Possible Relationship Between Vocal Communication System and Fat Reserve in Wintering Birds: a Test of the Optimal Body Mass Theory

POSSIBLE RELATIONSHIP BETWEEN VOCAL COMMUNICATION SYSTEM AND FAT RESERVE IN WINTERING BIRDS: A TEST OF THE OPTIMAL BODY MASS THEORY

A Thesis by

Gamage Dilini Nuwanthika Perera

Bachelor of Science, University of Peradeniya, 2014

Submitted to the Department of Biological Sciences and the faculty of the Graduate School of Wichita State University in partial fulfillment of the requirements for the degree of Master of Science

December 2017

The following faculty members have examined the final copy of this thesis for form and content, and recommend that it be accepted in partial fulfillment of the requirement for the degree of Master of Science with a major in Biological Sciences.

F. Leland Russell, Committee Chair

Mark A. Schneegurt, Committee Member

Kandatege Wimalasena, Committee Member

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DEDICATION

To my parents, family and friends who always encouraged and supported me, and made me the person I am today.

ACKNOWLEDGEMENTS

I would like to thank my advisers, Christopher M. Rogers and F. Leland Russell for their many months of thoughtful, patient guidance and support along the journey of my graduate career. I would also like to thank Wichita State University, for the use of their facilities and resources. WSU has provided a great opportunity for me to proceed along the journey that is graduate school. I thank especially F. Leland Russell for taking responsibility for me after Christopher Rogers was on medical leave. Finally thanks to my family, friends and colleagues for their support and encouragement throughout my career.

ABSTRACT

Fat reserve is a key adaptation in wintering small birds for maximizing individual fitness in a variable environment. Optimal body mass models suggest that winter fat reserve maximizes winter survival by balancing costs, such as greater predation risk, and benefits, such as ability to withstand food scarcity, of fat deposition. Flocking integration may be important in determining the fat reserve of birds. I am testing the hypothesis that if bird species have a complex vocal repertoire, then they will have high communication efficiency (which reduces predation risk) and this allows a high fat reserve. I tested this hypothesis by recording vocalizations of the Dark-eyed Junco (DEJU) and American Tree

Sparrow (ATSP) in Kansas. The junco is fatter in winter than the tree sparrow and is predicted to have a larger vocal repertoire within its winter flocks. A Marantz digital recorder with a Sennheiser directional microphone was used to record vocalizations at winter feeding stations. Raven software was used to describe vocalizations within each species. Consistent with the hypothesis, DEJU produced more than one call type in every observation period, while ATSP produced only one call type throughout the observations.

Even though ATSP had a mean call rate of 1.62 calls / bird / minute whereas DEJU had a mean call rate of 0.12 calls / bird / minute a significant difference was not detected. ATSP frequently gave false alarm calls (alarm calls with no predators in the vicinity) at the winter feeding station providing deceptive information to flock mates and potentially impeding flock integration. These results support the hypothesis that communication ability plays a significant role in determining interspecific variation in fat levels of small wintering birds.

TABLE OF CONTENTS

Chapter Page

1. INTRODUCTION ...... 1

2. METHODS ...... 7

2.1: Study Species ...... 7 2.2: Study site...... 11 2.3: Data Collection ...... 13 2.4: Statistical Analyses...... 16

3. RESULTS ...... 17

4. DISCUSSION ...... 26

4.1: High vocal complexity coincides with high fat storage ...... 26 4.2: Patterns in vocalizations by the American Tree Sparrows and Dark-eyed Juncos ...... 29 4.3 Conclusion ...... 32

5. REFERENCES ...... 3

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LIST OF FIGURES

Figure Page

1: Sonograms of Dark-eyed Junco calls; A: Seep, B: Twitter, C: Twit, D: Chack, E: Kew ...... 8

2: Wichita State University, Biological Field Station, Ninnescah Reserve. Locations of the feeding stations are indicated by stars...... 12

3: Marantz PMD 661 recorder with Sennheiser ME67 directional microphone...... 14

4: Feeding station for Dark-eyed Juncos with scattered bird seed...... 14

5: Frequency distribution of call types of Dark-eyed Juncos at winter feeding stations and along transects...... 18

6: Call rates of American Tree Sparrows (ATSP) and Dark-eyed Juncos (DEJU) at winter feeding stations. Values are mean + SE...... 19

7: Average flock size of American Tree Sparrows (ATSP) and Dark-eyed Juncos (DEJU). Values are mean + SE...... 21

8: Relationship between flock size and call rate of Dark-eyed Juncos (DEJU): with a potential outlier. Each dot represents a 30 minute observation period. The regression equation is y=0.6822-0.1189x+0.0055x2...... 22

9: Relationship between flock size and call rate of Dark-eyed Juncos (DEJU): without the potential outlier. Each dot represents a 30 minute observation period. The regression equation is y= 0.1741-0.0084x...... 23

10: Relationship between flock size and call rate of American Tree Sparrows (ATSP): with potential outliers. Values are mean + SE. No regression equation is provided because the relationship is not statistically significant...... 24

11: Relationship between flock size and call rate of American Tree Sparrows (ATSP): without potential outliers. Values are mean + SE. The regression equation for the marginally significant relationship is y=0.5135-0.0893x...... 25

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LIST OF TABLES

Table Page

1: Number of call types produced by Dark-eyed Juncos (DEJU) and American Tree Sparrows (ATSP) during 30 minute observation intervals at winter feeding stations...... 20

CHAPTER 1

INTRODUCTION

Trade-offs are an essential component in understanding the evolutionary ecology of life history strategies (Gadgil and Bossert 1970, Stearns 1989). One of the most widely studied trade-offs involves the cost of reproduction. Cost of reproduction involves two major components: 1. Cost paid in survival and 2. Cost paid in future reproduction (Obeso

2002). Trade-offs between reproductive effort and adult survival or adult growth have been recorded in a wide range of field studies and manipulation experiments for both plants and animals. The trade-off between reproductive effort and adult survival has been studied in oviparous and viviparous fish species (Gunderson 1997). Reproductive effort has been measured as the gonadosomatic index which is the calculation of gonad mass as a proportion of the total body mass. Gunderson (1997) recorded a significant positive correlation between gonadosomatic index and adult mortality. He also studied the allometric scaling for mortality, gonadosomatic index and age at maturity with body size of fish. As a summary of this study, body size played a significant role in the trade-off between reproductive effort and adult survival.

Understanding selection pressures that influence the evolution of optimal morphological, physiological and behavioral traits is a major concentration of animal studies (Alexander 1996). Animals living in unpredictable environments need to make appropriate resource and time allocation choices because those choices can directly affect their survival and reproduction. Resource and time allocation strategies associated with foraging for food can strongly affect an animal’s fitness (Stephens and Krebs 1986). An

animal’s foraging strategy is the product of the individual’s energy requirements and the nature of the environment which they inhabit (McNamara and Houston 1986). Foraging strategies can be either short term strategies (e.g. seasonal) or long term strategies (e.g. annual or across a lifetime) (McNamara and Houston 2008, Arthur, Hindell et al. 2016).

Birds are a unique case among terrestrial animals when examining foraging decisions because they forage in a three-dimensional environment, moving both vertically and horizontally in search of food (Kooyman 2012). Fat storage in small-bodied wintering birds is an example of a seasonal foraging strategy used to overcome unpredictable environments (Rogers 2015).

Observed winter fat level of birds reflects an adaptive trade-off between costs and benefits of fattening (McNamara and Houston 1990, Houston and McNamara 1993,

Bednekoff and Houston 1994, Rogers 2015). The ability to fast through unexpected resource shortage, such as snowfall, is a benefit of fattening for small wintering birds. Costs of fattening include increased predation risk, which results from increased exposure to predators while feeding to fatten (Ekman 1986, Witter and Cuthill 1993, van der Veen and

Lindström 2000, Rogers 2015) and decreased maneuverability under predator attack

(Witter, Cuthill et al. 1994, Metcalfe and Ure 1995, Kullberg, Fransson et al. 1996, Kullberg,

Jakobsson et al. 2000). In addition, greater fat storage can increase the energetic cost of flight. Winter fat reserve of birds maximizes winter survival by balancing costs and benefits of fattening.

Small wintering birds experience higher energetic demands due to cold weather with long nights of starvation and high wind exposure with lack of foliage (Lima 1986,

McNamara and Houston 1990, Houston and McNamara 1993, Houston, McNamara et al.

1993, Bednekoff and Houston 1994, McNamara, Houston et al. 1994, Cuthill, Maddocks et al. 2000). Models have predicted that fat will increase when starvation risk increases under worse feeding conditions, involving a number of environmental factors acting individually (Blem 1990, Ekman and Hake 1990, Rogers and Smith 1993, Bednekoff and

Krebs 1995, Witter, Swaddle et al. 1995, Cuthill and Houston 1997, Smith and Metcalfe

1997, Witter and Swaddle 1997, Cuthill, Maddocks et al. 2000) as well as together

(McNamara and Houston 1990, Rogers and Reed 2003). Models of adaptive avian fat storage depict that fat store increases when resources become unpredictable, therefore fat reserves are beneficial.

Related North American field studies that focused on the relationship between fat reserves and the vertical gradient of resource predictability (Rogers 1987, Rogers and

Smith 1993, Rogers 2015), support the predicted pattern of greater fat storage in less predictable environments. Three foraging guilds that differ in the predictability of food availability can be identified, i.e.: (1) Ground foraging guild, (2) Tree foraging guild and (3)

Ground-tree foraging guild. The ground foraging guild consists of those species that feed exclusively on the ground. It experiences the most unreliable food resources. For example, snow can unpredictably cover the ground. The tree foraging guild, which consists of those species that feed exclusively on hibernating arthropods, fruits and seeds found on trunks, branches or leaves, experiences the most reliable food supply. Throughout much of North

America, tree-borne food is not likely to be covered by snow. The ground-tree foraging

guild consists of those species that exploit both resource bases by foraging both on the ground and in trees. They have a partial energetic dependence on each resource base.

Therefore, this guild experiences intermediate resource predictability. Consistent with expectations based upon the predictability of resource availability, studies show that the tree foraging guild maintains lower fat reserves than the ground-tree and ground foraging guilds (Rogers 1987, Rogers and Smith 1993, Rogers 2015).

Within different vertical feeding guilds, more subtle differences in spatial patterns of resource utilization among species can influence the predation risk that the species experience. Within the ground-feeding guild two winter habitats can be identified, i.e.: open winter habitat and closed winter habitat. A closed winter habitat is defined as a habitat with dense vegetation where aerial predation is lowered. By contrast, an open habitat is a habitat with less vegetation and more predation pressure from aerial predators such as hawks (Rogers 2015). Since predation risk is a cost of fattening, birds occupying open winter habitats have a lower fat reserve than the birds occupying closed winter habitats because birds in closed habitats are less exposed to predators (Rogers 2015). However, there is still considerable unexplained variation in the amount of fat stored among bird species within vertical feeding guilds and similar cover habitats.

Fat storage by birds can be measured or estimated using several methods. Total fat of birds is used to measure the total fat deposition. Magnetic resonance imaging (MRI) was developed to visualize the internal organs of birds and seasonal body composition in large bodied birds and small birds (Piersma and Klaassen 1999, Berthold, Elverfeldt et al. 2001,

Rogers 2003). MRI clearly reveals bulk tissues including fat, bone, muscle and tendon

(Rogers 2003). Total electrical body conductivity (TOBEC) is another method that is used

to estimate lean mass of a bird (Walsberg 1988, Rogers 2003). Lean body mass refers to the weight of the body that is not fat. This method becomes inaccurate as the body size decreases (Walsberg 1988). Estimating visible subcutaneous fat level is an alternate, non- invasive method of measuring fat of birds. It is especially effective for measurements of small bodied birds in the field.

According to Rogers (2015), Dark-eyed Juncos and American Tree Sparrows are two bird species that occupy open winter habitats in south-central Kansas and differ in visible subcutaneous fat level. From the previous available data, it is evident that Dark-eyed Juncos are fatter than American Tree Sparrows (Rogers 1987). This difference in fat storage between Dark-eyed Juncos and American Tree Sparrows has been corroborated by studies elsewhere in their ranges. For example, the fat level in Dark-eyed Juncos and American

Tree Sparrows was measured during the winters of 1962-1963 near Lewisburg,

Pennsylvania (Helms, Aussiker et al. 1967, Helms and Robert 1969). These studies also found the fat level of the body to be greater in Dark-eyed Juncos than in American Tree

Sparrows (Helms, Aussiker et al. 1967, Helms and Robert 1969). If both species occupy the same habitat and are exposed to similar predation pressure then the difference in the body fat level must be occurring due to some other factor.

Predation is one of the most important selection pressures acting on phenotypic traits of animals (Abbey-Lee, Kaiser et al. 2016). In birds, communication is an important behavioral adaptation that may enhance escape from predators by allowing alarms in the presence of a predator to be spread through a flock. Communication involves a variety of intraspecific and interspecific contexts with both benefits and energetic costs

(Stoddard and Salazar 2011). Vocal communication includes songs and calls. Singing is used to advertise quality of the male, discourage other males and attract females whereas calls are used to share information between neighbors in the flock (Abbey-Lee, Kaiser et al.

2016). Different calls aid in different information-sharing functions, including maintaining social organization, signaling the presence of food, synchronizing and coordinating flight, degree of aggressive and sexual conflict and alarming about predators (Marler 2004). It is possible that bird species with more complex vocal repertoires of calls can communicate within the flock and alarm the flocking mates about predators more efficiently than birds with less complex vocal repertoires. If predation risk is a cost of fattening, bird species with complex vocal repertoires may be able to support higher fat levels than birds with less complex vocal repertoires because they will have a high flocking integration with better ability to detect predators.

In this research, I am testing the prediction that a greater vocal repertoire allows greater fat storage using Dark-eyed Juncos (abbreviated DEJU) and American Tree

Sparrows (abbreviated ATSP). Specifically, I am asking whether the species with greater fat storage 1) communicates using a greater number of different call types and 2) gives calls at a greater frequency than the species with less fat storage. I address these questions by collecting data on these species’ vocalizations during two winter periods at Wichita State

University’s Biological Field Station in south-central Kansas.

CHAPTER 2

METHODS

2.1: Study Species

Study species 1: - The Dark-eyed Junco, one of the most common North American passerines, is distributed across the continent from northern Alaska south to northern

Mexico (Nolan, Ketterson et al. 2002). Juncos join ground-feeding winter flocks that often can be found in suburbs, in open woodlands, fields, parks, roadsides and backyards. They hop around the bases of trees and shrubs in forests or venture onto lawns looking for fallen seeds. The Junco plumage is unique with the white outer tail-feathers that flash when the bird takes flight. The Junco is characterized by a gray or blackish head, nape and throat and dark back that contrast with its whitish breast and belly and a pink bill. It is a medium- sized sparrow 14.5-16.5 cm in length and averaging 18-22 g in weight.

Winter migrant Dark-eyed Juncos arrive at their wintering habitats over a period of several weeks, but they form distinct foraging groups (Sabine 1949, Sabine 1956). Flocking

Dark-eyed Juncos exhibit a fairly rich repertoire of vocal signals, and communicate almost constantly with each other (Balph 1977). Most frequent Junco calls are (using terms from

(Balph 1977, Nolan, Ketterson et al. 2002) the seep, kew, twitter, twit and chack. Seep is a single-syllabled buzzing sound that has a constant mean center frequency from beginning to the end (Fig. 1)(Balph 1977). Kew is a sharp but musical syllable, usually repeated several times. It is given year-round but during the winter it is given more often by the winner of dominance interactions, causing the other individuals to move away (Nolan,

Ketterson et al. 2002). Twitter is a repeated series of high-frequency syllables

(Balph 1977). It is produced by females during a precopulatory display and by both sexes

during agonistic behavior (Nolan, Ketterson et al. 2002). Twit is a thin, high-frequency

syllable given in flight in all seasons (Balph 1977). Chack is a wide-frequency, short-

duration single syllable generally used as an alarm call in winter (Nolan, Ketterson et al.

2002).

Figure 1: Sonograms of Dark-eyed Junco calls; A: Seep, B: Twitter, C: Twit, D: Chack, E: Kew

Figure 1: (continued)

Male Juncos are highly territorial in the breeding season (Nolan, Ketterson et al.

2002). During winter, flocks do not defend territories and the occupants in a large area can change often (Nolan and Ketterson 1990). But, individuals rarely change their flock (Sabine

1955).

Study species 2: - The American Tree Sparrow is a familiar migrant and winter visitor in many areas of North America (Naugler 1993). They can be found in small flocks hopping about on the ground, scrabbling for grass and weed seeds. In winter, birds foraging in flocks keep a spacing of 15 cm from each other, although communal roosting is recorded in snowfall (Naugler 1993). American Tree Sparrows breed in the far north and are rarely seen south of northern Canada in summer (Naugler 1993). The American Tree

Sparrow is a small bird with a length of 14 cm and weight of 18 g. American Tree Sparrow adults differ from the other sparrows by a rusty cap, yellow mandible and grayish-white underparts with a dusky central breast-spot (Naugler 1993).

Male American Tree Sparrows sing only a single song type, which is a relatively long, melodious series of notes, usually associated with some aspect of courtship (Naugler

1993). It has a function of defending territory. But both sexes possess a number of calls.

Commonly heard calls include a two-note feeding call teel-wit and a hard tseet. The teel-wit call is a flock note given on migration and in winter, whereas the tseet is an alarm call given year round (Naugler 1993). The flock note given by various flock members may serve flock integration, while the alarm call serves to indicate the presence of a predator, especially near the nests (Naugler 1993).

2.2: Study site

Data were collected during two winter periods in 2015-2016 and 2016-2017 (1st

December to 1st March) at the Wichita State University Biological Field Station, Ninnescah

Reserve in southwestern Sedgewick County, Kansas (37° 32 ’N 97°41’ W) (Fig. 2). This study site contains a landscape habitat mosaic consisting of dense riparian woodland, shrublands and old fields within a largely agricultural landscape. Woody vegetation occurs as trees and shrubs and is mostly Osage orange (Maclura pomifera), red cedar (Juniperus virginiana), Siberian elm (Ulmus pumila), and box elder (Acer negundo). Winter avian predators who are likely to take small birds include the Cooper’s (Accipiter cooperi) and

Sharp-shinned (A. striatus) Hawks. Also present each winter are the Northern Harrier

(Circus cyaneus) and Red-tailed Hawk (Buteo jamaicensis), both of which may prey on small birds but focus largely on mammalian prey.

Figure 2: Wichita State University, Biological Field Station, Ninnescah Reserve. Locations of the feeding stations are indicated by stars.

Climate data was collected from the Conway Springs weather station that is 37km north of the field station. Average monthly temperatures during December – March are

1.75 to 7.5oC with minimum temperatures -5.4 to 0.9oC (High Plains Climate Research

Center, 2017). Especially in midwinter, extensive periods of below-freezing temperatures occur. Winter months may include light to heavy snow cover. Monthly mean snowfall for

December, January, February and March is 4.8, 5.3, 5.8, 2.4 cm, respectively, based on the period from 1944-2017 (High Plains Climate Research Center, 2017). However, snowfall

during my two winters of data collection was exceptionally light. In 2015-2016, there was less than 0.03 cm in December, zero snowfall in January and February and 7.62 cm in

March. During my 2016-2017 data collection period, snowfall was 3.6 cm in December and zero snowfall in January, February and March respectively (High Plains Climate Research

Center, 2017, https://hprcc.unl.edu).

2.3: Data Collection

Wintering bird calls were recorded using a Marantz PMD 661 digital recorder with a

Sennheiser ME67 directional microphone with a windscreen (Fig. 3). Bird calls were recorded at two winter feeding stations for Dark-eyed Juncos (37° 32’ N 97°40’ W and 37°

32’ N 97°40’ W) and one winter feeding station for American Tree Sparrows (37° 31’ N 97°

40’ W) (Fig. 2). Feeding stations that were used by Rogers in 2015 in prior studies were re- used as the Dark-eyed Junco feeding stations (Fig. 4). The American Tree Sparrow feeding station was located according to observations of where tree sparrows flock usually. Wild bird seed, which included sunflower seeds and cracked corn, was scattered at the feeding stations weekly.

Figure 3: Marantz PMD 661 recorder with Sennheiser ME67 directional microphone.

Figure 4: Feeding station for Dark-eyed Juncos with scattered bird seed.

Calls were recorded in three-minute segments up to a total of 30 minutes per day.

Using three-minute segments reflected behavioral considerations, such as the expected duration of birds’ visits to the feeding station, and file size limitations of the software. A three-minute recording segment was terminated when the birds left the feeding station or upon reaching three-minutes. As a result of early departures by the birds being recorded during some recording segments, total time recorded per day was not always a multiple of three. Number of individuals in the flock was counted to determine the flock size. The maximum number of individuals seen during the recording time was used as the quantification of flock size. Data for Dark-eyed Juncos were collected in winter 2015 and data for American Tree Sparrows were collected in winter 2016 following the same procedure. Recordings for American Tree Sparrows were done in winter 2016 due to absence of American Tree Sparrows in winter 2015.

Raven software (Cornell Lab of Ornithology, Bioacoustics research program) was used to describe and quantify different vocalizations within species. Audio files from

Macaulay Library at Cornell lab of Ornithology were used as a guide in identification of the different call types of both study species.

To confirm that call types produced by flocks at the feeding stations were representative of call types produced by natural flocks for both study species, Dark-eyed

Junco and American Tree Sparrow, 11 winter transects were surveyed in February 2016 at the WSU Biological Field Station, Ninnescah Reserve. These transects were located in a variety of habitats (field, shrub and trees). For 40 minutes, CM Rogers and I walked along each transect and recorded all call types heard for the two study species.

2.4: Statistical Analyses

All statistical analyses were conducted using RStudio version 3.3.2. To determine whether data from the two Dark-eyed Junco feeding stations could be pooled for further analysis, call rate was compared between the feeding stations using a Wilcoxon signed rank test. I calculated “call rate” as the number of calls per bird per minute. Call types per bird per minute was also compared between the feeding stations using Wilcoxon signed rank test. Frequency distributions of call types of Dark-eyed Juncos given at each feeding station were compared with the call types given along the walking transects using Pearson’s Chi- squared test.

I compared call rate between Dark-eyed Juncos and American Tree Sparrows using

Welch’s t test. Number of call types produced by Dark-eyed Juncos and American Tree

Sparrows during each observation period was compared using Fisher’s exact test. Mean flock size of Dark-eyed Juncos and American Tree Sparrows was compared using Welch’s t- test.

For each species I examined the relationship between flock size and call rate. For the Dark-eyed Junco I used polynomial regression. For the American Tree Sparrow, I used linear regression.

CHAPTER 3

RESULTS

Comparison of call rates (number of calls /bird/ minute) at the two winter feeding stations for the Dark-eyed Junco showed that there was no significant difference between the feeding stations (v = 58 ,P = 0.24). Similarly, there was no significant difference between the two winter feeding stations for call types (number of call types/ bird/ minute) produced by Dark-eyed Juncos (v = 50, P = 0.12). The lack of differences between feeding stations in these two key variables indicates that data from the two feeding stations can be pooled for further analysis.

Comparison with data collected along walking transects showed that call types produced by flocks at the feeding stations included all call types produced by natural flocks for Dark-eyed Juncos. Dark-eyed Juncos at feeding stations made “Twit” calls most often with “Twitter” and “Seep” occurring slightly less frequently (Fig. 5). “Chack” and “Kew” calls were made rarely, each constituting less than 2% of recorded calls. Dark-eyed Juncos at transects made “Twitter” calls more frequently with “Twit” and “Seep” calls made less frequently. Consistent with the distribution of call types produced at the feeding stations,

Juncos made “Chack” and “Kew” calls rarely along transects. Pearson’s chi squared test shows that there is a significant difference in the distribution of call types between transects and feeding stations (χ2 = 23.523, df = 4, P = 9.953e-05). The strength of this effect likely results from high levels of statistical power associated with large sample sizes of calls at feeding stations.

Transects Feeing stations 4500 4234 4000 3540 3536 3500 3000 2500 2000 1500 Number calls ofNumber 1000 500 181 194 15 31 5 2 1 0 Twit Twitter Seep Chack Kew

Call types

Figure 5: Frequency distribution of call types of Dark-eyed Juncos at winter feeding stations and along transects.

Although there was a large difference in mean call rates between the species, large variation in American Tree Sparrow call rates lessened my ability to detect significant differences between the species. Mean call rate of the Dark eyed Junco was 0.12 calls / bird

/ minute whereas the mean call rate of American Tree Sparrow was 1.62 calls / bird / minute (Fig. 6). Welch’s t-test suggests that there is no significant difference in mean call rates of the two species (t = 1.57, df= 24.02, P = 0.13).

Figure 6: Call rates of American Tree Sparrows (ATSP) and Dark-eyed Juncos (DEJU) at winter feeding stations. Values are mean + SE.

Number of call types given per observation period differed between the two species.

Dark-eyed Juncos produced more than one call type in every observation period, while

American Tree Sparrows produced only one call type, which was their alarm call, throughout the observations (Table 1). Fisher’s exact test suggests that there is a significant association between the number of call types given per observation period and bird species (P = <2.2e-16).

Table 1: Number of call types produced by Dark-eyed Juncos (DEJU) and American Tree Sparrows (ATSP) during 30 minute observation intervals at winter feeding stations.

Species

DEJU ATSP

One call type 0 25 Call Diversity More than one call type 36 0

There is a large difference in the mean flock size of Dark-eyed Juncos and American

Tree Sparrows at the winter feeding stations. Mean flock size of Dark-eyed Juncos is 8.71 birds whereas the mean flock size of American Tree Sparrows is 2.57 birds (Fig. 7). Welch’s t test suggests that there is a significant difference in mean flock size between the two species (t = -7.2901, df = 22.51, P= 2.314e-07).

Figure 7: Average flock size of American Tree Sparrows (ATSP) and Dark-eyed Juncos (DEJU). Values are mean + SE.

For both bird species, call rate (calls / bird / minute) appears to be related to their flock size. Dark-eyed Juncos have a negative quadratic relationship between their flock size and call rate (F 1, 15 value = 11.426, Pr = 0.004) (Fig. 8). A significant negative linear relationship can be observed when one potential outlier is removed from the Dark-eyed

Junco data (F 1, 20 value = 10.059, Pr = 0.006) (Fig. 9).

Figure 8: Relationship between flock size and call rate of Dark-eyed Juncos (DEJU): with a potential outlier. Each dot represents a 30 minute observation period. The regression equation is y=0.6822-0.1189x+0.0055x2.

Figure 9: Relationship between flock size and call rate of Dark-eyed Juncos (DEJU): without the potential outlier. Each dot represents a 30 minute observation period. The regression equation is y= 0.1741-0.0084x.

American Tree Sparrows do not display a positive or negative relationship between the flock size and their call rate (F 1, 22 value = 0.020, df = 1, Pr = 0.887) (Figure 8).

Figure 10: Relationship between flock size and call rate of American Tree Sparrows (ATSP): with potential outliers. Values are mean + SE. No regression equation is provided because the relationship is not statistically significant.

When potential outliers were removed, a negative trend, which is not a significant relationship, between the flock size and the call rate of American Tree Sparrows were detected (F 1, 19 value = 3.082, df = 1, Pr = 0.095) (Figure 9).

Figure 11: Relationship between flock size and call rate of American Tree Sparrows (ATSP): without potential outliers. Values are mean + SE. The regression equation for the marginally significant relationship is y=0.5135-0.0893x.

CHAPTER 4

DISCUSSION

4.1: High vocal complexity coincides with high fat storage

Previous studies have sought to explain variation in fat store among small bodied wintering bird species by focusing upon differences in feeding guilds and habitats.

However, even within species that belong to the same feeding guild and use the same habitats substantial variation in fat store remains unexplained. I carried out a study over two winter field seasons in order to explain the difference in fat storage in Dark-eyed

Juncos and American Tree Sparrows, both ground-feeding species in open habitats. The goal of my study was to test the hypothesis that small bodied wintering bird species with more complex vocal communication systems can sustain greater fat reserve than bird species with less complex vocal communication systems. Dark-eyed Juncos and American

Tree Sparrows differed consistently in the diversity of call types that they produced at winter feeding stations. Supporting the hypothesis, Dark-eyed Juncos, which stores more winter fat, produced more than one call type in all observation periods whereas American

Tree Sparrows, which stores less winter fat, produced only one call type throughout the observations. Surprisingly, the only call type produced by American Tree Sparrows during the observation periods was their alarm call.

Although Dark-eyed Juncos used their alarm call rarely, the commonly used calls that I documented may allow greater vigilance by sharing information required for other tasks. The Twit call is associated with flight or preparation for flight. Response to twit by others would be to attend to the caller or to follow their direction of flight (Balph 1977);

therefore it aids in flock integration. Since twit was produced most frequently by Dark-eyed

Juncos at feeding stations, high flock integration can be observed in Dark-eyed Juncos. Seep calls are produced usually upon arrival at patches of food. When individuals locate food at feeding stations they produced their seep call frequently. Since bird seed is available at the feeding stations, the seep call was produced frequently at the feeding stations. Juncos perform a bill-up display near a scarce resource in the presence of another bird. Twitter is usually produced by either or both participants in the bill-up display (Sabine 1949, Balph

1977). Since food at the feeding station is a limited resource they produced the twitter call frequently at the feeding stations. By sharing information concerning common and necessary tasks, these three calls may free junco attention for predator awareness.

The two more rarely produced call types, Chack and Kew, are critical to communication, but they are used in situations that birds encounter less frequently. The

Chack call is often expressed near a ground predator (Hostetter 1938) and it is a general alarm call during winter (Bent 1968). Therefore, it is relatively a rare call. The Kew call of

Dark-eyed Junco is a distance increaser, which is given when rivals approach at feeding stations (Balph 1977). Balph (1977) had observed that when juncos gave Kew calls they generally produced the call without stopping their eating upon the arrival of rivals. The incoming bird responded by advancing no further or by leaving the feeding station. When juncos feed in flocks, rivals are least expected. Since this call is produced among rivals, it is produced less compared to the other call types.

Communication among birds can be a function of both call diversity and call frequency. Dark-eyed Juncos produced a total of five different call types with a call rate of

0.12 calls / bird / min and American Tree Sparrows produced only one call type with a call rate of 1.62 calls/ bird / min. Although American Tree Sparrows produced only one call type, they produced it more often than the Dark-eyed Juncos. Since the vocal repertoire can be a measure of the number of call types produced and the frequency of the calls being produced, call rate plays a significant role in determining the size of the vocal repertoire.

However, physical characteristics of calls, such as the pitch and loudness of each call, rather than the absolute size of the vocal repertoire may be most important to effective communication (Collias 1987). Therefore a bird species with more call types aiding in different functions will have a complex vocal repertoire, where they can communicate efficiently with more information. Hence, even though American Tree Sparrows has a higher mean call rate, their communication is not efficient as Dark-eyed Juncos.

Wintering bird calls of DEJU were recorded in winter 2015 whereas bird calls of

ATSP were recorded in winter 2016. Data collection on the different species in different winter periods might potentially have a confounding effect on the results. However, winter

2015-2016 and winter 2016-2017 were similar climatically (see Study Site section of the

Methods). Both winters of my data collection were exceptionally warm and had little snowfall. Hence, we can assume that bird behavior was not substantially influenced by differences between the two years.

The hypothesis that complex vocal repertoire allows greater fat storage can be further tested in consecutive years to identify a general pattern in communication. Similar experimental results in consecutive years would provide strong support for my hypothesis.

This will also provide information on any variation in communication patterns with

regards to mean temperature and mean snowfall during winters. Juncos use numerous visual and vocal signals to maintain contact with flock members and therefore enhance flock integration (Balph 1977). Since non-vocal communication also plays a significant role in bird communication, using video recordings would be appropriate to identify which bird produces the vocal signals and non-vocal signals while feeding. Using this technique we can also identify visual cues of American Tree Sparrows that have not been recorded yet.

This study addressed causes of differences in fat storage in small wintering birds in open habitats in the ground foraging guild. However, this interspecific comparison provides only one case study in support of the hypothesis. There is variation in fat deposition among bird species that use closed winter habitats in the ground foraging guild and this variation provides an opportunity to further test the hypothesis of a positive correlation between vocal communication complexity and fat storage (Rogers 2015). The fattest bird species in the closed winter habitat is the White-throated Sparrow (Zonotrichia albicollis), while the Fox Sparrow (Passerella iliaca) has the least fat deposition. The White- crowned Sparrow (Zonotrichia leucophrys), Song Sparrow (Melospiza melodia), Swamp

Sparrow (Melospiza Georgiana), Harris’ Sparrow (Zonotrichia querula) and Spotted Towhee

(Pipilo maculatus) have intermediate levels of fat deposition. The hypothesis can be further tested using other sparrow species in the closed winter habitats in ground foraging guild following the same procedure since they have a variation in their fat deposition.

4.2: Patterns in vocalizations by the American Tree Sparrows and Dark-eyed Juncos

During this research American Tree Sparrows produced only one call type at feeding stations, which was their alarm call. American Tree Sparrows often made this alarm call

when there was no predator in the vicinity. This result suggests that American Tree

Sparrows produce a false alarm call during times of limited food supply. A previous experiment on fasting ability of American Tree Sparrows and Dark-eyed Juncos revealed that there is no evidence that American Tree Sparrows reduce metabolic expenditure during fasting compared to Dark-eyed Juncos or that they engage in any behavioral changes that seem to result in energy saving. Both American Tree Sparrows and Dark-eyed Juncos become restless based upon the level of remaining energy stores, not upon the amount time since they fed last (Stuebe and Ketterson 1982). Even though American Tree

Sparrows and Dark-eyed Juncos respond to fasting in similar manner, American Tree

Sparrows become stressed sooner than Dark-eyed Juncos when deprived of food (Stuebe and Ketterson 1982). Therefore American Tree Sparrows might be more likely to produce a false alarm call to drive away their conspecifics.

A comparison of mean flock size of the two species supports the idea that American

Tree Sparrows may be attempting to deter competing conspecifics with false alarm calls.

Mean flock size of Dark-eyed Juncos is 8.71 and mean flock size of American Tree Sparrows is 2.57, significantly smaller. A negative trend was observed between call rate and flock size of American Tree Sparrows. This also supports the hypothesis that American Tree

Sparrows produce a false alarm call in winter to increase access to scarce food.

The behavior of producing false alarm calls during times of food scarcity has been documented for several small-bodied wintering bird species. Great tits (Parus major) use false alarm calls in order to get access to food (Møller 1988). Similar dishonest alarm calls were described for Marsh tits (Parus palustris) and Willow tits (Parus montanus)

(MATSUOKA 1980). According to Moller’s observations, Great tits produce false alarm calls when food is scarce, such as during snow storms, or when Great tits feed rapidly in order to refill fat stores. 63% of the alarm calls of Great tits were classified as false alarm calls because no predators were seen in the vicinity when the call was made. But Moller observed that during adverse weather conditions Great tits produced false alarm calls more frequently (90.2+ 11.1%) than during benign weather conditions (26.6+24.3%).

Further, use of false alarm calls to deter conspecifics from limited food resources may be a taxonomically widespread strategy in birds. For example, Fork-tailed Drongos (Dicrurus adsimilis) produced false alarm calls 48+8% from a perch when the other target bird was handling a food item (Flower 2011).

False alarm calls may become ineffective when made too frequently relative to honest alarm calls. The limit on how frequently a false alarm call can be used effectively will depend on the frequency of attacks by real predators and the cost to the individuals that is being influenced (Møller 1988). But, the cost of not responding to an alarm call will be capture by a predator. I am unable to explain the reason why American Tree Sparrows produced no call types except the alarm call. To further explain this situation, time between two alarm calls can be taken into consideration to calculate the frequency of the calls produced. During my observations I counted the absolute number of calls during 30 minutes. But, to get this 30 minutes, I was in the field for more than two to three hours. If I can consider the time gap between two alarm calls, I can get an idea about how frequently they produce the call. As a future study, we can present a predator to American Tree

Sparrow flocks to calculate the frequency of alarm calls produced by American Tree

Sparrows. This future study will reveal the difference between the frequencies of alarm

calls produced when there is a predator compared to when predators are absent.

Therefore, this proposed study would help confirm that American Tree Sparrows produce a false alarm call.

The negative quadratic relationship between flock size and the call rate of Dark- eyed Juncos was an unexpected result. The quadratic nature of the relationship is driven by one observation that involved a very high call rate in a very small flock. A negative linear relationship is observed when this observation is removed. There are several possible hypotheses for why call rate should decline with increasing flock size. First, once Dark-eyed

Junco individuals have integrated the flock to locate food resources, they might not need to vocally communicate further. Since neighbors are close to one another, they can use visual signals to communicate. The value of information given by an individual of the flock who is vigilant to changes in the environment is thought to decrease with increasing distance between individuals (Seppänen, Forsman et al. 2007, Boujja‐Miljour, Leighton et al. 2017) and the vigilance rate seems to increase with group size (Elgar, Burren et al. 1984).

Therefore, when neighbors are close together, they can use non-vocal communication to share information. Second, Dark-eyed Juncos may not produce calls with their mouths full.

Once a large enough flock is assembled, a few flock members may remain vigilant while the other birds feed.

4.3 Conclusion

There is substantial variation in fat deposition in small wintering birds that belong to the same feeding guild and use the same habitats. The present study is the first to suggest the relationship between winter fat deposition and vocal communication system of

small wintering birds. Dark-eyed Juncos consistently produced more than one call type whereas American Tree Sparrows produced only one call type throughout the observations. American Tree Sparrows produced a false alarm call to drive away the conspecifics from the limited food supply. Therefore they are dishonest with their communication providing false information. By contrast, Dark-eyed Juncos produced honest signals and that help in true communication. True communication of Dark-eyed

Juncos helps in detecting food resources, maintaining interactions within the individuals in flock and alarming flock members about the presence of predators. Therefore Dark-eyed

Juncos can have a high fat reserve and at the same time they can escape from predators. In conclusion, these results support the hypothesis that communication ability plays a significant role in determining interspecific variation in fat levels of small wintering birds.

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