Predation and Population Density of White-Footed Mice

ABSTRACT

THE EFFECTS OF PREDATION AND SUPPLEMENTAL FOOD ON FORAGING AND ABUNDANCE OF WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS) IN RELATION TO FOREST PATCH SIZE by Gregg Marcello

The purpose of this study was to examine some of the possible causes for the negative density-area relationship reported for the white-footed mouse, Peromyscus leucopus. I examined predation and food availability in three small and three large forest fragments. Giving up density trays and various odors were used to test the variation in foraging behavior in the presence of a predator odor. Nest boxes and counts of periodical cicada emergence holes were used to test the effects of an emergence of periodical cicadas on P. leucopus population densities. Predator odors had no effect on foraging behaviors. P. leucopus responded to indirect, but not direct, cues of predation. Estimated densities of periodical cicada emergence holes were strongly related to the relative population density of P. leucopus. Continued study of predation and food differences in forest fragments of different sizes is needed to further examine the negative density-area relationship of P. leucopus.

THE EFFECTS OF PREDATION AND SUPPLEMENTAL FOOD ON FORAGING AND ABUNDANCE OF WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS) IN RELATION TO FOREST PATCH SIZE

A Thesis Submitted to the Faculty of Miami University In partial fulfillment of The requirements for the degree of Master of Science Department of Zoology by Gregory James Marcello Miami University Oxford, OH 2005

______Douglas B. Meikle (Advisor)

______Nancy G. Solomon (Reader)

______Thomas O. Crist

______Robert L. Schaefer TABLE OF CONTENTS Page List of tables iii List of figures iv Dedication v Acknowledgements vi Chapter 1 Introduction 1 Chapter 2 Predation and population density of white-footed mice (Peromyscus leucopus) in relation to forest patch size Introduction 3 Methods 6 Results 8 Discussion 8 Chapter 3 Effects of periodical cicadas on population densities of Peromyscus leucopus in relation to forest patch size Introduction 14 Methods 16 Results 18 Discussion 19 Chapter 4 Summary 28 Literature Cited 31

ii LIST OF TABLES Table 1: Mean giving up density (±SEM) for edge and interior habitat in small and large forest fragments outside of Oxford, OH in 2004

Table 2: Mean values (±SEM) for forest fragments outside of Oxford, OH in 2004

Table 3: Mean values (±SEM) for forest fragments outside of Oxford, OH in 2002

iii LIST OF FIGURES Figure 1: Diagram of the olfactometer used in the scent response portion of the study

Figure 2: Mean giving up density (mean dry mass+SEM) of seeds in each month in A) small and large fragments and B) edge and interior habitat outside of Oxford, OH. GUDs are significantly different in each month (p=0.0002) but not in different sizes (p=0.15) or habitats (p=0.71).

Figure 3: Relationship between the mean number of white-footed mice and mean number of cicada emergence holes in forest fragments outside of Oxford, OH

Figure 4: Density-fragment area relationship for white-footed mice (mean+SEM) in forest

fragments outside of Oxford, OH in 2002 and 2004. The year by size interaction is significant (F

(1,120) =11.35, p=0.001).

Figure 5: Relationship between mean number of white-footed mice and complexity of understory vegetation in forest fragments outside of Oxford, OH in 2002 and 2004

iv DEDICATION I would like to dedicate this thesis to my parents, Vince and Betty Marcello, for giving me a good start and to my fiancée, Vicki Smith, for keeping me on track. Without that combination, I would not be where I am today. I would also like to dedicate this to my advisor, Doug Meikle, for providing a direction and a focus for my efforts.

v ACKNOWLEDGEMENTS I would like to thank my advisor, Doug Meikle, for his help and support on this project. I would also like to thank my committee, Tom Crist, Bob Schaefer, and Nancy Solomon. Their assistance with experimental design, statistical analysis, and overall knowledge has been invaluable. I would also like to thank the landowners in Ohio and Indiana for allowing me onto their property to conduct my research. The Ohio DNR, the Indiana Division of Fish and Wildlife, and the Naturals Areas Committee of Miami University also provided permission to conduct this study. My project was funded by the Department of Zoology at Miami University. I would like to thank several people for assistance in the field: G. Sizemore, V. Smith, G. Gerald, T. Levine, L. Spezzano, A. Duncan, and L. Douglas. Finally, I would like to thank C. Anderson and S. Wilder for blazing a trail for me to follow.

vi Chapter 1 INTRODUCTION Destruction of most of the continuous forested habitat and subsequent patchy regrowth of forest has resulted in the current fragmented forest landscape of the eastern United States (Yahner 1988, Fahrig 1997, Anderson et al. 2003). Small forest fragments may differ from large forest fragments in several ways (Nupp and Swihart 1996, Fuller and Kittredge 1996, Thorson et al. 1998). Smaller fragments have a greater proportion of edge to interior habitat than larger ones (Bowers and Dooley 1993, Wolf and Batzli 2001). Edge habitat differs from the forest interior in several abiotic factors (Laurance and Yensen 1991, Anderson et al. 2003). There are steep environmental gradients of light, temperature, and wind that decrease from edge to interior (Burke and Nol 1998). Many mammal species have higher population densities in larger than in smaller forest fragments, and some species show no relationship between density and forest fragment size (Bowers and Matter 1997, Connor et al. 2000, Anderson et al. 2003). However, some generalist forest rodents (e.g. Peromyscus leucopus, the white-footed mouse, and Apodemus sylvaticus, the wood mouse), have been shown to have a negative relationship between density and forest fragment size (Nupp and Swihart 1996, 1998, 2000; Diaz et al. 1999; Anderson et al. 2003). This negative relationship is important because such species play an integral part in community structure and function due to their important ecological role as prey, predator, and competitor. Raptors, reptiles, and mammals prey on white-footed mice (Kirkpatrick and Conway 1947, Hockman and Chapman 1983, Durner and Gates 1993). The mice, in turn, are predators of seeds, invertebrates, and passerine bird nests (Schmidt et al. 2001, Ostfeld et al. 1997). Hence, investigating the negative relationship between density and forest fragment size for P. leucopus may help to understand the effects of forest fragmentation on animal and plant community structure. Several factors may drive the negative relationship between density of P. leucopus and forest fragment area. In my study, I examined two of these possible factors in forest fragments of different sizes: predation and food availability. Predation is difficult to study directly, in part because predators generally have a larger home range than their prey, and are therefore harder to locate and monitor than prey. In addition, it is difficult to capture an actual predation event either visually or on film. Investigators are usually unable to determine if animals are not

1 recaptured due to predation, dispersal, or chance. To avoid some of these difficulties, I examined the responses of the prey, P. leucopus, to the perceived risk of predation rather than actual predation rates. Specifically, I experimentally tested whether mice in small fragments showed less of a response to predation risk than did mice in larger fragments. In the second part of my study, I examined the relative population density of P. leucopus in a situation where food was unlikely to be the limiting factor to population size. A 2004 emergence of periodical cicadas in much of the midwestern United States provided the opportunity to test the effect of a superabundant supplemental food source on populations of mice in forest fragments of different sizes. Many experiments using food supplementation can be faced with potential difficulties; however, by using periodical cicadas, a widespread, naturally occurring food source, I was able to avoid some of these difficulties. I investigated the hypothesis that an emergence of periodical cicadas would have a positive effect on the relative population density of P. leucopus because they would be a source of food for the mice.

2 Chapter 2 Manuscript title: PREDATION AND POPULATION DENSITY OF WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS) IN RELATION TO FOREST PATCH SIZE Introduction Removal of most of the continuous forested habitat for agricultural purposes and suburban development has resulted in a fragmented forest landscape across much of the eastern United States (Yahner 1988, Fahrig 1997, Anderson et al. 2003). Small forest fragments may differ from large fragments in several biotic and abiotic factors (Nupp and Swihart 1996, Thorson et al. 1998, Fuller and Kittredge 1996). Many animal species have higher population densities in larger than in smaller forest fragments, and some species show no relationship between density and forest fragment size (Bowers and Matter 1997, Connor et al. 2000, Anderson et al. 2003). However, some generalist forest rodents (e.g. Peromyscus leucopus, the white-footed mouse, and Apodemus sylvaticus, the wood mouse), have been shown to have a negative relationship between density and forest fragment size (Nupp and Swihart 1996, 1998, 2000; Diaz et al. 1999; Anderson et al. 2003). This negative relationship may be of significance because such species can affect many other species due to their important ecological role as prey, predator, and competitor. The reasons for the negative relationship between habitat area and density for P. leucopus are not well understood, but several factors may be responsible. Nupp and Swihart (1996) hypothesized that small fragments may contain fewer competitors for food and space, thus allowing P. leucopus to reach higher densities than in larger fragments. However, P. leucopus consumes a wider variety of food resources relative to many of its granivore competitors (Ivan and Swihart 2000). Furthermore, P. leucopus shows no preference for seed type regardless of nutrient content or size (Ivan and Swihart 2000). This suggests that competition for food may not be as important a factor in controlling densities of mice as it seems to be, although experimental evidence for the presence or absence of interspecific competition is lacking. Small forest fragments may have a greater availability of food due to both primary (e.g., fruits and seeds) and secondary (e.g., invertebrates) production (Parmenter and MacMahon 1983, Yahner 1992, Ostfeld et al. 1996, Wilder and Meikle in press a). The greater food resources may be due to greater complexity of understory vegetation in small fragments, especially in edge

3 habitat (Anderson et al. 2003). Since small fragments have a larger proportion of edge to interior habitat than large fragments, they may allow a generalist species such as the white-footed mouse to maintain high population densities (Anderson et al. 2003, Wilder and Meikle in press a, Wilder and Meikle in press b). Another factor that may contribute to the negative density-habitat area relationship of P. leucopus is lower predation pressure in small forest fragments due to fewer predators (Fuller and Kettredge 1996) or increased vegetative cover from predators (Lima and Dill 1990). Due to their high vagility, predators could visit several small fragments while hunting. Yet some evidence suggests that predators are less likely to be present as often in small as in large fragments (Kirkpatrick and Conway 1947, Hockman and Chapman 1983). Hence, it is not understood how predation influences the relative abundance of P. leucopus in relation to forest fragment size. Animals are expected to use a resource-rich over a resource-poor patch in the presence of a predation risk (Brown 1988). Holtcamp et al. (1997) showed that deer mice (Peromyscus maniculatus) spent more time foraging in a rich patch than a poor patch in the presence of a predator (fire ants) but no patch preference in the predator’s absence. This supports the idea that P. leucopus may reach higher densities in small fragments because of greater foraging gains combined with a decreased risk of predation. Mice in small fragments may have a lower risk of predation because those fragments have a proportionately greater amount of edge habitat (≤15 m from the field/forest transition) than large fragments. Edge habitats generally have a greater complexity of understory vegetation, which provides more cover from predation (Wolf and Batzli 2002, Anderson et al. 2003). Dickman (1992) showed that Mus domesticus in Australia preferred areas of greater vegetative complexity (i.e. more cover) when perceived risk of predation was high. By choosing areas where predators were naturally present or absent, Dickman (1992) was able to evaluate the responses of predator-naïve vs. experienced mice. Naïve mice showed no avoidance of predator odors (Dickman 1992). There was also no obvious use by naïve mice of dense vegetation in the presence of predator scent. Mice with some exposure to predators avoided traps with predator scent, even if the specific predator was unfamiliar. They also selected relatively dense vegetation in general; this predisposition was more pronounced in the presence of predator scent. Naïve and experienced mice were relocated to areas containing predators, and animals were later recaptured to assess survival rates. These transplantation experiments showed the use of dense

4 vegetation to be an effective anti-predator response in that experienced mice had survival rates that were almost three times greater than naïve mice (Dickman 1992). Habitat-use strategies by P. leucopus, similar to those reported by Dickman (1992) for Mus, have been shown in North America where P. leucopus have been exposed to predators for generations (Barnum et al. 1992). Understory vegetation, generally common in edge habitats, was shown to play a large role in pathway choice by P. leucopus. In particular, P. leucopus chose pathways that offered both visual and auditory protection from predation (Barnum et al. 1992). While the mice may not actively decide which forest fragment to live in, reduced predation pressure may allow greater recruitment and survival in small fragments, leading to higher population densities. I tested the hypothesis that P. leucopus exists at greater densities in small forest fragments, in particular the edges of small fragments, in part because there are fewer predators and mice may be able to avoid predation because of the greater complexity of understory vegetation. One way to compare predation effects in small vs. large fragments is to use the giving up density (GUD) of seeds in artificial foraging trays. The GUD is the amount of food remaining in a patch (i.e. tray) when an animal stops foraging (Brown 1988). GUDs provide a measure of the amount of effort an animal is willing to invest in foraging in one area. A high GUD (i.e. fewer seeds eaten) can indicate that the animal perceives high predation risk and/or that there is abundant food in the surrounding area (Brown 1988). When presented with foraging opportunities, mice should show less of a response to the scent of a predator if they perceive a lower risk of predation in a habitat. If there is reduced predation pressure in small fragments than in large, I predicted that giving up densities (GUDs) of seeds in foraging trays would be lower (i.e. more seeds eaten) in small fragments than large regardless of scent. I also predicted that the GUDs from both “control” and “control scent” (those with the odor of a nonpredator) trays would be lower than GUDs from predator scent trays. Finally, I predicted that this difference would exist in all fragments, but would be more pronounced in large fragments, particularly in the interior. These predictions are based on the hypotheses that there is reduced predation pressure in small fragments and that the mice are able to perceive the reduced level of predation and adjust their behavior accordingly (i.e. forage longer).

5 Other investigators have examined how predator odors can affect rodent foraging behavior (Orrock et al. 2004, Powell and Banks 2004). Orrock et al. (2004) used various scents in conjunction with GUD trays placed in different microhabitats to examine the response of oldfield mice (P. polionotus) to direct (predator odors) and indirect (amount of cover) cues of predation risk. Similarly, Powell and Banks (2004) used GUD trays with fox odor and varying microhabitat characteristics to examine the foraging behavior of house mice (Mus domesticus). Both studies reached similar conclusions: rodents base their foraging decisions on indirect cues of predation risk but not direct cues (Orrock et al. 2004, Powell and Banks 2004). However, neither study examined the possibility of differences in response to the odor of a predator in forest fragments of different sizes. Here I examine the potential differences in foraging by P. leucopus living in small and large forest fragments. Methods Study site I used six fragments of secondary-growth deciduous forest within 25 km of Oxford, OH (Butler and Preble Counties, OH and Franklin County, IN). Three of the fragments were 1-2 ha (small), and the other three were >100 ha (large). The surrounding matrix was primarily row crops (corn and soybeans), but some fragments were bordered by fields or pasture. Fragments were separated from the nearest forested area by at least 50 m. Responses to scent Prior to field experiments, a laboratory experiment was conducted to determine the response of P. leucopus to various commercially available predator scents. Forty mice (20 from a small fragment and 20 from a large fragment) were trapped and housed in the Miami University animal facility. These two fragments were not included in the six fragments in which the study was conducted. Ten males and ten females from each fragment were used in the trials. All mice were housed individually in polycarbonate “shoebox” cages (15x29x17 cm). The room was maintained at 20°C and at 40-60% relative humidity with a 14:10-h light-dark cycle. Water and Purina Mills Autoclavable Rodent Breeder Diet 5013 were available ad libitum. An olfactometer was used to observe the responses of mice to various odors (Figure 1). The olfactometer consists of a central chamber that has two darkened cylinders entering it from each side, about 2.5 cm above the floor of the central chamber. These cylinders are each connected by small tubing to two other small cylinders containing scent. The scents used were

6 from a typical predator (red fox, Vulpes vulpes; Hockman and Chapman 1983), an historical predator (bobcat, Lynx rufus; McLean et al. 2005), a nonpredator species (white-tailed deer, Odocoileus virginianus) to control for confounding effects of a strong odor (“control scent”), and distilled water (“control”). Air was pumped through each small cylinder and into the chamber with the subject. For each trial, a single mouse was placed in the central chamber. I recorded the duration of visits to one cylinder or the other, during a 20-min session (Meikle et al. 1995). Mice were considered to be in a cylinder when all four feet were up in the cylinder. I then compared the responses of mice to the odor of deer vs. water, fox vs. water, and bobcat vs. water and determined the intensity of the response to the different scents. The olfactometer was washed with soap and water between trials. In addition, three olfactometers were used to allow drying time between uses. Each mouse was tested with all three scents in random order, and there were at least three days between trials for the same mouse. Giving up densities To test the relative importance of predation in small vs. large forest fragments, I used giving up density (GUD) trays treated with either fox urine, deer urine, or distilled water. The results of the preliminary laboratory experiment indicated no significant differences in the responses of P. leucopus to any tested scent compared to controls. Foxes and deer are currently present in this area, and bobcats are not, hence, I chose to use scents that mice would be likely to encounter naturally. The GUD trays were plastic trays (32x16x8 cm) with Plexiglas lids. The clear lid simulated an open tray while still protecting the contents from the elements (Wilder and Meikle in press a). Treatments were applied to each tray by taping a cotton ball moistened with four drops of the appropriate liquid to the side of the tray. The trays were placed 1 m apart in triangular groups of three (fox, deer, and water) to form a station. In each fragment, stations were placed approximately 30 m apart in two rows of three stations each (n=18 trays per fragment). The rows were at approximately 5 m (edge habitat) and 50 m (interior habitat) from the forest edge. I based my definition of edge habitat on evidence that microclimate (i.e. light penetration and soil moisture) and understory vegetation (i.e. shrub cover and vegetation complexity) are greater within 15 m of the abrupt transition from field to forest than in more interior habitat (Ranney et al. 1981, Burke and Nol 1998, Gehlhausen et al. 2000, Anderson et al. 2003). Each tray contained 4 g of millet mixed into 1 L of sand. All trays were used

7 simultaneously for a one-night acclimation period followed by three nights of data collection, in August, September, and after leaf fall in December 2004. This design provided nine nights of GUD data for each fragment. After each night, the millet and scent were replenished. The remaining millet was cleaned, dried overnight in a 60°C oven, and weighed. Statistical analysis Responses to odors in the laboratory experiment were analyzed with a repeated measures analysis of variance (ANOVA; Proc MIXED, SAS Institute). A repeated measures ANOVA (Proc MIXED, SAS Institute) was also used to analyze GUDs. Factors in the model were fragment size, name of fragment, habitat, month, and scent. Post hoc analyses of effects were done using LSMEANS and Bonferroni tests. Only significant interactions were reported. Results The preliminary laboratory experiment showed that mice did not respond to any of the tested scents (F (2, 34) =0.51, p=0.6). Contrary to my predictions, there was no effect of scent on giving up density for P. leucopus (F (2, 8) =1.15, p=0.36). Likewise, there was no effect of forest fragment size (F (1, 4) =3.18, p=0.15) or habitat type (edge or interior; F (1, 4) =0.16, p=0.71).

However, the time of the year did have a significant effect (F (2, 8) =28.92, p=0.0002) with mean GUDs increasing from August to December (Table 1).

The month by habitat interaction was not significant (F (2, 10) =2.66, p=0.12). However, there was a nonsignificant tendency for GUDs to be higher in interior habitat than edge habitat in December (p=0.09). Conversely, the absolute value of the GUDs in September was higher in edge habitat than interior habitat (Figure 2). Discussion These results did not support the prediction that P. leucopus would alter its foraging behavior in the presence of a predator odor. However, they do indicate that perceived predation risk and abundance of food can affect GUDs. The differences in giving up densities in the different habitats from August to December may reflect seasonal changes in food availability and predation risk. Since forest fragment edges are more heavily vegetated than interiors (Anderson et al. 2003), the higher absolute value GUDs in the edge in September (which is prior to deciduous leaf fall) may be due to the abundance of fruits and seeds available in the fall (Parmenter and MacMahon 1983, Yahner 1992, Ostfeld et al. 1996, Wilder and Meikle in press a). However, in December, the higher GUDs in the less vegetated interior may be due to the

8 increase in the perceived risk of predation caused by leaf fall. Edges may be perceived as safer than interiors due to the woody structure of the remaining understory vegetation. I observed an overall tendency towards higher giving up densities in both edge and interior habitats in small forest fragments than in large forest fragments. This may be because small fragments generally have greater complexity of understory vegetation than large fragments. Hence, small forest fragments can have more food than large fragments, resulting in higher GUDs (Wilder and Meikle in press a). It is also possible the GUDs in small forest fragments could be higher because predators hunt them more intensively or mice perceive them to be more dangerous. However, it seems unlikely that this is the case, since the greater complexity of vegetation in small forest fragments would provide greater protection from aerial and some terrestrial predators (Wilder and Meikle in press a). This pattern may not have been significant because of the unusual amount of food that may potentially been available in large fragments due to fertilization (Yang 2004) by the emergence of periodical cicadas (Brood X) earlier in the year. My results are consistent with the findings of other researchers (Orrock et al. 2004, Powell and Banks 2004) that rodents base their foraging behaviors on indirect cues of predation risk (e.g. habitat structure) more than on direct cues (predator odors). Several researchers have shown that rodents base their use of microhabitat on habitat characteristics that reduce their risk of detection by predators (coarse woody debris, shrubs, etc.; Kaufman et al. 1983, Barnum et al. 1992, Matter et al. 1996, Roche et al. 1999). Since predator odors are presumably widespread in the environment (Powell and Banks 2004), it seems likely that odor cues are disregarded by foraging mice unless odors are accompanied by some other cue. When presented with no further indications of the immediate presence of a predator, the mouse must balance the risk of predation against the costs of a missed foraging opportunity (Charnov 1976), and indirect cues of predation risk, such as moonlight and/or vegetation complexity, become more important. While the results of the field component of my study support previous work (Orrock et al. 2004, Powell and Banks 2004), the laboratory portion showed no difference in the response of P. leucopus from forest fragments of different sizes to the odor of a predator. This could be due to the artificial testing environment. Choice experiments in an olfactometer probably do not accurately reflect actual decisions made during foraging. In addition, due to time and space constraints, scents were only compared to a control, not to other scents. Other odor avoidance

9 trials may reveal differences in response to scents. In addition, longer periods of observation in the odor avoidance trials may more closely simulate the duration of the field component and allow detection of potential changes in odor avoidance over time.

10 Figure 1: Diagram of the olfactometer used in the scent response portion of the study

Table 1: Mean giving up density (±SEM) for edge and interior habitat in small and large forest fragments outside of Oxford, OH in 2004

Small fragments Large fragments Edge Interior Edge Interior August 2.03±0.15 2.09±0.14 0.94±0.13 0.99±0.11 September 2.92±0.13 2.46±0.12 1.73±0.14 1.49±0.12 December 3.44±0.08 3.64±0.03 2.03±0.17 2.92±0.13

A 4.0 3.5 3.0 ) g (

2.5 D large U 2.0 G small 1.5 ean M 1.0 0.5 0.0 August September December Month

B 4.0 3.5 3.0 ) g (

2.5 D edge U 2.0 G interior 1.5 ean M 1.0 0.5 0.0 August September December Month

13 Chapter 3 Manuscript title: EFFECTS OF PERIODICAL CICADAS ON POPULATION DENSITIES OF PEROMYSCUS LEUCOPUS IN RELATION TO FOREST PATCH SIZE Introduction Densities of some mammalian species do not vary with fragment area, whereas some species show a positive relationship (Bowers and Matter 1997, Connor et al. 2000). In contrast, some forest rodent generalists such as Peromyscus leucopus (white-footed mice) and Apodemus sylvaticus (wood mice) consistently show a negative relationship between density and fragment area (Yahner 1992; Nupp and Swihart 1996, 1998; Diaz et al. 1999; Krohne and Hoch 1999; Mossman and Waser 2001; Anderson et al. 2003). One factor that may contribute to the negative density-area relationship shown by P. leucopus is that small fragments contain greater food resources for P. leucopus than large fragments (Bowers and Dooley 1993). More food can result in greater adult body masses, higher levels of reproduction and survivorship, and higher population densities (Doonan and Slade 1995, Nupp and Swihart 1996). Some investigators (e.g. Hansen and Batzli 1979, Taitt 1981, Briggs 1986, Wolff 1986, Krohne et al. 1991) have used supplemental food to determine whether food resources influence the population density of P. leucopus, but these studies have produced conflicting results. For example, Wolff (1986) and Krohne et al. (1991) reported little or no effect of supplemental food on densities of P. leucopus. On the other hand, Briggs (1986) reported that some populations receiving supplemental food increased relative to a control population. Use of commercial rodent chow or unnatural dispersion patterns such as regularly spaced feeding stations may confound the results of supplemental feeding studies (Krohne et al. 1991). One solution to the potential problems of provisioning animals with food is to use a naturally occurring food source to test the effects of food on the population density of P. leucopus. Yunger (2002) reported an increase in a population of P. leucopus that lived in a fragment that produced a large mast crop, but he attributed it to increased immigration rather than reproduction. Variation in local tree community composition can result in mast crops in discrete areas (Yunger 2002), and animals may immigrate to those areas to take advantage of such a localized abundant resource. However, an emergence of 17-year periodical cicadas

14 (Brood X, Magicicada spp.), such as occurred in 1987 and 2004, provided an opportunity to test the effects of supplemental food on P. leucopus because it presented a naturally occurring, superabundant source of food that was widespread across the entire landscape (Ostfeld and Keesing 2004, Hahus and Smith 1990). Because of their distribution, however, periodical cicada studies lack the controls that other supplemental feeding studies can have. Krohne et al. (1991) compared the population densities of P. leucopus and Blarina brevicauda (Northern short-tailed shrew) during a Brood X cicada emergence in 1987 to their densities in seven other years. B. brevicauda (an insectivore) showed a clear increase in density in response to the increased food supply. Densities of P. leucopus did not show such a clear response. P. leucopus densities were variable throughout the eight years of the study, but their density during the emergence (1987) was higher than in five of the other seven years when there was not an emergence of cicadas (Krohne et al. 1991). Furthermore, Peromyscus species have previously been shown to respond positively to the abundant food provided by an insect outbreak (Holling 1959). Periodical cicadas reach higher population densities at forest edges (Rodenhouse et al. 1997), which are more heavily vegetated than the forest interior (Burke and Nol 1998, Anderson et al. 2003). The higher densities at the edge may be because emergence times are dependent on soil temperatures with earlier emergence times in sunlit areas (i.e., edge habitats; Heath 1968, Forsythe 1977). Individuals that emerge later are attracted to the chorusing centers that form in sunny areas in the edge for courtship and mating (Williams and Smith 1991, Rodenhouse et al. 1997). Because females oviposit in sunlit trees near chorusing centers, the density of emerging cicadas may be greater in edge habitats (Lloyd and White 1976, Karban 1981, Rodenhouse et al. 1997). Similarly, P. leucopus have higher densities in the edge than in the interior of forest fragments (Yahner 1992, Nupp and Swihart 1996, Anderson et al. 2003, Wilder and Meikle in press a). Hence, periodical cicadas may provide a significant pulse of food for P. leucopus and have a substantial effect on their densities. In particular, densities may be greatly affected in small fragments due to their greater proportion of edge habitat (Bowers and Dooley 1993, Wolf and Batzli 2001). Thus far, there has not been any investigation of the effects of a cicada emergence on P. leucopus in relation to forest fragment size. The 2004 emergence of Brood X allowed me to test several predictions regarding the effect of a superabundant natural food supply on population

15 densities of P. leucopus in several small and large forest fragments. To test these predictions, I compared results from 2004 to a subset of data from a previous year (2002) without cicadas (Wilder and Meikle in press a, Wilder and Meikle in press b) during which they collected data using nearly identical methods in the same fragments. The goal of this study was to determine if the availability of periodical cicadas causes the density of P. leucopus to increase, and specifically, if the effect of cicadas on the relative population density of P. leucopus differs in relation to forest fragment size. I hypothesized that periodical cicadas would have a positive effect on the relative population density of P. leucopus because cicadas serve as a large source of food. I predicted that (1) population densities of P. leucopus in 2004 would be higher than in 2002 due to the cicada emergence; (2) population densities of P. leucopus in 2004 would be positively correlated with the number of cicada emergence holes; (3) there would be more cicadas in edge than in interior habitat and, therefore, more mice in the edge; (4) there would be more cicadas in small than in large forest fragments and, therefore, more mice in small fragments; and (5) size and habitat differences in P. leucopus densities would be significantly greater than the differences observed in 2002. Methods Study site I used six fragments of secondary-growth deciduous forest within 25 km of Oxford, OH (Butler and Preble Counties, OH and Franklin County, IN). Three of the fragments were 1-2 ha (small), and the other three were >100 ha (large). The surrounding matrix was primarily row crops (corn and soybeans), but some fragments were bordered by fields or pasture. Fragments were separated from the nearest forested area by at least 50 m. Population density In each forest fragment, I used 15 “edge” nest boxes (5 m from the field/forest transition) and 15 “interior” nest boxes (50 m from the field/forest transition) for a total of 180 nest boxes for the six fragments. The boxes were spaced 15-20 m apart and attached to a tree at a height of ~1.5 m. Nest boxes were censused six times between May and November 2004. During each census, all fragments were censused over several consecutive days. Small and large fragments were censused in a balanced design. Mice were caught individually in a plastic bag and scanned for the presence of a passive integrated transponder (PIT tag; AVID®). The PIT tag identification number, weight (to the nearest 0.5 g), length (tail and body), sex, and number and

16 collective weight of offspring (<9 g) were recorded for each individual with a PIT tag. At first capture, each mouse had the same measurements taken and, if ≥ 9 g, was lightly anesthetized with isoflurane and injected with a PIT tag subcutaneously in the interscapular area (see Anderson et al. 2003). I used the number of individual mice captured in each fragment over the course of the study as an estimate of the relative population density of P. leucopus (Slade and Blair 2000, Wolf and Batzli 2002, Anderson et al. 2003). Cicada density I counted cicada emergence holes in June 2004 in order to estimate the relative densities of cicadas. In each fragment, I systematically placed 20 1-m2 quadrats (ten in the edge and ten in the interior) approximately 15 m apart between adjacent nest boxes. Vegetation was carefully cleared from each quadrat, and I counted emergence holes for each quadrat and summed them for the entire forest fragment. Understory vegetation complexity In each fragment, I also established four transects, each with seven vegetation-sampling sites with 10 m spacing between sampling sites. The transects were parallel to the field/forest transition and were located at 0 and 10 m (edge habitat) and 30 and 40 m (interior habitat) from the edge of the fragment. I based my definition of edge habitat on evidence that microclimate (i.e. light penetration and soil moisture) and understory vegetation (i.e. shrub cover and vegetation complexity) are significantly greater within 15 m of the abrupt transition from field to forest than in more interior habitat (Ranney et al. 1981, Burke and Nol 1998, Gehlhausen et al. 2000, Anderson et al. 2003). In July 2004, I recorded the number of 0.5 m sections of a 2 m rod that were in contact with vegetation (0=no vegetation, 1=vegetation at one height, etc.) at each point of my grid (Anderson et al. 2003). Vegetation scores in each fragment were averaged for the entire forest fragment. Monthly rainfall Monthly rainfall was estimated for the months of May-November 2004 using precipitation data from the National Climatic Data Center (www.ncdc.noaa.gov/oa/ncdc.html). I used data from five weather stations: four surrounding the study site (approximately 15-20 km in each direction) and one located approximately in the middle of the study site (i.e. Miami University). Mean monthly rainfall for these five sites was averaged in order to obtain an estimate of the mean monthly rainfall for the entire study site.

17 Between-year comparisons In 2002, Wilder and Meikle (in press a, in press b) used a similar experimental design in three small and three large forest fragments. I used four of the six forest fragments (two small and two large) that Wilder and Meikle used in 2002. The number and placement of nest boxes was nearly identical in relation to edge and interior habitat. I used a subset of the population density and vegetation complexity data from 2002 to analyze data from an equal sampling effort in both 2002 and 2004 (Wilder and Meikle in press a, Wilder and Meikle in press b). Six of the ten nest box censuses for 2002 were selected to correspond as closely as possible to the dates of the six censuses in 2004. Similarly positioned (in relation to their distance from the forest edge) vegetation transects were selected for the two years, and mean vegetation scores were compared between years. Vegetation complexity, mean monthly rainfall, and diameter at breast height (DBH) of nest box trees in 2002 and 2004 were compared to determine if factors other than abundance of periodical cicadas were different between the two years. Statistical analysis Population densities of P. leucopus and densities of cicada emergence holes were analyzed with a repeated measures analysis of variance (ANOVA; Proc MIXED, SAS Institute). Factors in the model were fragment size, name of fragment, habitat, and month. Post hoc analyses of effects were done using LSMEANS and Bonferroni tests. A Pearson correlation was used to analyze the relationship between P. leucopus and cicadas. I estimated the rate of recruitment by regressing the cumulative number of individuals captured at each census against the census number (1-6). The slope of the resulting line was then regressed against the number of cicada emergence holes in each fragment. The number of litters in each fragment was also regressed against cicada emergence holes. Vegetation complexity and densities of P. leucopus were compared between years with a repeated measures ANOVA (Proc MIXED, SAS Institute). Mean rainfall and DBH of nest box trees were analyzed with a two-sample t-test between 2002 and 2004 (Sokal and Rohlf 1995). Only significant interactions were reported. Results As predicted, there was a significant positive relationship between cicada emergence holes and relative population densities of P. leucopus (r=0.76, p=0.0043, Figure 3).

There were more cicada emergence holes in edge than interior habitat (F (1, 9) =12.14, p=0.007),

although there was not a relationship between cicadas and fragment size (F (1, 9) =0.57, p > 0.15).

18 There was a significant year by size interaction (F (1,120) =11.35, p=0.001) with more mice in large fragments in 2004 than in 2002 (p=0.0002) and approximately the same number of mice in small fragments in both years (p=0.35, Figure 4). There were significantly more mice in 2004

(Table 2), when periodical cicadas emerged, than in 2002 (Table 3; F (1,120) =4.19, p=0.043).

Relative densities of mice were not related to fragment size in either year (F (1, 6) =0.01, p=0.91), although the absolute numbers of mice in 2002 were greater in small fragments (Wilder and Meikle in press a). For the two years combined, I also found a nonsignificant tendency towards higher relative densities of mice in edge than interior habitat (p=0.06) with the edge having significantly more mice in 2004 than 2002 (p=0.03) and more mice than the interior in both years (2002: p=0.006; 2004: p=0.04). Relative densities of P. leucopus were not related to understory vegetation complexity in

2002 or 2004 (2002: F (1, 5) =5.13, p=0.08; 2004: F (1, 5) =0.09, p=0.77, Figure 5). However, the slope of the regression for 2004 was in the direction opposite what was expected based on data from previous years. There was a tendency towards more understory vegetation in 2004 than

2002 (F (1, 10) =3.62, p=0.08), which may be due to greater vegetation in the interior in 2004. Although most habitat comparisons within and between years showed that there was more vegetation in edge than interior, complexity of understory vegetation in the edge in 2002 was not different from that for the interior in 2004 (p=0.09). This implies greater than usual understory vegetation complexity in forest interiors in 2004. An analysis of the rates of recruitment into the population for each forest fragment showed that the fragments with the highest number of cicada emergence holes also had the

fastest rate of recruitment (F(1,5)=11.15, p=0.028). Similarly, the same fragments tended to have more litters produced by female white-footed mice (F (1, 5) =6.73, p=0.06). The mean rainfall for May-November was not different between the two years (t=0.07, df=11, p=0.94). In fact, the total rainfall in 2002 was greater than that in 2004. Similarly, the mean DBH of trees with a nest box on them was not different between the two years (t=1.48, df=8, p=0.18). Discussion My results indicate that the relative abundance of cicadas had a positive influence on the relative abundance of P. leucopus. Not only was there a strong positive association between cicadas and abundance of mice, but for the first time at these study sites, I observed a positive

19 density-area relationship for P. leucopus (Anderson et al. 2003, Wilder and Meikle in press a). In fact, I captured 20% more mice with 6/10th of the trapping effort in 2004 than were caught in 2002 (Wilder and Meikle in press a). My results differ from those of Krohne et al. (1991), because the relative population density of P. leucopus in 2004 appeared to respond strongly to a periodical cicada emergence. The density of P. leucopus reported for the periodical cicada emergence year (1987) in Krohne et al.’s (1991) study was higher than in five of the seven other years. It is possible that other factors such as vegetation, competition, or precipitation masked the effect of cicadas on P. leucopus by elevating the population densities in some (non-emergence) years of Krohne et al.’s (1991) study or, alternatively, limiting the density of mice in 1987 (the previous Brood X emergence). For example, P. leucopus populations can be affected by factors such as mast that would not affect B. brevicauda. In addition, Krohne et al.’s (1991) study was focused on the forest interior (i.e. >15 m from the interface between the forest and the surrounding matrix; see Krohne and Baccus 1985, Gehlhausen 2000, Wolf and Batzli 2002). My study found significantly more mice and cicadas in edge habitat than in interior, indicating that some aspect of edge habitat (sunlight, understory vegetation, etc.) is important to both species. Hence, Krohne et al. (1991) may have been unable to observe population changes in other areas near the study site. The hypothesis that cicadas would have an impact on the population density of P. leucopus is based on a previous study that shows that P. leucopus will eat periodical cicadas. Hahus and Smith (1990) reported that during a periodical cicada emergence, P. leucopus greatly increased the proportion of arthropods in their diet with cicadas constituting 37% of arthropod volume and 14.4% of the overall diet. Likewise, I observed large numbers of cicada wings and body parts in nest boxes at my study site. Hahus and Smith (1990) reported a functional response (Holling 1959) for P. leucopus, since, as the density of periodical cicadas increased, mice consumed a larger number of them. I found evidence for a numerical response (Holling 1959) of P. leucopus to periodical cicadas. The fragments with the highest numbers of cicada emergence holes also had the fastest rates of recruitment and a tendency to have more litters. While these increases could have been due to increased immigration (and subsequent reproduction) or increased reproduction by residents, cicadas are widespread in the landscape (Rodenhouse et al. 1997), and it is unlikely that mice

20 would disperse from one fragment to another in search of them. Thus, it is likely that these increases in litter production and recruitment are due to increased reproduction by residents. Another factor that could have caused the higher relative density of P. leucopus in 2004 than in 2002 is the trend towards greater understory vegetation complexity in 2004. The increase in vegetation in 2004 was probably not due to rainfall differences, since the absolute amount of rainfall was greater in 2002. In fact, Yang (2004) found that cicadas are a significant source of nutrients vital to plant growth. He documented increases in foliar nitrogen content and soil nitrogen due to decomposition of cicadas. The soil nitrogen levels persisted after cicadas were gone from the environment and resulted in increased seed sizes in experimental plants relative to controls (Yang 2004). This could potentially explain the slightly greater vegetation complexity found in 2004 compared to 2002. The increased cover and food provided by the fertilized plants could also partly explain the continued increase in mouse densities after the cicadas were no longer present. However, the increase in complexity of vegetation occurred in the fragment interiors, not in the edges where the densities of mice were higher. In addition, the slope of the regression for mouse densities and understory vegetation complexity was opposite to the direction expected (Figure 5). This suggests that the presence of cicadas, not the complexity of the understory vegetation, was the driving force behind the higher densities of P. leucopus. Investigators who examine the effects of supplemental food on the population density of P. leucopus must overcome some potential difficulties. One of these involves the use of manufactured foods such as commercial rodent chow. While rodent chow is designed to provide essential nutrients and calories, it is unclear whether wild animals consume it as they would a natural food source. Another potential difficulty arises with the use of regularly spaced feeding stations. For supplemental feeding to be effective, food must be available to as many individuals as possible. In a territorial species such as P. leucopus, feeding stations may be defended by one or two individuals. This largely removes the benefit of supplemental food from the rest of the population. Broadcast dispersion of food or use of a woodlot undergoing a mast year can avoid one or both of these difficulties. However, Yunger (2002) attributed a population increase in a woodlot with a large mast (acorn) crop to immigration, presumably from areas without abundant food. Periodical cicadas generally are more uniformly distributed across the landscape (Rodenhouse et al. 1997) and can emerge at densities exceeding 2.5 x 106 individuals/ha (Dybas and Davis 1962,

21 Williams and Smith 1991). This indicates there is little reason for individual mice to leave one forest fragment for another in search of food. Yunger (2002) also documented a dramatic decline in the number of P. leucopus following the mast event. I saw no such decline after the cicada emergence, perhaps due to fertilization of vegetation by cicadas (Yang 2004) and/or the timing of the cicada emergence (spring) compared to a mast event (autumn). However, one drawback to studying an emergence of periodical cicadas as a supplemental food source is the lack of control plots caused by their widespread distribution. Taken together, my results show that an emergence of periodical cicadas has a strong positive effect on the relative population density of P. leucopus. The large input of food provided by periodical cicadas is enough to override the typical fragment size and habitat characteristics that determine population densities of mice at my study site (Anderson et al. 2003, Wilder and Meikle in press a, Wilder and Meikle in press b). For the first time in five years, the absolute number of P. leucopus was higher in large forest fragments than in small fragments. This suggests that availability of food may be one of the factors causing the negative density- area relationship usually shown by P. leucopus (Yahner 1992; Nupp and Swihart 1996, 1998; Krohne and Hoch 1999; Mossman and Waser 2001; Anderson et al. 2003). Further study in other areas experiencing a periodical cicada emergence may reveal other factors limiting population densities of P. leucopus, and perhaps help to explain the reasons for the negative density-area relationship more completely.

Table 2: Mean values (±SEM) for forest fragments outside Oxford, OH in 2004

Small fragments Large fragments Edge Interior Entire Edge Interior Entire habitat habitat fragment habitat habitat fragment Cicada emergence 352.3±84.7 201.7±39.8 554±123.6 472.7±74.2 178±39 650.7±92.1 holes Number of

mice 64±28.6 48.3±16.7 112.3±45.1 94.7±23.8 72±8.3 166.7±31.9 captured Understory vegetation 2.1±0.1 1.7±0.2 score DBH (cm) 32.9±1.8 29.9±1.4 Rainfall 3.6±0.6 3.6±0.6 (cm)

Table 3: Mean values (±SEM) for forest fragments outside Oxford, OH in 2002

Small fragments Large fragments Edge Interior Entire Edge Interior Entire habitat habitat fragment habitat habitat fragment Number of

mice 47±8.4 63.3±3.2 110.3±7.5 58±8.5 46.7±5.9 104.7±7.5 captured Understory vegetation 1.9±0.2 1.6±0.3 score DBH (cm) 35.7±4.3 34.2±1.2 Rainfall 3.7±0.8 3.7±0.8 (cm)

24 250 d e

r 200 u t

150 ce cap i m f 100 o r e b

m 50 u N 0 0 200 400 600 800 1000 Number of cicada emergence holes

Figure 3: Relationship between the mean number of white-footed mice and mean number of cicada emergence holes in forest fragments outside Oxford, OH

25 250 d e r

tu 200 cap ce

i 150 small m f o

large 100 er b m u 50 n ean

M 0 2002 2004 Year

Figure 4: Density-fragment area relationship for white-footed mice (mean+SEM) in forest fragments outside of Oxford, OH in 2002 and 2004. The year by size interaction is significant (F (1,120) =11.35, p=0.001).

250 d e

r 200 u t 2004 150

ce cap 2002 i

m 2004 f 100 o

r 2002 e b

m 50 u N 0 0.5 1.0 1.5 2.0 2.5 Vegetation complexity

Figure 5: Relationship between mean number of white-footed mice and complexity of understory vegetation in forest fragments outside of Oxford, OH in 2002 and 2004

27 Chapter 4 SUMMARY The purpose of this study was to examine some of the possible causes for the negative density-area relationship reported for the white-footed mouse, Peromyscus leucopus (Nupp and Swihart 1996, 1998, 2000; Anderson et al. 2003). In particular, I examined two of the possible causes: predation and food availability. Predation My observation that scent had no effect on giving up densities did not support the prediction that P. leucopus would alter its foraging behavior in the presence of a predator odor. However, my results and the results of others (Orrock et al. 2004, Powell and Banks 2004) indicate that rodents base their foraging behaviors on indirect rather than direct cues of predation risk. This is supported by the month-to-month differences in vegetation (pre- and post leaf fall) and the corresponding differences I found in GUDs. I also observed a tendency toward higher giving up densities in both habitats (edge and interior) in small fragments than in large fragments. This may be because small fragments generally have a greater complexity of understory vegetation than large fragments, due, in part, to their higher proportion of edge habitat. These higher GUDs in small fragments may represent more food or a higher perception of the risk of predation in small fragments (Brown 1988). While the results of the field component of my study support previous work (Orrock et al. 2004, Powell and Banks 2004), the laboratory portion suggests an interesting difference in the response of P. leucopus from forest fragments of different sizes to the odor of a predator. Further odor avoidance trials (i.e., different odor combinations) may reveal other differences. In addition, overnight observation in the odor avoidance trials would allow examination of potential changes in odor avoidance over time (i.e., habituation). Food availability My results indicate that the relative abundance of cicadas had a positive influence on the relative abundance of P. leucopus. Not only was there a strong positive association between numbers of cicadas and numbers of mice, but for the first time at my study sites, I observed a positive density-area relationship for P. leucopus (Anderson et al. 2003, Wilder and Meikle in press a).

28 The hypothesis that cicadas would have an impact on the population density of P. leucopus is based on a study that shows that P. leucopus eat periodical cicadas (Hahus and Smith 1990). Hahus and Smith (1990) reported a functional response (Holling 1959) for P. leucopus during the 1987 emergence of periodical cicadas. I found a numerical response (Holling 1959) of P. leucopus to periodical cicadas. Numbers of cicada emergence holes were related to rates of population growth and there was a tendency toward production of more litters. While these increases could have been due to either increased immigration or increased reproduction of residents, the ubiquity of periodical cicadas in forested areas in the landscape (Rodenhouse et al. 1997) makes it unlikely that mice would disperse from one fragment to another in search of them. Understory vegetation complexity also could have caused the higher relative density of P. leucopus in 2004 than in 2002. The increase in vegetation in 2004 was probably not due to rainfall differences, since the absolute amount of rainfall was greater in 2002. Cicadas have been reported to fertilize plants (by their death and decomposition) during an emergence year (Yang 2004). This could explain the slightly greater vegetation complexity found in 2004 compared to 2002. This seems to indicate that the presence of cicadas, not the complexity of the understory vegetation, was the driving force behind the higher densities of P. leucopus with both direct and indirect effects. My results indicate that an emergence of periodical cicadas has a strong positive effect on the relative population density of P. leucopus because they serve as a superabundant food source. For the first time in five years, P. leucopus existed at higher relative densities in large forest fragments than in small fragments. This suggests that availability of food may be one of the factors causing the negative density-area relationship usually shown by P. leucopus (Yahner 1992; Nupp and Swihart 1996, 1998; Krohne and Hoch 1999; Mossman and Waser 2001; Anderson et al. 2003). Further study in other areas experiencing a periodical cicada emergence may reveal other factors limiting population densities of P. leucopus. Conclusion I conclude that food may be a limiting factor for population growth of P. leucopus in large forest fragments, and that it may play a role in the negative density-area relationship of that species. However, predation cannot be ruled out as another factor in that density-area relationship. Further work is needed both in the field and in the laboratory to further define the

29 part played by predation. Likewise, analysis of the differences in food supply in forest fragments of different sizes and possible causes of those differences (i.e. vegetation complexity, matrix type, etc.) is needed to continue to study the effects of habitat fragmentation on Peromyscus leucopus.

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