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Golden mouse (Ochrotomys nuttalli) and white-footed mouse (Peromyscus leucopus) dietary resource partitioning under experimental field conditions.

ABSTRACT

Ochrotomys nuttalli and Peromyscus leucopus are two small-mammal species that have similar life histories. This results in a relationship with a high degree of sociality between the two species, including extreme niche overlap. We investigated differences in diet preference and daily caloric intake under experimental field conditions in order to clarify this close relationship. Diets were based on reported food preferences in their natural environment. Five food resources were provided to 20 adult individuals (10 male, 10 female) of each species for three consecutive days. Individuals were contained in separate covered mesocosm tanks located in a riparian forest ecosystem. White-footed mice consumed more energy per day than golden mice (0.89 and 0.70 kcal * g live [wt.sup.-1] respectively), which is considerably less (2.38 and 1.48 kcal * g live [wt.sup.-1] respectively) than those reported by Gibbes and Barrett (1) when fed identical diets under controlled, laboratory conditions (22 [degrees] C). This study also suggests that nest cavities and soundscape assist in mitigating environmental perturbations, such as food scarcity and predation, in their natural habitat.

Keywords: dietary resource partitioning, Ochrotomys nuttalli, Peromyscus leucopus, mesocosm, soundscape

INTRODUCTION

Past investigations of similar small-mammal species have examined the roles of competition (2), (3), (4), and niche partitioning (5), (6). However, only recently has ecological facilitation via shared resources been considered important among species of plants and animals (7), (8). This study queried how dietary resource partitioning might partially explain the coexistence of two species of small mammals with similar life histories. The golden mouse (Ochrotomys nuttalli) and white-footed mouse (Peromyscus leucopus) have similar life histories, body masses, nest-site preferences, food preferences, periods of activity, home-range sizes, and are semi-arboreal (9), (10), (11). It has been shown, however, that the species differ in how they inhabit three-dimensional space, with white-footed mice found more frequently at ground level and golden mice building globular or communal nests aboveground (2).

Additionally, these two species have been double-captured in the same live trap (13), and adult scrotal males have been observed in the same nest box together on different occasions (11). The competition exclusion principle (i.e., that no two species can occupy the same niche) does not explain this observed coexistence and, therefore, their close social; relationship in their natural environment warrants additional study. In a previous study (12), P. leucopus was removed from experimental grids to observe how its removal would affect O. nuttalli abundance. These researchers observed no significant difference in abundance between experimental and control grids. To further investigate the relationship, we addressed the differences in caloric intake and, diet preferences in semi-natural conditions to quantify both small-mammal species' dietary behavior.

Several studies have compared the bioenergetics of white-footed mice (P leucopus) and golden mice (O. nuttalli) under experimental laboratory conditions (1), (14), (15). However, this is the first comparative study quantifying the bioenergetics of these two species under field mesocosm conditions. We investigated the differences in caloric intake and diet preferences of both species by offering five different diets that are considered important in the diet of O. nuttalli and P leucopus (9), (15), (16), (17), (18), (19), (20), (21), (22). All of these diets are abundant seasonally within our experimental site. Three of them, flowering dogwood fruits (Cornus florida), water oak acorns (Quercus nigra), and white oak acorns (Q. alba), are from native species. However, Chinese privet seeds (Ligustrum sinense) and staghorn sumac seeds (Rhus typhina) are from invasive species. We hypothesized that the three native diets would rank higher as dietary food preferences than the two nonnative diets, particularly C. florida and Q. nigra due to the caloric and food quality of these two diets. We also hypothesized that the animals fed under experimental field conditions would consume a higher caloric diet compared with the animals fed under laboratory conditions in the Gibbes and Barrett (1) experiment due to the much lower ambient temperatures experienced by the mice in their natural environment, and their endothermic nature.

MATERIALS AND METHODS

This study was conducted during spring, 2010, at the HorseShoe Bend (HSB) Ecology Experimental Research Site in proximity to Athens, GA (33 [degrees] 57' N, 83 [degrees] 23' W). HSB is a 14.2-ha forested peninsula created by the meandering North Oconee River. Five food resources, reported as important in the diet of O. nuttalli and P. leucopus, were collected in the fall of 2009, and then stored in a refrigerator before the feeding experiment. These.diets were Chinese privet seeds (L. sinense), flowering dogwood fruits (C, florida), staghorn sumac seeds (R. typhina), water oak acorns (Q. nigra), and white oak acorns (Q. alba). Table I summarizes the caloric values and percentage protein for each food item. Ten adults of each species (5 male, 5 female) were collected from nest boxes or live traps at HSB. At HSB each animal was released into one of five cylindrical mesocosm tanks (80 cm in diameter, 88 cm in depth) located in the forest riparian habitat. Each mesocosm tank was covered by a sheet of outdoor plywood, and contained a nest box (18.5 cm in width, 27.5 cm in length, and 20.5 cm in height), including nonabsorbent cotton (nesting material), situated in the center. Each nest box was positioned 5 cm above the bottom of the tank with a central entrance/escape portal (3.5 cm in diameter) located at the base of the nest box. Around the edge of the tank, located 72 [degrees] apart, were five ceramic food dishes; each dish contained one of the five food items. Each animal was acclimated in the mesocosm tank, which included water and each diet, for 24 hours.
Table I. Summary of caloric values (Kcal * g live wt-(1) [+ or -] SD)
and percentage protein for each food item based on 5 samples per diet.

       Diet             Caloric value      Percentage protein

Quercus nigra         5.2[+ or -]0.17 (a)    3.99[+ or -]0.10
Quercus alba          3.6[+ or -]0.03 (a)    4.68[+ or -]0.07
Cornus florida        5.2[+ or -]0.12        7.90[+ or -]0.03
Ligustrum sirtense    4.8[+ or -]0.13       10.46[+ or -]0.03
Rhus typhina          4.6[+ or -]0.18        5.93[+ or -]0.23

Note: After Gibbes and Barrett (1)
(a.) Acorn minus outer pericarp shell


Individual feeding studies were conducted for three consecutive days between 23 January and 6 April 2010 following the one-day acclimation period. At the beginning of each day, each of the five dietary options (~ 5 g per container, weighed to the nearest 0.1 g) was placed into the tank. After 24 h, the remaining food from each diet was weighed and recorded. Weight of the seeds and fruits remaining was subtracted from the weight of seeds and fruit initially placed in each dish to determine the amount of food consumed (Kcal * g live [wt.sup.-1] * [day.sup.-1]). Five petri dishes containing 10 g of flowering dogwood and Chinese privet were placed in a drying oven at 40 [degrees] C for 72 h to determine the water content in both diets. Ambient maximum/minimum temperature data were collected from the weather station at Athens-Ben Epps Airport (AHN). Thermometers also were placed in the mesocosm tanks to measure maximum/minimum temperatures inside the tanks. We followed guidelines approved by The American Society of Mammalogists for the Use of Wild Animals in Research (23) and The University of Georgia Animal Care and Use Committee (AUP #A2010 7-116).

This study was a "split-plot" design because we were interested in (a) comparing rates of ingestion for each small-mammal species and sex, and (b) the dietary preference and rate of ingestion for individual mouse. We performed an ANOVA to identify significant predictors of consumption (i.e., species, sex, and diet). The criterion for statistical significance was P [less than or equal to] 0.05.

RESULTS

The ranking of food preferences based on Kcals consumed (Kcal * g live [Wt.sup.-1] * [day.sup.-1]) for male golden mice was water oak > white oak > flowering dogwood > Chinese privet > staghorn sumac, and for male white-footed mice the ranking of food preferences was water oak > white oak > Chinese privet > flowering dogwood > staghorn sumac. For female golden mice the food preference ranking was water oak > white oak > Chinese privet > staghorn sumac > flowering dogwood, and for female white-footed mice the food preference ranking was water oak > white oak > flowering dogwood > Chinese privet > staghorn sumac. The rate of ingestion for male P. leucopus (0.91 [+ or -] 0.18 SD Kcal * g live [wt.sup.-1] * [day.sup.-1]) was greater than male O. nuttalli (0.72 [+ or -] 0.12 SD Kcal * g live [wt.sup.-1] * [day.sup.-1]), the rate of ingestion for female P. leucopus (0.86 [+ or -] 0.22 SD Kcal * g live wt"1 * day'1) was also greater than female O. nuttalli (0.68 [+ or -] 0.09 SD Kcal * g live [wt.sup.-1] * [day.sup.-1]). The average daily ambient high temperature for male O. nuttalli was 20 [degrees] C and the average low was 4.1 [degrees] C, and for female O. nuttalli the average high was 21 [degrees] C and the average low was 4.8 [degrees] C. For male P. leucopus the average high was 16.5 [degrees] C and the average low was 4.9 [degrees] C; for female P. leucopus the average high was 14.4 [degrees] C and the average low was 3.5 [degrees] C.

The most parsimonious model identified for these data indicated species and diet as the two statistically significant predictors of caloric consumption (the P < 0.05 level of significance). There was no significant interaction found between species and diet, indicating the two species of small mammals have similar preferences regarding the proportion of caloric consumption from each diet. P. leucopus consumed significantly more daily calories per diet on average than O. nuttalli (0.89 and 0.70 kcal * g live [wt.sup.-1], respectively). Q. nigra was preferred to all other diets for both species, and Q. alba was preferred to C. florida, L. sinense, and R. typhina for both species (Fig.1).

[FIGURE 1 OMITTED]

DISCUSSION

Several studies have focused on the bioenergetics of the white-footed mouse and the golden mouse (14), (15), (24), (25), (26), (27). Each of these stud-ies was conducted under laboratory conditions, typically in metabolism units at room temperature (~ 20-22 [degrees] C). Only Layne and Dolan (28) attempted to investigate bioenergetics of P.nuttalli in varying ambient temperatures and to compare these data with P leucopus. The objective of our investigation was to compare the bioenergetics of P leucopus and O. nuttolli under natural, mesocosm field conditions. We hypothesized that both species would exhibit higher rates of food ingestion under natural ambient temperatures ranging from 4.1 [degrees] C at night to 21.0 [degrees] C during daytime hours.

To our surprise, the ingestion values were considerably less (0.89 and 0.70 Kcal * g live [wt.sup.-1] * [day.sup.-1]) than those reported by Gibbes and Barrett (1) for R leucopus and O. nuttalli (2.38 and 1.48 Kcal * g live [wt.sup.-1] * [day.sup.-1]) when fed identical diets under controlled laboratory mesocosm conditions (22 [degrees] C). These values, however, were similar to the ingestion values (0.82 and 0.61 Kcal * g live [wt.sup.-1] * [day.sup.-1] for P. leucopus and O. nuttalli, respectively) measured at 20 [degrees] C by Knuth and Barrett (14). Table II is a summary of ingestion values for O. nuttalli and P. leucopus when fed a variety of diets under controlled laboratory conditions. Our study is the first to use a mesocosm established in a riparian forest habitat and exposed to natural ambient temperature conditions and functioning within a natural biophony soundscape (29).
Table II. Summary of ingestion values (Kcal * g live [wt.sup.-1] *
[day.sup.-1]) for 0. nut-talli and P. leucopus based on a diversity
of diets when fed under controlled laboratory conditions.

                      Rate of
Treatment            ingestion            Diet             Citation

Grouped O. nuttalli       0.41  Husked sunflower seeds         25

Ungrouped O.              0.50  Husked sunflower seeds         25
nuttalli

O. nuttalli               0.61  Rubus frondosus, Prunus        14
                                serotina, Zea

P leucopus                0.82  mays, Lonicero mackii,         14
                                and Rhus typhina

O. nuttalli               0.80  Purina lab chow (75%)          24
                                Sunflower seeds (25%)

O. nuttalli               0.09  Smooth sumac (1 year           27
                                old)

O. nuttalli               0.95  Japanese honeysuckle           26
                                berries

0. nuttalli               0.42  Eastern red cedar              26
                                berries

0. nuttalli
                          1.06  Water oak acorns and           15

P. leucopus               1.72  Privet berries                 15

0. nuttalli               1.48  Water oak and white oak         1
                                acorns,

P leucopus                2.38  staghorn sumac, privet          1
                                seeds, and flowering
                                dogwood fruits


Our rates of ingestion values (0.70 Kcal * g live [wt.sup.-1] * [day.sup.-1] for O. nuttalli and 0.89 Kcal * g live [wt.sup.-1] * [day.sup.-1] for P. leucopus) under field conditions were considerably less than those ingestion values reported by O'Malley et al. (15) and Gibbes and Barrett (1) under controlled laboratory conditions (20-22 [degrees] C). Individual mice of both species participating in our study, even under colder nocturnal conditions, collected water oak acorns (their diet of preference) and mostly consumed this dietary resource while in the their nest box; the nest-box cavity had numerous acorn shells each morning. Q. nigra shared the highest caloric value (5.2 Kcal * g dry [wt.sup.-1]) of the five diets, while also an easily cached and consumed food resource. Over 90% of the assimilated energy by each species is used for respiration (14). Therefore, we hypothesized that under natural ambient temperatures (the average daily minimum temperature was 4.5 [degrees] C for O. nuttalli and P. leucopus), individuals would have higher average rates of ingestion compared to individuals under controlled laboratory conditions of 20-22 [degrees] C in order to maintain body temperatures necessary for important metabolic processes. However, that was not what we observed. The natural environment appears to have a different effect on the behavior of the study individuals. For example, both species spent less time foraging, though more time foraging cacheable diets and feeding in their insulated nest boxes. They also heard predators, such as owls, and instinctively sought refuge in the nest boxes. This observation helps to explain why these species of small mammals cache acorns in nest cavities during winter months - a strategy that provides a food resource during months of food scarcity, while avoiding avian predators in low foliage cover. We recommend that future bioenergetics or behavioral studies be conducted under natural field conditions.

ACKNOWLEDGMENTS

We thank the cadre of researchers at the HorseShoe Bend Ecology Experimental Site for helping to capture the small mammals used in this investigation. We thank Amanda Bramlett and Kim Love-Meyers, Statistical Consulting Center, Department of Statistics, University of Georgia, for statistical analyses. We thank Terry L. Barrett for critical review of this manuscript. We are grateful to Mark A. Froetschel, Department of Animal and Dairy Science, University of Georgia, for assistance in caloric and nutritional analyses. This study was supported in part by funds from the Eugene P. Odum Endowed Chair in Ecology held by Gary W. Barrett.

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Alexander D. Wright and Gary W. Barrett *

Eugene P. Odum School of Ecology University of Georgia Athens, GA 30602

* Corresponding Author: gbarrett@uga.edu
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Author:Wright, Alexander D.; Barrett, Gary W.
Publication:Georgia Journal of Science
Article Type:Report
Geographic Code:1USA
Date:Jun 22, 2011
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