes continued for 80 days. Mice were then presented with odor choice tests in a Y-maze olfactometer. Mice from each treatment group were tested for their choices between known and novel prey odors (NPO), and between known odors and a novel pure chemical odor (NCO). Control mice exhibited a preference of 70% for the known prey odor (cricket) and only 30% for the NPO (wolf spider, Hogna carolinensis). In contrast, EG mice showed a significantly higher preference (70%) toward the NPO. Only 20% of the IG animals chose the NPO. In addition, EG mice made decisions on which odor to investigate significantly faster than CG or IG animals. These results indicate that O. arenicola relies on olfactory cues when making decisions concerning prey choice during foraging bouts. They also suggest that knowledge of olfactory cues associated with prey is not innate in this species, but is acquired during early sensitive periods of development (olfactory imprinting). This is the first demonstration of olfactory imprinting in a murid rodent within the genus Onychomys.

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Previous studies have shown that early olfactory experience can affect the subsequent foraging behaviors or prey choice of adult predators including insects (Chapman et al. 1987), spiders (Punzo & Kukoyi 1997), rock crabs (Rebach 1996), turtles (Punzo & Alton 2002), lizards (Punzo 2003a), polecats (Apfelbach 1973), ferrets and other mustelids (Apfelbach 1992), murid rodents (Berdoy & Macdonald 1991), shrews (Churchfield 1990; Punzo 2003b) and canids (Weldon 1990). Furthermore, a study on the ferret Mustela putorius showed that olfactory imprinting may be involved because certain odors encountered by young animals during sensitive periods can serve as acquired sign stimuli for subsequent prey identification and selection (Apfelbach 1992). However, little information is available on the effects, if any, of early olfactory experiences on subsequent foraging behavior in murid rodents (Frank & Heske 1992).

Mearns' grasshopper mouse, Onychomys arenicola (Rodentia: Muridae) is an inhabitant of low desert areas in west Texas. They prefer foothills, xeric flats and mesquite-covered mesas with sandy soils (Whitaker 1996), and feed primarily on a variety of arthropods and small vertebrates as well as seeds (Horner et al. 1965; Brown & Zeng 1989; Punzo 2000). The purpose of the present study was to assess the influence of early olfactory experience on subsequent searching behavior and odor preferences of adults of O. arenicola.

MATERIALS AND METHODS

All animals used in these experiments were the second or third generation offspring of adults originally collected from several localities within a 4 km radius of Redford, Texas (Presidio County) in 1999 and 2000. This area lies within the northern region of the Chihuahuan Desert. The experimental protocol used in this study was similar to that employed by Apfelbach (1978). To summarize, 10 newly weaned mice were randomly assigned to each of three groups, all of which were fed a diet of crickets (Acheta domesticus) and mealworms (Tenebrio molitor) until they were 20 days old. After this time, each group was fed on a different diet regime until the age of 80 days. A control group (CG) continued to receive crickets and mealworms; another group (EG) was fed an "enriched" diet consisting of crickets, mealworms, roaches (Periplaneta americana) and commercial cat and dog chow (Ralston Purina, St. Louis, MO). An impoverished group (IG) received only crickets. In addition, to enhance olfactory deprivation, the IG group was exposed to an artificial olfactory environment saturated with the odor of geraniol. It has been reported that the continuous exposure to a single predominant odor can mask the ability of an animal to experience other environmental odors resulting in what has been termed a state of olfactory deprivation (Weldon 1990).

Behavioral studies were conducted on adult males from the three groups (n = 10/group) when they reached 7 months of age. These animals were tested in a Y-maze olfactometer to determine if there was any preference shown toward certain odor cues. Two tests were given to each animal: one in which the subject was given a choice between a known prey odor and a novel prey odor, and another test where the choice was between a known prey odor and a novel pure chemical odor. There was a 10 min delay between tests. The general procedure was similar to that employed by Apfelbach (1992). To summarize, the olfactometer consisted of a Y-maze constructed of plexiglass (Fig. 1) connected to sources of odor via glass tubing (GT). The air and odor flow were controlled through the use of flowmeters (F) located before and after the odor saturators (odors). Teflon valves (V), located at each end of the Y-maze, were used to control the direction of flow of the odors. Test odors were randomly introduced into the left or right end of the maze before a mouse was allowed to leave the start box. Test odors consisted of a known prey odor (cricket), a novel prey odor (wolf spider, Hogna carolinensis) and a novel pure chemical odor (oil of wintergreen). At the start of each trial an individual mouse, food-deprived for 72 hr, was placed into the start box and allowed to remain there for a period of 10 min. The start box door was then lifted, and the mouse was allowed to enter the maze. A record was made of which arm of the maze was chosen (% choice) for each trial, as well as the time (sec) needed for a mouse to make its decision. An arm was considered chosen if the animal moved into it at least as far as point C or F. All observations were made behind a one-way mirror to minimize disturbance to the animals.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Data on odor preference tests and time needed to make a decision were analyzed using Chi-Squared and Kruskal-Wallis tests (Sokal & Rohlf 1995).

RESULTS

The results of the odor preference tests are shown in Fig. 2. In the choice condition of known prey odor (crickets) versus novel prey odor (NPO; wolf spiders), control animals (CG) exhibited a preference of 30% toward the NPO, and 70% to the cricket odor. In contrast, animals exposed to an enriched diet (EG) showed a preference of 70% toward the NPO, whereas only 20% of the IG animals chose the NPO. The differences between the CG and EG, and between CG and IG were significant (P < 0.01). In addition, novel chemical odors (NCO) were less attractive to these mice than were novel prey odors.

[FIGURE 3 OMITTED]

The time needed by these animals to make a decision as to which odor to investigate is shown in Fig. 3. In the choice condition of known prey odor vs. NPO, mice exposed to the enriched diet (EG) made decisions significantly faster than controls (P < 0.01) and IG (P < 0.001) animals. Similar results were obtained when a novel chemical odor (NCO) was presented rather than a NPO.

DISCUSSION

These results indicate that the cricetid rodent Onychomys arenicola utilizes olfactory cues when making decisions during foraging bouts. They also suggest that knowledge of olfactory cues associated with prey is not innate in this species, but is acquired during early periods of development. This type of olfactory imprinting on cues associated with prey or other food items has been reported for animals from a diversity of taxa including insects (Thorpe 1939; Chapman et al. 1987), spiders (Punzo & Kukoyi 1997), turtles (Burghardt & Hess 1966; Punzo & Alton 2002), lizards (Punzo 2003a), polecats (Apfelbach 1973), ferrets (Apfelbach 1992), and murid rodents (Berdoy & Macdonald 1991). To the author's knowledge, this is the first demonstration of olfactory imprinting in a murid rodent within the genus Onychomys.

It has been argued that the ability to imprint on specific environmental cues during an early sensitive maturational period would allow an animal to combine the advantages of hardwired specialist feeders with those of generalists who rely to a greater extent on learning (Johnston 1982; Stephens 1991). The situation whereby a predator is exposed to only a small number of prey items during some early sensitive period of life might facilitate the formation of an olfactory search image, thereby focusing food searching behavior for specific prey (Burghardt 1993). Thus, even though an animal may have the capacity to feed on a variety of food types (broad trophic niche), by concentrating on a single, abundant and reliable food encountered early in life, individuals would minimize energy costs associated with trial-and-error learning while benefiting from the increased foraging efficiency associated with having a single search image to facilitate hunting. In these experiments, grasshopper mice that were exposed to only a small number of prey objects early in life, did not respond strongly to novel prey odors and even less to a novel chemical odor, both of which convey less important olfactory information.

Onychomys arenicola is found in xeric habitats, where seasonal fluctuations in prey availability are common (Punzo 2000). Although it is a generalist predator that feeds on a variety of arthropods, small vertebrates and seeds (Horner et al. 1965; Brown & Zeng 1989; Whitaker 1996), the ability to form an early search image associated with one or a few prey types that may be more locally abundant and available, would contribute to its overall fitness.

ACKNOWLEDGMENTS

I thank R. J. Edwards, S. Jenkins, C. Lowell, G. Price and anonymous reviewers for comments on an earlier draft of the manuscript, L. Hane for assistance in procuring some of the research literature, and A. Nardelli for assistance in maintaining the animals in captivity. This study was supported by a Faculty Development Grant from the University of Tampa.

LITERATURE CITED

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Whitaker, J. O., Jr. 1996. Field guide to North American mammals. Alfred Knopf, New York, 936 pp.

Fred Punzo

Department of Biology

University of Tampa

Tampa, Florida 33606

FP at: fpunzo@ut.edu
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Author:Punzo, Fred
Publication:The Texas Journal of Science
Geographic Code:1U2NY
Date:May 1, 2004
Words:2192
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