ground squirrel research project

The Effect of Habitat on Aggression in the Thirteen-Lined Ground Squirrel (Spermophilus Tridecemlineatus)

Alexandra Klimovitz

The University of Michigan Biological Station EEB 453 July 2014

ABSTRACT

We tested the hypothesis that interspecific aggression of the thirteen-lined ground squirrel (S. tridecemlineatus) varies with habitat type (i.e. decreased woodland habitat). We defined aggression as an encounter in which an individual thirteen-lined ground squirrel acted to prevent an opponent of any species from accessing food resources. These encounters occurred with significantly greater frequency in the border habitat (43%; n=100; p<0.05) as opposed to the open (31%; n=116; p<0.05) or shrub habitats (26%; n=42; p<0.05). The thirteen-lined ground squirrel displaced opponents in 81% of encounters in the open (n=100), whereas only 61.9% in shrub habitat (n=42). While we did not observe more interspecific aggression among S. tridecemlineatus and other diurnal sciurids in open habitats, thirteen-lined ground squirrels did win a higher percentage of encounters in the open habitats. This supports the prediction that S. tridecemlineatus wins more aggressive encounters over resources than other sympatrically-occurring diurnal sciurids in deforested areas. We expect that the small mammal distribution in areas affected by deforestation will be altered by the high rates of aggression we observed by S. tridecemlineatus.

July 2014 OBSERVING AGGRESSION IN SPERMOPHILUS TRIDECEMLINEATUS 2

INTRODUCTION

Human interference is most often cited as having a negative impact on the ability of

an organism to survive and reproduce in a particular environment (Datta & Pal, 1993;

Anderson & Keith, 1980; Hartley & Hunter, 2008). However, there have been instances

reported in which man-made disturbances have positively impacted species reproductive

fitness (Bojsen & Barriga, 2002). With over 31% of forest cover in The United States lost

within the 21st century alone, it has become urgent to study the implications—both good and

bad—that disturbances such as deforestation have on the current fitness of native species.

(Hansen et al, 2013). This study aims to investigate why some North American grassland

species such as Spermophilus tridecemlineatus (thirteen-lined ground squirrel) have thrived

in these disturbed areas (Streubel & Fitzgerald, 1978).

Between 1900 and 1950 in Michigan the geographic distribution of S.

tridecemlineatus spread from the open grassland areas along the southwestern border to

include the mixed forest habitats of the northern lower peninsula (Streubel & Fitzgerald,

1978). Our study site, in which S. tridecemlineatus recently became common, is along the

shoreline of Douglas Lake at The University of Michigan Biological Station.

While generally S. tridecemlineatus is considered to be non-territorial, this species

often exhibits interspecific aggression and readily defends areas with high-quality food

resources (Streubel & Fitzgerald, 1978). The frequency and success of these aggressive

encounters typically increases as hibernation in early September approaches (Streubel &

Fitzgerald, 1978). Thirteen-lined ground squirrels exploit high levels of sex hormones in

order to build up large quantities of muscle (Boonstra et al, 2011). These hormones have

been shown to promote interspecific aggression by both sexes in areas with high competition


for limited resources (Lumia et al, 1994). We intended to learn more about how this

aggression and increased woodland destruction may contribute to their recent surge of

reproductive success.

In order to do this, we observed aggressive encounters in this species and studied how

different habitat types (open, border, and shrub) affect these behaviors. We hypothesized that

observations of feeding behavior in open areas, as opposed to shrubby or border areas, would

be characterized by more interspecific aggression in addition to higher success rates by S.

tridecemlineatus.

METHODS

Location

Our class of 15 undergraduate students conducted this study within residential areas

at The University of Michigan Biological Station (UMBS) along the shoreline of South

Fishtail Bay on Douglas Lake in Cheboygan Co., Michigan (45.559, -84.673)., from June

28th, 2014 to July 11th, 2014.

Study Site Description

We designated three zones approximately 230 square meters in size: Zone 1 (45.560,

-84.672), Zone 2 (45.560, -84.669), and Zone 3 (45.561, -84.668), (see Fig. 1). Zones had a

sandy soil composition with a variety of vegetation present. Each zone was broken down into

three habitat types: open, border, and shrub. Open habitats consisted of small leafy

vegetation with pine needle groundcover, shrub habitats consisted of small woody plants, and

border habitat was combination of the two (see Table 2 and Fig. 2 for species).


Trapping

We trapped S. tridecemlineatus from June 28th to July 7th, 2014 between 9am-4pm.

We used 54 (45cm x 12cm x 12cm) Havahart Small 2-Door Traps (Woodstream Corp.,

Lititz, PA), six (40cm x 12cm x 12cm) Original Series Tomahawk Live Traps (Tomahawk

Live Trap, Hazelhurst, WI), and sunflower seeds (1/2 cup) to bait each trap. Students

checked the traps hourly and brought all trapped individuals (including bycatch: Sciurus

carolinensis, Tamiasciurus hudsonicus, Tamias stiatus) to the classroom and held them

captive with food for no longer than six hours. We weighed, sexed, marked (using Nyanzol D

dye), and determined the lactating condition (e.g. “post lactating") of S. tridecemlineatus to

for identification during observation session and data analysis We prepared the Nyanzol D

fur dye using hydrogen peroxide and isopropyl alcohol as presented in the methods of

Melchior and Ewen (1965). We released S. tridecemlineatus and bycatch animal

simultaneously after 4pm in their respective zones.

Behavioral Experiment

We conducted behavioral observations of aggression from June 28th to July 12th, 2014

at least once per day for one hour throughout peak activity hours from 9am-4pm (Streubel,

1978). In order to study the variation in success and incidence of aggression based on habitat

type, we lured individuals to an observation station designated within one of three habitat

types in each zone—border, open, or shrub—using sunflower seeds (1 cup) placed upon

wooden trays (1’ by 1’).


We used encounter-induced aggressive behavior as a measurement of interspecific

aggression and encounter outcomes as a measurement of the ability of an animal to defend a

food territory. We defined aggressive behavior according to the behavioral ethogram we

developed from preliminary observations of the S. tridecemlineatus (see Table 1). We

recorded the following upon recognition of aggression (Table 1) at the feeding tray: time of

encounter, name of squirrel performing the behavior, species of incomer, behavior exhibited

by focal squirrel, behavior exhibited by incomer, win or loss for focal, win or loss for

incomer. We defined winning as when a mammal managed to gain access or maintain its

own access to a food source. We defined losing as when a mammal fled or otherwise lost

access to a food source.

Analysis of Data

We used a chi-square test for independence to analyze ratios of wins and losses

among different species and the three different habitats. We considered values at the 0.05

alpha level to be statistically significant. An analysis of proportion of encounters won

allowed us to affirm trends inferred through the chi-square statistical analysis. Scatter plots

equipped with lines of best fit were used to analyze correlations between weight and both the

total number of aggressive encounters and the ratio of wins to losses observed

RESULTS

Eight S. tridecemlineatus were captured and uniquely marked, with weights ranging

from 45g - 165g (Table 3). Unmarked thirteen-lined ground squirrels were not recorded as


focal species, however they were recorded as opponents against a marked thirteen-lined

ground squirrel if this behavior was observed.

The proportion of encounters won by thirteen-lined ground squirrels differed

significantly depending on whether the encounters took place in open, border, or shrub

habitats ( χ² = 6.39, df = 2, p<0.05; Table 3). Aggressive behavior by S. tridecemlineatus that

resulted in a win against any intruder was observed 20% more when the encounter took

place in open habitat than when the encounter took place in a shrub habitat (thirteen-lined

ground squirrels won 81 of 100 encounters in the open, and only 26 of 42 encounters in the

shrub, p<0.05; Fig. 2).

We found that the total number of aggressive encounters observed in each habitat was

significantly different (χ2 = 14.97, df = 2, p<0.05; Table 5), with the highest proportion of

encounters taking place in border habitats (45%, n = 116, p<0.05; Fig. 3).

Thirteen-lined ground squirrels won significantly more of encounters against eastern

chipmunks (n = 140 wins against chipmunks) than encounters against red squirrels (n = 20

wins against red squirrels; χ2= 20.00, df = 1, p<0.05; Table 5). While not statistically

significant due to a small sample size, we observed that thirteen-lined ground squirrels won

87.5% of encounters against red squirrels (n = 22) in open habitat , but lost 100% of

encounters in shrub habitat (n=140, p>0.05; Table 7, Fig. 4). The same trend was true of the

thirteen-lined ground squirrel in encounters with the eastern chipmunk, a win by a thirteen-

lined ground squirrel was observed 30% more of the time when the encounter took place in

open habitat than when the encounter took place in a shrub habitat (thirteen-lined ground

squirrels won 140 of 160 encounters against chipmunks, and only 20 of 36 encounters

against red squirrels, p>0.05; Fig. 6).


A scatter plot equipped with a line of best fit shows a positive correlation between the

weight of a thirteen-lined ground squirrel and total number of aggressive encounters by that

individual observed in all habitat types with all species of opponent (R2=0.40) (Fig. 7).

Additionally, through an additional scatter plot with a line of best fit we see that weight of

individuals has a slightly negative correlation to the ratio of wins to losses observed in all

habitat types with all species of opponent (R2=0.53), (Fig. 8).

A stacked line graph displaying of the proportion of total wins per hour versus time of

day shows that S. tridecemlineatus was most successful in open habitat between the hours of

9am-10am with a steady decrease in the frequency of aggressive activity as the day

progressed (Fig. 9). The observed trends of border and shrub habitats were much more

variable, however both plots display an increase in the proportion of total wins from 10am -

12 noon (Fig. 9).

DISCUSSION

We observed significant differences in the frequency of encounters observed in each

habitat type, however this data was not consistent with our hypothesis that open habitats

would be characterized by a greater number of aggressive encounters. Additionally, we

observed significant differences in the proportion of wins that took place in each habitat type,

and this data was consistent with our hypothesis that thirteen-lined ground squirrels would

have more success in open habitats.

The higher success rates for S. tridecemlineatus in aggressive encounters in open

areas further suggest that this species is able to thrive in the increasing number of open

grassy habitats due to human disturbance. Areas that have been cleared of woody plants and


shrubs enable S. tridecemlineatus to see and defend themselves more efficiently against

predators and competition (Arenz & Leger, 2000). The higher frequency of observed

encounters—but lower success rate—in border habitats may correspond to higher rates of

aggression and foraging behavior of T. hudsonicus in areas of more dense vegetation (Steele,

1998).

This observation is consistent with the lower success rate we observed between the

thirteen-lined ground squirrel and the red squirrel when compared to encounters with the

chipmunk. For encounters with both red squirrels and chipmunks we observed the trend that

open habitats led to higher success rates, which is consistent with our data thus far. We

predict that the thirteen-lined ground squirrels initiated these encounters where they

encountered T. hudsonicus with high frequency in border areas, however were unable to

adequately defend the food territory due to decreased vision (Steele, 1998).

The correlations between weight, number of encounters, and proportion of

wins/losses displays the trend that larger squirrels initiated more aggressive encounters,

despite the smaller squirrels winning a larger proportion of encounters. One possible

explanation for this observation is the increased nutritional need of smaller squirrels,

predicting that these individuals would have higher levels of aggression-inducing sex

hormones being utilized prior to hibernation (Boonstra et al, 2011). These juvenile thirteen-

lined ground squirrels are known to spend less time visually scanning the environment for

competitors due to this increased nutritional need, explaining the reason fewer encounters

were initiated (Arenz & Leger, 2000).

The peak in aggression in thirteen-lined ground squirrels we observe in open habitats

at 9am overlaps with the peak activity of male T. striatus in the morning during mating


season—which runs from late June to early July (Snyder, 1982). Peaks in aggression in

border and shrub habitats between 10am and 12 noon in addition to a corresponding decrease

in aggression in open habitats may correspond to peak activity of T. hudsonicus, which

forages in the late morning and early afternoon in areas of high density vegetation (Steele,

1998).

We suggest that the increasing rates of deforestation will lead to increased

reproductive fitness of S. tridecemlineatus as more open habitat becomes available for use by

the species (Streubel & Fitzgerald, 1978). Consequently, we may see an increased incidence

of aggression toward species like T. stiatus and T. hudsonicus as the populations compete for

limited resources.

We did experience a few limitations that may have affected our data, including an

unequal number of hours spent observing each habitat type, and the possible bias of data

toward a few squirrels that were seen most often—which may have been influenced by

distance of the feed tray to the individual's burrow. Nonetheless, this study is relevant to

research on how human disturbance affects species distribution. The interactions of these

species play a vital role in the balance of this forest ecosystem as sciurids play an essential

role seed distribution, and are important prey to a variety of predators including snakes,

foxes, birds of prey, and coyotes. This increase in aggression has the potential to impact the

distribution of all three species in the near future. We suggest that a more long term study be

performed that also examines the reproductive fitness impact this aggression has on T. stiatus

and T. hudsonicus in order to fully grasp the implications of this changing ecosystem.


FIGURES

Type of

Behavior Behavior Code Description

Aggression Biting B Animal's teeth contact another animals body while engaging with it

Chasing C Animal approaches and pursues another animal

Pushing P Animal exerts force with extremities or body on another

Vocalization V Animal uses verbal communication such as growling /chattering/chirping/alarm calling

Fleeing F Animal runs away from an aggressive encounter with another animal

Table 1. Behavioral Ethogram of aggression observed in S. tridecemlineatus


Table 3. Sex and weight of all S. tridecemlineatus trapped, marked, and released whose behaviors were observed and recorded throughout the study.

Squirrels Sex Weight

(g)

1 female 165 2 female 148

3 female 185

4 male 115

5 male 105 6 male 40

7 male 45

8 female 45

Figure 2. Proportion of wins/losses by S. tridecemlineatus based on each individual habitat type. Figure shows a significant difference between total number of wins/losses observed in open, border, and shrub habitats.

Table 4. χ-square test for independence for total number of wins/losses of S. tridecemlineatus in each individual type of habitat. Figure shows a significant difference between total number wins/losses observed in open, border, and shrub habitats.

Open Border Shrub DF P Observed Expected Observed Expected Observed Expected 2.00 <0.05

Wins 81.00 76.74 91.00 89.02 26.00 32.23 Crit

Value χ2

Value Losses 19.00 23.26 25.00 26.98 16.00 9.77 5.99 6.39


Figure 3. Proportion of aggressive encounters by S. tridecemlineatus based on habitat type, corrected for the proportion of total hours spent observing each habitat. Figure shows a significant difference between total number of aggressive encounters observed in open, border, and shrub habitats.

Table 5. χ-square test for independence for total number of aggressive encounters observed by S. tridecemlineatus in each individual type of habitat, corrected for the proportion of total hours spent observing each habitat. Figure shows a significant difference between total number of aggressive encounters observed in open, border, and shrub habitats.

Open Border Shrub DF = 2 P<0.05

Observed Expected Observed Expected Observed Expected Crit

Value χ2 Value Total # of

Aggressive Encounters 100.00 107.73 139.20 107.73 84.00 107.73 5.99 14.97

Table 6. χ-square test for independence for total number of wins/losses by S. tridecemlineatus observed against T. hudsonicus/T. stiatus in all habitat types combined. Figure shows a significant difference between total number of wins/losses by S. tridecemlineatus against T. hudsonicus/T. stiatus

T. hudsonicus T. stiatus DF P Observed Expected Observed Expected 1.00 <0.05

Wins 20.00 29.39 140.00 130.61 Crit Value χ2 Value Losses 16.00 6.61 20.00 29.39 3.84 20.00


Figure 4. Proportion of wins/losses by S. tridecemlineatus observed against both T. hudsonicus/T. stiatus in all habitat types combined. Figure shows a significant difference between total number of wins/losses by S. tridecemlineatus against T. hudsonicus/T. stiatus.

Figure 5. Proportion of wins/losses by S. tridecemlineatus observed against only T. hudsonicus in each individual habitat type. Figure does not show a significant difference between total number of wins/losses by S. tridecemlineatus against T. hudsonicus because n<8.

Figure 6. Proportion of wins/losses by S. tridecemlineatus observed against only T. stiatus in each individual habitat type. Figure does not show a significant difference between total number of wins/losses by S. tridecemlineatus against T. stiatus because n<8.


Figure 7. Scatter plot equipped with a line of best fit comparing the total number of aggressive encounters we observed in all habitat types as a function of thirteen-lined ground squirrel weight.

Figure 8. Scatter plot equipped with a line of best fit comparing the ratio of wins/losses observed in all habitat types as a function of thirteen-lined ground squirrel weight.


Figure 9. Graph of the proportion of total wins recorded throughout the duration of the experiment in each habitat during hours of observation (9am-4pm).


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ground squirrel research project

Documents

habitat type

border habitat

woodland habitat

effect of habitat

interspecific aggression

greater frequency

food resources