Examining Calf Behavioral Development in Beluga Whales

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Master's Theses

Spring 5-1-2019

First Thirty Days of Life: Examining Calf Behavioral Development in Beluga Whales (Delphinapterus leucas) and Pacific White-Sided Dolphins (Lagenorhyncus obliquidens) at One Zoological Facility

Kendal Smith University of Southern Mississippi

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Recommended Citation Smith, Kendal, "First Thirty Days of Life: Examining Calf Behavioral Development in Beluga Whales (Delphinapterus leucas) and Pacific White-Sided Dolphins (Lagenorhyncus obliquidens) at One Zoological Facility" (2019). Master's Theses. 606. https://aquila.usm.edu/masters_theses/606

This Masters Thesis is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Master's Theses by an authorized administrator of The Aquila Digital Community. For more information, please contact [email protected]. FIRST THIRTY DAYS OF LIFE: EXAMINING CALF BEHAVIORAL DEVELOPMENT IN BELUGA WHALES (DELPHINAPTERUS LEUCAS) AND PACIFIC WHITE-SIDED DOLPHINS (LAGENORHYNCHUS OBLIQUIDENS) AT ONE ZOOLOGICAL FACILITY

Kendal Smith

A Thesis Submitted to the Graduate School, the College of Education and Human Sciences and the School of Psychology at The University of Southern Mississippi in Partial Fulfillment of the Requirements for the Degree of Master of Arts

Approved by:

Mark Huff, Committee Chair Lance Miller Richard Mohn Don Sacco

______Dr. Mark Huff Dr. Joe Olmi Dr. Karen S. Coats Committee Chair Director of School Dean of the Graduate School

May 2019

Kendal Smith

2019

Published by the Graduate School

ABSTRACT

Cetacean development is important for general comparative understanding and the implementation of informed husbandry policies. Due to the inaccessibility of many of these species in the wild, researchers can study managed care populations to better understand basic developmental patterns of cetaceans, as well as to improve husbandry policies for facility animals. However, no previous studies have attempted to observe the behavioral development of Pacific white-sided dolphins (Lagenorhyncus obliquidens).

Eight beluga whale calves and four Pacific white-sided dolphin calves were observed for the first 30 days of life to determine the developmental trajectory of several typically monitored behaviors. The first occurrence and developmental trajectory for each behavior are described to identify variation and to document differences between successful calves, those that survived the 30-day period, and unsuccessful calves, those that did not survive the 30-day period, of both species. A single-case time series design analyzed developmental pattern differences within the 30 days for the successful calves. Overall, beluga whales and Pacific white-sided dolphins exhibited similar developmental trends; however, beluga whale calves had significantly higher nursing duration and frequency and rates of slipstream position than Pacific white-sided dolphin calves. Nursing behaviors and slipstream behaviors of the unsuccessful calves of both species were either inconsistent or delayed compared to the successful calves. The results of this study may be used to better understand norms of cetacean development and to stimulate future research in the early identification of abnormal development in the hopes of increasing calf survival rates.

ACKNOWLEDGMENTS

Thank you to the staff of the John G. Shedd Aquarium in Chicago, Illinois. The data contribution made the success of this project possible, and the assistance and continue support offered by the staff members and trainers ensured the project’s completion.

I would like to acknowledge the support and extensive contributions from Dr.

Lance Miller. His instruction provided me with unmatched knowledge about the field of marine mammal behavioral research, and I am truly grateful for the experience.

Thank you, as well, to the ladies of the Marine Mammal Behavior and Cognition

Lab at the University of Southern Mississippi. The emotional and intellectual support provided by my fellow lab members made the successful completion of this project and my Masters degree progression possible.

I would also like to acknowledge the support and contribution from Dr. Mark

Huff, my thesis advisor. His willingness and ability to step out of his comfort zone and research field to oversee my project’s progression made the completion of my degree a possibility.

iii

DEDICATION

This Master’s thesis is dedicated to Dr. Stanley Kuczaj II. Although you were not around to see the completion of this project, I still believe that you would have been proud of the work I have accomplished thus far. The pain of your loss still affects me to this day, but the drive to push and succeed in your name motivates me to continue to pursue my dreams of working in marine mammal research.

This thesis is also dedicated to my mother, Dr. Patti Rasberry Smith. I have always admired your strength and compassion. I never truly understood nor appreciated how fierce and how passionate you are to have accomplish everything you have done.

The ability to have obtained a PhD while working a full-time job and raising three children simply stuns me. I can only hope that one day as I follow this path that I can display the amount of strength you have.

Finally, this thesis is dedicated to Michael Vines. You were my foundation during the adversity I have faced. Without your emotional support, I do not think this project would have ever succeeded. Thank you for motivating me and for holding me accountable during this process. Words can’t describe how much I appreciate all that you have done to keep me focused and sane.

TABLE OF CONTENTS

ABSTRACT ...... ii

ACKNOWLEDGMENTS ...... iii

DEDICATION ...... iv

LIST OF TABLES ...... viii

LIST OF ILLUSTRATIONS ...... ix

CHAPTER I – INTRODUCTION ...... 1

Use of Developmental Trajectories ...... 1

Cetacean Calf Development ...... 3

Beluga Whales ...... 5

Pacific White-Sided Dolphins...... 7

Nursing Patterns ...... 8

Swim Positions...... 11

Association Rates ...... 13

Respiration Rates ...... 15

Current Study ...... 16

CHAPTER II – METHODS ...... 18

Ethics Statement...... 18

Facility and Subjects ...... 18

Data Collection ...... 20 v

Data Analysis ...... 20

CHAPTER III – RESULTS ...... 23

Observer Reliability ...... 23

Nursing Patterns ...... 23

Nursing Bouts ...... 23

Nursing Duration ...... 29

Nursing Average ...... 32

Calf Position...... 36

Associations ...... 40

Maternal Associations ...... 40

Conspecific Association...... 44

Respiration ...... 50

CHAPTER IV – DISCUSSION...... 54

Developmental Norms ...... 54

Unsuccessful Calves ...... 57

Conclusions ...... 61

APPENDIX A – Subjects and Ethogram ...... 62

APPENDIX B – Results: Tables ...... 64

APPENDIX C – Results: Figures ...... 70

APPENDIX D – Research Approval ...... 74 vi

REFERENCES ...... 75

vii

LIST OF TABLES

Table A1. Demographic Information of Subject Animals ...... 62

Table A2. Operational Definitions for Coded Behaviors ...... 62

Table B1. Descriptive Statistics for First Occurrence of Behaviors ...... 64

Table B2. Descriptive Statistics of Calf Behaviors for Successful Beluga Whales Over 30

Days ...... 65

Table B3. Descriptive Statistics of Calf Behaviors for Successful Pacific White-sided

Dolphins Over 30 Days ...... 66

Table B4. Descriptive Statistics of Calf Behaviors for Unsuccessful Calves...... 67

Table B5. Mean Difference Values for Behaviors in Each Time Period for Individual

Beluga Calves and Group ...... 68

Table B6. Mean Difference Values for Behaviors in Each Time Period for Individual

Pacific White-Sided Dolphin Calves and Group ...... 69

viii

LIST OF ILLUSTRATIONS

Figure 1. Whale Harbor enclosure ...... 19

Figure 2. Secluded Bay enclosure ...... 19

Figure 3. Mean nursing onset (in hours) following birth of Pacific white-sided dolphins and beluga whales. Bars = 95% CI...... 24

Figure 4. Mean nursing onset (in hours) following birth of successful and unsuccessful calves...... 25

Figure 5. Mean daily nursing bout frequency between each 10-day time period...... 26

Figure 6. Developmental onset of daily mean nursing bouts of successful and unsuccessful calves...... 28

Figure 7. Mean daily nursing duration between each 10-day time period...... 30

Figure 8. Developmental progression of total daily nursing duration of calves over 30 days...... 32

Figure 9. Mean nursing seconds per bout between each 10-day time period...... 33

Figure 10. Developmental progression of daily mean nursing seconds per bout over 30 days...... 35

Figure 11. Mean slipstream rate between each 10-day time period...... 37

Figure 12. Developmental progression of daily slipstream rate over 30 days...... 39

Figure 13. Mean maternal association rate between each 10-day time period...... 41

Figure 14. Developmental progression of daily rate of maternal association over 30 days.

...... 43

Figure 15. Mean conspecific association onset (in days) following birth of beluga whales and Pacific white-sided dolphins. Bars = 95% CI...... 44

Figure 16. Mean conspecific association onset (in days) following birth of successful and the unsuccessful calves...... 46

Figure 17. Mean conspecific association rate between each 10-day time period...... 47

Figure 18. Developmental progression of daily rate of conspecific association over 30 days...... 49

Figure 19. Mean respiration rate between each 10-day time period...... 51

Figure 20. Developmental progression of mean daily respiration rate over 30 days...... 53

Cetacean Calf Watch Behavioral Ethogram ...... 63

Figure C1. Developmental progression of mean daily nursing frequency for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 70

Figure C2. Developmental progression of mean daily nursing duration for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 71

Figure C3. Developmental progression of daily mean duration per nursing bout for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 71

Figure C4. Developmental progression of mean daily slipstream rate for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 71

Figure C5. Developmental progression of mean daily maternal association rate for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 72

Figure C6. Developmental progression of mean daily rates of conspecific association for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 72

Figure C7. Developmental progression of mean daily respiration rate for beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI...... 73

CHAPTER I – INTRODUCTION

Understanding physical, social, and cognitive developmental changes of animals across the lifespan has several practical implications for researchers, zoo personnel and conservation policy makers alike. Zoo and aquarium settings provide researchers with long-term opportunities to observe behavioral and biological factors that serve as objective measures for assessing positive welfare conditions (Hill, Dietrich, et al., 2015).

These professionally managed environments allow humans to study the behavioral repertoire of several different well-known species to identify behavioral and developmental norms on an individual and group level. Establishing developmental norms is crucial for cetacean populations and can provide necessary information to assist facility personnel in assessing the health and welfare of the animals under their care.

Identifying developmental norms is considered just as important for maintaining these cetacean populations as collecting biological indicators of health, such as infant survival rates, fertility rates, and rates of stillbirths (Hill, 2009; Hill, Guarino, Crandall, Lenhart,

& Dietrich, 2015).

Use of Developmental Trajectories

Developmental information must be gathered for newborn cetaceans both within professional human care and in the wild. Understanding normative developmental trajectories is of utmost importance for increasing the likelihood of survival of these young individuals in zoo and aquarium settings. Once these developmental landmarks have been established, animal care staff can better identify potential health concerns of future offspring. Facility personnel can create more informed policies about the

appropriateness of when to intervene to increase survival rates of cetaceans under their care (George & Noonan, 2014). The results provided by developmental studies may also facilitate cross-species comparisons, to further facilitate the implementation of effective intervention policies that are appropriate for each species (Clark & Odell, 1999; Drinnan

& Sadleir, 1981).

Data collected in zoos and aquariums also have utility in field settings. To conserve wild populations of cetaceans, developmental behavioral patterns need to be established. Conservation efforts are of increasing importance, not only to researchers but to the public community, as many wild marine mammal species undergo threats to the preservation of their natural habitats, affecting their natural reproductive behavior (Hill,

2009). For instance, developmental trajectories of beluga whales (Delphinapterus leucas) under human care follow developmental trajectories of their wild counterparts (Hill,

Campbell, Dalton, & Osborn, 2013). Trajectories that are established by zoo and aquarium communities may therefore be used as a guideline for assessing the health of wild populations (Miller, Styer, Decker, & Robeck, 2002).

Behaviors, such as social interactions, maternal care, nursing patterns, and respiratory patterns, are all important indicators to monitor the developmental trajectories of cetaceans housed in human care facilities (Hill et al., 2013; Hill, Alvarez, Dietrich &

Lacy, 2016; Robeck et al. 2005). However, it is of equal importance to assess the population averages of each of these behaviors, as well as any abnormal patterns that could indicate developmental pathologies of and potential health threats to individuals within the population. For instance, Hill (2009) reported increased rates of swimming in both echelon and infant positions, swim positions where the calf aligns itself aside the

mother to reduce the physical demands of swimming alone, in an ill beluga whale calf.

Identifying this abnormal behavioral pattern could have prompted facility staff to medically intervene. Previous research has focused on the development of beluga whales in marine parks; however, no such studies have been conducted on Pacific white-sided dolphins (Lagenorhyncus obliquidens), establishing a need for developmental research to be conducted on this species.

Cetacean Calf Development

Beluga whales and Pacific white-sided dolphins are both members of the sub- order Odontoceti. Odontocetes, or toothed whales, dolphins, and porpoises, exhibit similar developmental patterns to ungulates and primates (Karenina, Giljov, Ivkovich,

Burdin, & Malashichev, 2013). Odontocete infants exhibit early, strong social bonds with their mothers, usually maintained for longer periods of time when compared to other taxonomic groups. An extended gestational period is crucial for offspring survival in odontocetes, as cetacean calves are born without being physically fully developed

(Tardin, Espécie, Lodi, & Simão, 2013). However, cetaceans physically develop at exponential rates. Calves typically double their weight within the first week of life and continue these rapid growth patterns during the first year (Russell et al., 1997). Cetacean calves must begin swimming immediately after birth, relying heavily on maternal assistance at first then increasing in independence with physical maturity. One-month old calves can reach 32% of adult swim speeds on average (Noren, Biedenbach, & Edwards,

2006). Likewise, the behavioral changes that occur during the first month of life are typically the most extreme changes to occur when compared to the rest of the individual’s

lifespan. Typically, early social interactions that occur within the first month of life are indicative of behavioral responses that will persist into adult social relationships

(Krasnova, Bel’Kovich, & Chernetksy, 2009).

Cetacean mothers play a significant role in protection for their calves. Beluga dams provide a physical buffer between their calves and any potential threat, including conspecifics, older males, or predators. While at breeding grounds, mother-calf pairs of several species avoid any males to prevent interrupting competitive bouts (Sardi, Connor,

& Weinrich, 2005). Extended gestational periods also provide infants the opportunity to gain motor and social experience, while still reaping the benefits of increased protection and access to nutritional resources (Tardin et al, 2013; Tyack, 1986). Offspring typically match maternal swim patterns, respiration, foraging behaviors, and behavioral responses in social situations (Szabo & Duffus, 2008). Beluga whale calves learn migration patterns from members of their pod by traveling along the routes with them (Colbeck et al., 2012;

Matthews & Ferguson, 2015). Young whale calves are not physically able to make deep foraging dives, so mothers will also alter their behavior by foraging at shallower depths and limiting the duration of feedings so their calves can observe these behaviors

(Mishima et al., 2015). Hill, Dietrich, et al. (2015) reported that two-day old bottlenose dolphin calves initiate sociosexual interactions with their mothers, presumably to learn the appropriate behaviors for this context.

Although the developmental trajectory of cetacean species is an important area of study for both wild and managed care populations, it is a relatively understudied topic, with only a few studies conducted on the changes in behavioral patterns in beluga whales e.g., Caron, 1987; George & Noonan, 2014; Hill et al., 2013, 2014; Krasnova,

Bel’kovich, & Chernetsky, 2006; Morgan, 1979; Robeck et al., 2005. No known studies have examined the behavioral development of Pacific white-sided dolphins.

Beluga Whales

Beluga whales, an ancestral species belonging to the family monodontidae, were the first aquatic mammals to be placed under professional human care (Miller, Styer,

Decker, & Robeck, 2002; Recchia, 1994). Identifying and understanding developmental patterns of behavior in belugas housed in zoos and aquariums can be used as a starting point for future studies assessing similar patterns of behavior in wild belugas. Caron

(1987) showed that the behavioral patterns of belugas in human care are not significantly influenced by the presence of humans, making comparisons to wild populations valid.

Wild beluga whales are circumpolar, found around high-latitude Arctic and sub-

Arctic waters where they breed between the months of February and May before migrating to warmer calving grounds in the summer to birth and rear very young calves

(Boltunov & Belikov, 2002; Colbeck et al., 2012). They are a deep-diving species with an average lifespan of 50 years (Leung, Vergara, & Barrett-Lennard, 2010). Beluga whales typically return to the same calving grounds each year which are typically located in shallow waters to avoid possible predation from orcas in open waters (Lomac-MacNair,

Smultea, Cotter, Thissen, & Parker, 2016; Lucey et al., 2015).

Although belugas typically exhibit rapidly changing fission-fusion societies, members of a beluga whale pod, which range from two to hundreds of members (Hill,

Dietrich et al., 2015; Recchia, 1994), form relatively tight, stable bonds with other members of their group. (Krasnova et al., 2006). Mother beluga whales and their

offspring form tight, stable groups during migration periods (Krasnova, Chernetsky,

Zheludkova, & Bel’Kovich, 2014; Miller et al., 2002; Vergara, Michaud, & Barrett-

Lennard, 2010). This tight association between beluga whale mothers and their calves provides a stable core for the maternal pod (Hill, 2009; Krasnova et al.). Beluga whales have a gestation period of 15-16 months on average and nursing periods that last for an average of 24 months (Lilley, Smith, & Botero-Acosta, 2017; Matthews & Ferguson,

2015). Beluga whales have a calving period of three years, so only one offspring is usually cared for by the mother at a time (Steinman, O’Brien, Monfort, & Robeck, 2012).

Beluga calves are easy to identify, as they are born a dark grey color and lighten as they age until they eventually turn completely white by adulthood. Newborns are typically only one-third the length of their mothers, measuring an average of 150 cm

(Boltunov & Belikov, 2002). Within a year, calves will grow to 215 cm on average. Male calves are significantly longer than female calves but take more time to physically grow

(Krasnova et al., 2014; Recchia, 1994; Suydam, 2009). Forty percent of a beluga whale’s mass consists of blubber, which allows for thermoregulation, energy storage, and buoyancy (Birkeland, Kovacs, Lydersen, & Grahl-Nielsen, 2005). These layers are largest in April, when beluga whales have more access to their preferred prey (Boltunov

& Belikov).

Although beluga whales do exhibit similar developmental patterns to several other species of cetaceans, the ideal species for comparison has yet to be identified. The most common comparisons across species are usually made with species of the family delphinidae, including bottlenose dolphins and Pacific white-sided dolphins (Hill,

Dietrich et al., 2015). Although these species exhibit some behavioral differences, Yeater

et al. (2014) found that Pacific white-sided dolphins are phylogenetically similar to bottlenose dolphins, potentially identifying them as a valid species for comparative studies. Developmental similarities have previously been difficult to determine as few behavioral studies have been conducted on this species.

Pacific White-Sided Dolphins

Free-ranging Pacific white-sided dolphins are one of the most abundant species that inhabit the Northern Pacific Rim (Ferrero & Walker, 1996; Robeck et al., 2009).

Herds of Pacific white-sided dolphins in the wild usually travel together in large hunting groups that provide this smaller dolphin species protection from larger predators such as orcas (Yeater, Hill, Baus, Farnell, & Kuczaj, 2014). Pacific white-sided dolphins have distinct seasonal reproductive periods. Conception typically occurs between June and

August. This species has a comparatively short gestational period of 11 months (Robeck et al.). Pacific white-sided dolphins are a smaller species of cetacean, only weighing between 82-161 kg and are 1.72m-2.26m in length (Dalton, Robeck, & Young, 1995;

Miller et al., 2002). Male Pacific white-sided dolphins tend to be slightly longer than females, and calves on average are born 91.8 cm long (Ferrero & Walker, 1996). One of the only known predictors of calf mortality is birth weight and length. Calves that weighed more and measured longer than average were more likely to have birthing complications than average-sized calves (Dalton et al., 2005).

Certain behaviors are typically assessed when researchers are studying the developmental progression of a species and when facility staff members are assessing the developmental milestones of young animals in their care. The behaviors included in those

studies include nursing behaviors, calf position, sociality, and respiratory behaviors

(George & Noonan, 2014; Hill, 2009; Robeck et al., 2005). Appropriate changes in the frequency and duration of these behaviors may be critical indicators of normal development in each of these species.

Nursing Patterns

For all mammals, maternal care can be provided in the form of lactation, or nursing. Nursing is behaviorally defined as the transfer of milk from mother to calf when the calf is at the mother’s mammary slit (Gero & Whitehead, 2007; Krasnova et al., 2009;

Thomas & Taber, 1984). Milk present in the water after this behavior occurs can also be considered evidence of nursing or attempted nursing (Clark & Odell, 1999; Leung et al.,

2010). However, if milk is regularly present in the pool during or after a nursing bout, this could indicate the calf is not successfully nursing from the mother or may be experiencing disturbances during nursing bouts that cause the calf to remove its mouth too early (Eastcott & Dickinson, 1987). As stated previously, young mammals can use these lactation periods as an opportunity to physically and behaviorally develop until they reach independence (Suydam, 2009; Szabo & Duffust, 2007). In comparison to other mammals, cetacean milk is typically high in fat content (between 10-30%) so energy demands of young cetaceans are met while they learn to independently forage and acquire solid food (Matthews & Ferguson, 2015; Oftedal, 1997). Odontocetes are thought to use extended nursing as a social learning period for group foraging behaviors and to facilitate mother-calf bonds (Tyack, 1986).

Cetaceans are quite proficient at nursing, even shortly after birth. One study reported the first successful suckle of a bottlenose calf was at 21 hours after birth

(Eastcott & Dickinson, 1987). However, there is typically a period where the calf must learn the most efficient method of nursing; calves are born with extra fat deposits that are used as caloric buffers during this learning period (Robeck et al., 2009). For the first two weeks of life, bottlenose dolphin mothers roll to their side to help infants locate the mammary glands. After this learning period, the calves submerge to locate the mammary glands without assistance from the mother (Caron, 1987). The mother beluga whale, however, is mostly responsible for the calf’s ability to successfully nurse from her

(Robeck et al., 2005). For younger calves, beluga whale mothers also roll to the side, giving the calf the best opportunity to nurse (Caron; Drinnan & Sadleir, 1981). Initially, these nursing bouts for younger calves only last on average between four and six seconds

(Krasnova et al., 2006). Once the calves are older and are more experienced, beluga whale mothers typically slow down their rates of speed and lift their tails to allow calves better access to her mammary glands once they have submerged (Birkeland et al., 2005).

Bottlenose dolphin calves nurse on average every 30 minutes (Eastcott &

Dickinson, 1987) whereas beluga calves nurse on average every 32 to 42 minutes

(Russell et al., 1997). Although frequency of nursing tends to decrease with age, duration of nursing tends to increase; this is likely because calves must slightly submerge themselves to obtain milk from the mother’s mammary glands. Longer nursing bout durations are likely associated with both the calf’s physical ability to remain submerged for longer periods of time and increased nursing experience (Krasnova et al., 2009;

Thomas & Taber, 1984). Suckling frequency and duration for beluga whales peak

between 7-10 days of life before decreasing and usually stabilize and become more consistent approaching the first month of life (Russell et al.). Male beluga whale nursing patterns peak and stabilize faster than females (Clark & Odell, 1999). Pacific white-sided dolphins exhibit a similar peak in suckling patterns at 7 days of life, followed by decreasing rates until more consistent patterns occur (Dalton et al., 2005; Robeck et al.,

2005). Some nursing bouts may also be preceded by begging behavior in both beluga whales and bottlenose dolphins where the calf will bump the mammary slits of the mother, presumably to stimulate the release of milk and initiate a nursing bout (Krasnova et al., 2006; Miller et al., 2002; Recchia, 1994).

Odontocete calves begin to consume solid foods at approximately three to six months for smaller species, around a period known as mid-lactation where nursing duration and frequency stabilizes and ultimately decreases as the calves become increasingly reliant on solid food. Bottlenose dolphins typically begin consuming solid food between four and eleven months of age, yet they do not wean until approximately 18 months (Oftedal, 1997). Larger species of odontocetes, especially beluga calves, may not reach this mid-lactation period until approximately one year of life when their adult teeth emerge (Birkeland et al., 2005; Russell, Simonoff, & Nightingale, 1997). Despite this early consumption of solid food, lactation in beluga whales usually lasts for up to two years (Drinnan & Sadleir, 1981; Leung et al., 2010).

Monitoring and recording nursing behaviors of beluga whales and Pacific white- sided dolphins in human care are essential to the development of husbandry policies, as abnormal nursing patterns may be a useful diagnostic tool for uncovering a potential health problem (Robeck et al., 2005). In one study, a beluga calf experienced a severe

drop in nursing frequency and duration ten days before any other physical indicator of poor health was noted (Russell et al., 1997). Unfortunately, this calf eventually passed, but identification of abnormal development may have provided an intervention. Beluga calves with health issues are also known to essentially reduce or altogether stop suckling from their mothers (Drinnan & Sadleir, 1981).

Swim Positions

The calf’s swim position may also be used as an indicator of problems in several species of cetaceans. One of the closest associations found within mammal groups is the association between the mother and the infant (Caron, 1987). Infants of several different species, including various primates, right whales, sperm whales, and bottlenose dolphins, spend most of their time near their mothers (Recchia, 1994; Szabo & Duffust, 2007). Hill

& Campbell (2014) found that for one-year old beluga whales, mother-calf swims make up 32% of all swim behaviors versus 17.6% for solitary swims and 2.4% for swims with conspecifics, with the remaining observed time occupied by events outside the focus of the study. Hill and colleagues (2013) reported even higher rates of mother-calf swims, with female beluga whale calves swimming with their moms up to 60% of observation time and males swimming with their moms up to 90% of observation time. Immediately after birth, calves follow their mothers and learn locomotor, respiratory, and nursing or foraging behaviors, while also gaining the benefit of protection from predators and adult conspecifics (Krasnova et al., 2006; Tardin et al., 2013; Thomas & Taber, 1984).

Calves at certain developmental milestones will position themselves along the mother’s body based on their physical ability to swim alone for long periods of time.

During the first month of life, beluga whales have highly uncoordinated movements and spend a lot of time in the echelon position, which allows the mother’s slipstream to carry the calf without additional effort (Karenina, Giljov, Glazov, & Malaschichev, 2013).

Beluga calves also frequently align themselves below the mother’s peduncle, known as infant position; this position provides protection for the calf from predators, provides easy access for nursing, strengthens the maternal-calf bond, provides observational learning opportunities, and provides resting opportunities as the slipstream created by the mother’s movements reduces the physical demands of swimming for the calf (Krasnova et al., 2009; Tyson, Friedlaender, Ware, Stimpert, & Nowacek, 2012). Tardin and colleagues (2013) reported that infant position reduces fluke thrust of Guina dolphin calves, another small cetacean species, by approximately 60%. Miller and colleagues

(2012) similarly reported that more calves could be found swimming in infant position than any other type of swim position, but even calves as old as two months old were less likely to swim in infant position, presumably because once the calves have physically matured they no longer need the hydrodynamic benefits of the mother’s slipstream for locomotion (Krasnova et al.). Interestingly, the duration of time spent in positions other than infant or echelon position stays relatively stable for beluga whale calves (Xian et al.,

2012).

Deviation from these normal swim patterns could potentially indicate an underlying health issue of the calf. A study conducted on bottlenose dolphins found that a calf with health problems swam more often with his mother and could be found in infant

position more often to compensate for the lack of energy associated with illness (Hill,

2009). Once again, early identification is key to diagnosing and treating these potential calf health issues.

Association Rates

Calves and mothers remain in close proximity to each other even after the calves have become nutritionally independent (Recchia, 1994). At one week of life, bottlenose dolphin and beluga calves are rarely separated from their mothers (Hill, 2009). Young calves are typically restricted from interacting with other pod members by their mothers to protect them from threats associated with agonistic interactions (Krasnova et al., 2006;

Tardin et al., 2013). As beluga whale calves begin to grow and develop, within the first two weeks they begin to increase distance from their mothers and form associations with other members of the pod, separating at first for short periods of time (7 to 27 seconds) before increasing slowly in both frequency and duration (Krasnova et al., 2009). These early social interactions usually occur with younger calves and can be characterized by associative swims with conspecifics, brief tactile contact, and social play (Miller et al.,

2002; Hill et al., 2016).

Mothers initially are responsible for maintaining proximity to their calves, often retrieving them if separations do occur and monitoring them during times of separation

(Hill, 2009). Around one month of age, beluga whale and bottlenose dolphin mothers begin to decrease their interventions in calf social interactions, and calves become responsible for maintaining proximity with its mother (Hill et al., 2013; Karenina, Giljov,

Glazov, & Malashichev, 2013; Taber & Thomas, 1982). Consequently, calves

increasingly engage in more play behaviors with other members of the pod and imitate other whales’ behaviors more proficiently (Hill & Ramirez, 2014; Hill, Guarino et al.,

2015; Krasnova et al., 2014). Play allows calves the opportunity to practice newly acquired motor skills, as well as to form and maintain social relationships (Hill &

Ramirez, 2014; Thomas & Taber, 1984).

Once calves have sexually developed, approximately 4 to 7 years (Bel’kovich &

Yablokov, 1965), males often leave natal groups to form juvenile groups, allowing for more extensive social development. Odontocetes often form nursery groups, where multiple adult and juvenile female individuals assist in the care and protection of calves in the group, increasing the likelihood of calf survival (Tyack, 1986). Female calves typically remain in the same nursery group they are born in, providing an opportunity for females to further learn social behaviors, specifically maternal behaviors, through observation and imitation of older females.

Pacific white-sided dolphin calves, however, have been observed to first separate from their mothers slightly later than bottlenose dolphins and beluga whales, around 52 days old. Gradually, distance from mothers increase and social interactions between the mother and infant will decrease in favor of social interactions with conspecifics (Dalton et al., 1995).

Because calf social behaviors are shown to be representative of adult social behaviors, potential deficits in social behavioral development could have adverse lasting effects on future adult social relationships. Although no studies have observed these direct effects in cetaceans, abnormal social behavior can indicate poor welfare in goats

(Miranda de la Lama & Mattiello, 2010), rabbits (Bozicovich, Moura, Fernandes,

Oliveira, & Siqueria, 2016), and various species of farm animals (Rault, 2012).

Furthermore, Hill (2009) observed decreasing social interactions with conspecifics in a fatally ill calf. These findings indicate it is reasonable to expect changes in rates of association in calves with potential underlying health problems.

Respiration Rates

Respiration rates have widely been used as a rough diagnostic tool to assess the health status of several animal species in zoos and aquariums. Young cetacean calves’ respiratory systems are not fully developed at birth, so mothers with calves must remain closer to the surface to allow underdeveloped calves better access to breathe (Caron,

1987). Calves in all cetacean species typically have higher respiratory rates than the adults as respiration is positively correlated with measures of metabolic activity. Beluga whale and bottlenose dolphin calf respiration rates are on average 40% higher when compared to adult respiration rates, until approximately three years of age when respiration rates decrease to adult levels (Drinnan & Sadleir, 1981; George & Noonan,

2014). Higher respiration rates have also been associated with activities necessitating higher physical demand such as greater swim speeds and mating.

Monitoring respiration rates allow facility staff to determine if calves or other animals have an internal condition absent of additional external symptoms. Monitoring calf respiration after birth can help facility personnel decide if and when intervention is appropriate for a potentially ill calf. Changes in respiration rates, especially a significant increase, can be an indicator of a potential health problem. Early identification of poor

health can likely lead to earlier intervention and a better ultimate outcome, potentially increasing calf survival rates (George & Noonan, 2014).

The ideal subjects for a developmental study are cetacean mother and calf pairs.

Interactions between cetacean mothers and calves largely affect the physical, cognitive, and social development of calves (Karenina et al., 2010; Miller et al., 2002). During the first month of life, most behavioral events occur between the calf and its mother, making this pair of animals the ideal focus for a study attempting to observe the behavioral development during this stage of life (Recchia, 1994; Taber & Thomas, 1982). Although these behaviors have been studied extensively in bottlenose dolphins and beluga whales, none of these behaviors have been studied in Pacific white-sided dolphins.

Current Study

Identifying average developmental patterns is important general comparative understanding of cetacean species and implementing conservation and husbandry policies alike. If typical developmental norms for these species are identified, identification of abnormalities in developmental progression may be utilized to determine at risk calves.

Interventions could therefore be implemented to increase survival rates of beluga whale and Pacific white-sided dolphin calves.

The current study therefore aims to identify the first occurrence of several typically studied calf behaviors and determine the daily developmental progression of these same behaviors for the first 30 days of life in two species of cetaceans: Beluga whales and Pacific white-sided dolphins. The study also evaluates the onset and developmental progression in calves who later lived past the infancy period (successful)

and calves who did not live past the infancy period (unsuccessful). The present study focuses on the following four main categories of behaviors: Nursing, calf position, social association, and respiration. All behaviors were coded during 24-hour observation sessions for the first 30 days of life for approximately 720 hours of observations for 11 animals. Behaviors were coded using a combination of all-occurrence sampling and instantaneous sampling as well as prototypical procedures for recording respiration behaviors. The goals of this study are two-fold: 1) The study will attempt to examine the onset of these developmental behaviors and how these behaviors change within the first

30 days 2) The study will report differences between successful and unsuccessful calves in both species.

Hypothesis 1 is as follows: The developmental progression of these behaviors in the beluga calves are expected to be consistent with previous studies that examined these developmental behaviors, including nursing patterns, respiration rates, and association rates (Eastcott & Dickinson, 1987; Hill et al., 2013; Russell et al., 1997). Since beluga calves were not reported to show reliable differences in developmental trends from other odontocete species, especially bottlenose dolphins and orcas (Hill, 2009; Recchia, 1994;

Yeater et al., 2014), Pacific white-sided dolphin calves are expected to show similar behaviors. Hypothesis 2 is as follows: Unsuccessful calves in belugas and Pacific white- sided dolphins should display significant different in their developmental trends when compared to successful calves (George & Noonan, 2014; Hill, 2009. Unsuccessful calves are predicted to have lower frequency and duration of nursing behaviors, higher percentages of time spent in the infant position, lower rates of associations with other animals.

CHAPTER II – METHODS

Ethics Statement

The following procedures were approved for study by the John G. Shedd

Aquarium’s Research Committee as part of the staff’s standard animal care procedures for monitoring new calf births.

Facility and Subjects

The subjects for this study were housed during data collection at the John G.

Shedd Aquarium located in Chicago, Illinois. The Shedd Aquarium is an indoor public aquarium, and all cetaceans were housed in the Abbott Oceanarium exhibit in either the

Whale Harbor or the Secluded Bay enclosures. The Whale Harbor enclosure is approximately 8790 sq. ft2 with a maximum depth of 31 ft. and holds approximately 2 million gallons of manufactured salt water (Figure 1). The Secluded Bay enclosure is approximately 2695 sq. ft2 with a maximum depth of 18 ft. and holds approximately

400,000 gallons of manufactured salt water (Figure 2). The subjects for this study include seven beluga calves (six successful and one unsuccessful) and four Pacific white-sided dolphin calves (three successful and one unsuccessful). Specific information about each animal can be found in Appendix Table A1.

Figure 1. Whale Harbor enclosure

Located inside the Abbott Oceanarium exhibit at the Shedd Aquarium.

Figure 2. Secluded Bay enclosure

Inside the Abbott Oceanarium exhibit at the Shedd Aquarium. 19

Data Collection

Staff members, volunteers, and interns at the Shedd Aquarium collected 24-hour live observation samples for the first 30 days of each calf’s life. Staff members conducted focal-animal observations of all calves, using a combination of all-occurrence continuous sampling for nursing behaviors and instantaneous sampling every minute for calf associations and calf position (Altmann, 1974). Respiration rates were calculated using the paired protocol for recording respiration rates, where twice every hour of observation the total number of breaths for the focal animal are counted for five minutes, e.g., for the first hour, respirations are taken from 1:15-1:20 and 1:45-1:50 (Shedd Aquarium, 2016).

Staff members were effectively trained to code behaviors based on a behavioral ethogram

(Appendix Table A2). Data collection of all calves occurred between 1999 and 2016.

These 24-hour live observations were recorded onto data sheets and coded for this study

(see Appendix Figure A1).

Data Analysis

Nursing behaviors were the only behaviors recorded by all-occurrence continuous sampling. The number of all nursing bouts was recorded by recording the total daily occurrence of nursing bouts (Table A2 for behavioral ethogram). Total nursing duration for each day was also recorded and used to calculate the daily average duration per bout for each calf. Total observed for each day was corrected for birth and death times where applicable. Time spent in husbandry sessions with facility staff members was also removed from the total observation minutes per day, as this study attempted to observe the naturalistic behaviors of the subjects. Slipstream rate was calculated by dividing the

total daily number of slipstream behaviors by the total number of observation minutes per day. Maternal association rates were calculated for each day as the number of calf associations with its mother divided by the total number of observed minutes.

Conspecific association rates were calculated for each day as the number of calf associations with any animal other than its mother divided by the total number of observed minutes. Respiration rates for each day were calculated by counting the total number of respirations for five-minute observations collected every 30 minutes.

The first occurrence of two behaviors, nursing bout and conspecific association, were recorded for each subject. The average first occurrence of both behaviors was then compared between the two species and 95% confidence intervals (CIs) were calculated to determine significant variation (Table B1). The two unsuccessful calves were then compared to their respective species average to determine if they significantly differed in onset of the two behaviors.

A daily average of all coded behaviors was calculated for both species. A line graph was created for every behavior to better identify day to day changes for each species. Ninety-five percent CIs were calculated to determine whether the beluga whales

(Table B2) varied in the developmental progression from the Pacific white-sided dolphins

(Table B3), as well as whether or not the unsuccessful calves differed significantly from the healthy calves (Table B4).

Based on the results of the line graphs (Figures C1 to C7) and because most behaviors were expected to increase then plateau before decreasing, the data were split into three 10-day time periods (Time Period 1, Time Period 2, and Time Period 3) to determine if any significant changes occurred for each species throughout the 30-day

study. At this point, two unsuccessful calves B1 and D1 were excluded from any further analyses, as their behaviors were expected to be abnormal, and therefore could potentially confound the results. D1 also did not survive past Time Period 1, and therefore could not be compared throughout the remaining time periods.

Three single-case time series designs were then used to determine if significant variation occurred between the means for Time Periods 1 and 2, Time Periods 2 and 3, and Time Periods 1 and 3 for each behavior in the 9 remaining subjects. The first time period in each pair represented the baseline for the design, and the second time period in each pair represented the intervention for the design. The limits for each single-case time series design were 20 observations, with a minimum of 1 day for each time period, giving

18 possible intervention periods. Given the directional predictions of this study, a one- tailed t-test was used in each comparison to determine if the difference between the means of each time period were significant (see Tables B5 and B6). If the difference between the time period pairs was expected to decrease, data was transformed by subtracting all data points from a number larger than the original data points to create an inverse score for the individual (Dugard, File, & Todman, 2001). Effect sizes for significant differences were computed and interpreted based on the guidelines outlined by

Cohen (1988). Because only one unsuccessful calf was identified per species, significant results were reported with effect size r.

CHAPTER III – RESULTS

Observer Reliability

Because of the active schedules of all facility staff members, only one staff member or intern at a time was able to conduct the focal animal follows for some calves, making reliability testing impossible for this study. However, due to the consistency of behaviors between species and to previous findings, it is unlikely that the results of this study were greatly affected.

Nursing Patterns

Nursing Bouts

Beluga whales and Pacific white-sided dolphins were equivalent in onset of nursing. Beluga whales on average began nursing on average 17.23 hours after birth, with a range of 0.5 to 30.10 hours. Pacific white-sided dolphins on average began nursing on average 19.08 hours after birth, with a range of 6.83 to 30.67 hours (Figure 3).

Figure 3. Mean nursing onset (in hours) following birth of Pacific white-sided dolphins and beluga whales. Bars = 95% CI.

Unsuccessful beluga whale calf B1 differed in onset of nursing, falling far above the CIs for the successful beluga calves. B1 began nursing 100.57 hours following birth

(Figure 4a). Unsuccessful Pacific white-sided dolphin calf D1 began nursing at 28.33 hours after birth, which was similar to the onset of nursing of the successful Pacific white-sided dolphin calves (Figure 4b).

Figure 4. Mean nursing onset (in hours) following birth of successful and unsuccessful calves.

A: Mean nursing onset of successful and the unsuccessful beluga (B1). B: Mean nursing onset of successful and the unsuccessful

Pacific white-sided dolphin (D1). Bars = 95% CI. Beluga whale nursing bout remained consistent from Time Period 1 to Time

Period 3 (Figure 5a; mean difference = 13.29, p = 0.74). One female calf, B4, significantly decreased in average number of nursing bouts between Time Periods 1 and

3 (mean difference = 60.90, p = 0.048). Likewise, Pacific white-sided dolphins remained 25

relatively consistent in mean daily number of nursing bouts between Time Periods 1 and

3 (Figure 5b). The single-case time series design did not reveal significant variability between the Pacific white-sided dolphin calves throughout the 30-day observation period

(p = 0.26).

Figure 5. Mean daily nursing bout frequency between each 10-day time period.

A: Mean daily nursing bout frequency for beluga whale calves. B: Mean daily nursing bout frequency for Pacific white-sided dolphin calves. Bars = 95% CI.

Overall, Pacific white-sided dolphins nursed as frequently as belugas throughout the 30-day observational period, with Pacific white-sided dolphins falling below the 95% confidence intervals on days 10-14 (Figure C1).

Unsuccessful beluga calf B1 consistently exhibited fewer daily nursing bouts throughout the 30-day observational period than the successful beluga calves, falling below the 95% confidence intervals for the majority of the 30-day observation period

(Figure 6a; effect size: r = 0.60). B1 displayed much more variability after Day 6 (SD =

75.50) than the successful beluga whale calves (SD = 20.29). Unsuccessful Pacific white- sided dolphin calf D1 similarly showed fewer daily nursing bouts throughout the 30-day period than the successful calves, falling outside the 95% confidence intervals days 3 to 5

(Figure 6b; r = 0.70).

Figure 6. Developmental onset of daily mean nursing bouts of successful and unsuccessful calves.

A: Daily mean nursing bouts of successful and the unsuccessful beluga (B1). B: Daily mean nursing bouts of successful and the unsuccessful Pacific white-sided dolphin (D1). Bars = 95% CI.

Nursing Duration

Beluga whale nursing was computed throughout the observation period and was shown to decrease outside the 95% confidence intervals between Time Period 2 and Time

Period 3 (Figure 7a). Furthermore, the randomization test found that for beluga whales as a group, nursing duration decreased significantly between Time Period 1 and Time

Period 3 (mean difference = 617.68, p = 0.049). Pacific white-sided dolphins also displayed a decrease in nursing duration falling outside the 95% confidence intervals

(Figure 7b; mean difference = 292.20, p = 0.053).

Figure 7. Mean daily nursing duration between each 10-day time period.

A: Mean daily nursing duration for beluga whale calves. B: Mean daily nursing duration for Pacific white-sided dolphin calves. Bars

= 95% CI. Overall, beluga whales nursed far longer on average every day than Pacific white- sided dolphin calves following day 3 (Figure C2; effect size: r = 0.83).

The unsuccessful beluga calf B1 showed far more variability day-to-day in average nursing duration after day 6 (SD = 1432.38) than the successful beluga calves

(SD = 453.06). Notably in Time Period 1 and between days 19 and 23, B1 nursed far less than the successful calves, falling below the 95% confidence intervals. However, in Time

Period 2, B1 nursed longer than the successful calves, falling above the 95% confidence intervals. On Day 24, B1’s average nursing duration increased and was comparable to the healthy beluga calves (Figure 8a; effect size: r = 0.43). The unsuccessful Pacific white- sided dolphin D1 did not begin nursing until day 5, placing him well below the confidence intervals of the other Pacific white-sided dolphin calves between days 2 and 5

(Figure 8b; effect size: r = 0.72).

Figure 8. Developmental progression of total daily nursing duration of calves over 30 days.

A: Mean total daily nursing duration of the unsuccessful beluga calf (B1) and successful beluga whale calves. Mean total daily nursing duration of the unsuccessful Pacific white-sided dolphin calf (D1) and successful Pacific white-sided dolphin calves. Bars = 95% CI.

Nursing Average

Average nursing duration per bout for beluga whales did not vary significantly for beluga whales as a group throughout the 30-day period (Figure 9a; mean difference =

2.07, p = 0.26). However, calf B4 did significantly decrease in average nursing duration per bout between Time Period 1 and Time Period 2 (mean difference = 0.70, p = 0.046). 32

Pacific white-sided dolphins decreased throughout the 30-day period for average nursing duration per bout, falling below the 95% confidence intervals between Time Periods 2 and 3 (Figure 9b; p = 0.05).

Figure 9. Mean nursing seconds per bout between each 10-day time period.

A: Mean nursing seconds per bout for beluga whale calves. B: Mean nursing seconds per bout for Pacific white-sided dolphin calves.

Bars = 95% CI.

Overall Pacific white-sided dolphins on average displayed a lower duration per nursing bout than beluga whale calves for the majority of the 30-day observation period, falling below the 95% confidence intervals (Figure C3; effect size: r = 0.86).

Unsuccessful beluga calf B1 showed extreme variation in average duration per bout throughout the 30-day observational period, falling below the 95 % confidence intervals Days 2-5 and then above the confidence intervals at Day 12-20. After this point, average nursing duration per bout remained consistently higher for B1 than the successful beluga calves for the remainder of the observational period (Figure 10a; effect size: r =

0.20). After day 6, B1 showed more variation in average nursing duration per bout (SD =

3.23) than the successful beluga calves (SD = 1.45). Unsuccessful Pacific white-sided dolphin calf D1 fell below the 95% confidence intervals for average nursing duration per bout for the majority of the observation period (Figure 10b; effect size: r = 0.51).

Figure 10. Developmental progression of daily mean nursing seconds per bout over 30 days.

A: Developmental progression of daily mean nursing seconds per bout for unsuccessful beluga calf (B1) and successful beluga whale calves. B: Developmental progression of daily mean nursing seconds per bout of the unsuccessful Pacific white-sided dolphin calf

(D1) and successful Pacific white-sided dolphin calves. Bars = 95% CI.

Calf Position

The average time that calves remained in the slipstream position for beluga whales did not vary throughout the first two time periods followed by a decrease outside the 95% confidence intervals in Time Period 3 (Figure 11a). The randomization test revealed a significant decrease in slipstream rate between Time Period 1 and Time Period

3 for the beluga whale calves as a group (mean difference = 0.02, p = 0.04). Pacific white-sided dolphins displayed an overall decrease in slipstream rate falling outside the

95% confidence intervals from Time Period 1 to Time Period 2 before decreasing again in Time Period 3 (Figure 11b). However, the results of the single-case time series design randomization tests showed equivalent variations in slipstream behavior for all calves between each time period (p = 0.21).

Figure 11. Mean slipstream rate between each 10-day time period.

A: Mean slipstream rate of beluga whale calves between each 10-day time period. B: Mean slipstream rate of Pacific white-sided dolphin calves. Bars = 95% CI. In general, beluga whales and Pacific white-sided dolphins showed similar developmental progression of average slipstream rate, with Pacific white-sided dolphin calves displaying higher rate of slipstream position falling above the confidence intervals in Days 1-4 (Figure C4; effect size: r = 0.37).

Unsuccessful beluga calf B1 differed in rate of slipstream throughout the 30-day observational period, falling above the confidence intervals for successful beluga calves within Time Period 1 before falling below the confidence intervals at day 20. B1 showed slightly more variability in slipstream behavior after Day 6 (SD = 0.08) than the successful beluga calves (SD = 0.02). Otherwise, rate of slipstream position for B1 was comparable to the successful calves (Figure 12a; effect size: r = 0.33) Unsuccessful

Pacific white-sided dolphin calf D1 consistently fell below the confidence intervals throughout its life (Figure 12b; r = 0.47).

Figure 12. Developmental progression of daily slipstream rate over 30 days.

A: Developmental progression of daily slipstream rate of the unsuccessful beluga calf (B1) and mean daily slipstream rate of successful beluga whale calves over 30 days. Bars = 95% CI. B: Developmental progression of daily slipstream rate of the unsuccessful Pacific white-sided dolphin calf (D1) and the successful Pacific white-sided dolphin calves over 30 days. Bars = 95% CI.

Associations

Maternal Associations

Beluga whale maternal association remained equivalent throughout the 30-day observation period (Figure 13a; p = 0.69). Calf B7 reached a significant decrease in maternal association from Time Period 1 to Time Period 3 (p = 0.047). Pacific white- sided dolphins displayed an overall decrease in maternal association rate outside the 95% confidence intervals from Time Period 1 to Time Period 2 (Figure 13b; mean difference =

0.06, p = 0.65). Calf D4 did significantly decrease in maternal association rate from Time

Period 1 to Time Period 3 (mean difference = 0.07, p = 0.043).

Figure 13. Mean maternal association rate between each 10-day time period.

A: Mean maternal association rate of beluga whale calves. B: Mean maternal association rate for Pacific white-sided dolphin calves.

Bars = 95% CI.

Beluga whales and Pacific white-sided dolphins showed similar developmental progression of average maternal association rate throughout the 30-day observational period, with Pacific white-sided dolphins falling above the 95% confidence intervals days

1 to 4 (Figure C5; effect size: r = 0.86).

Unsuccessful beluga calf B1associated with his mother less than the successful beluga calves until day 15 (Figure 14a; effect size: r = 0.42). After day 15, beluga calf

B1’s maternal association rates (SD = 0.124) varied extensively compared to the successful beluga whale calves (SD = 0.028). Unsuccessful Pacific white-sided dolphin calf D1 did not differ in rates of maternal association from the successful Pacific white- sided dolphin calves until day 5, when maternal association rates dropped suddenly but not outside the 95% confidence intervals (Figure 14b; effect size: r = 0.12).

Figure 14. Developmental progression of daily rate of maternal association over 30 days.

A: Developmental progression of daily rate of maternal association of the unsuccessful beluga whale calf (B1) and mean rate of maternal association of successful beluga whale calves. B. Developmental progression of daily rate of maternal association of the unsuccessful Pacific white-sided dolphin calf (D1) and mean rate of maternal association of successful Pacific white-sided dolphin calves. Bars = 95% CI.

Conspecific Association

Beluga whales and Pacific white-sided dolphins differed in the first occurrence of conspecific associations, beluga whales associating much sooner after birth than Pacific white-sided dolphins. Beluga whales on average began associating with individuals other than their mothers approximately 2.33 days after birth, with a range of 1 to 7 days.

Pacific white-sided dolphins on average began associating with these individuals 6 days after birth, with a range of 4 to 7 days (Figure 15).

Figure 15. Mean conspecific association onset (in days) following birth of beluga whales and Pacific white-sided dolphins. Bars = 95% CI.

Unsuccessful beluga whale calf B1 did not vary in first occurrence of conspecific association from the successful beluga calves (Figure 16a). Unsuccessful Pacific white- sided dolphin calf D1 began associating with conspecifics on day 5, which did not vary from the average first occurrence of conspecific association of the successful calves

(Figure 16b).

Figure 16. Mean conspecific association onset (in days) following birth of successful and the unsuccessful calves.

A: Mean conspecific association onset (in days) following birth of successful beluga whale calves and the unsuccessful beluga whale calf (B1). B: Mean conspecific association onset (in days) following birth of successful and the unsuccessful Pacific white-sided dolphin calf (D1). Bars = 95% CI. Beluga whale conspecific association increased outside the 95% confidence intervals between Time Period 1 and Time Period 3 (Figure 17a). No significant variation was detected for beluga calves as a group between Time Period 1 and Time Period 3 (p = 46

0.94). Likewise, Pacific white-sided dolphins also displayed an overall increase in conspecific association rate, increasing outside the 95% confidence interval between

Time Period 1 and Time Period 2 (Figure 17b; p = 0.31).

Figure 17. Mean conspecific association rate between each 10-day time period.

A: Mean conspecific association rate for beluga whale calves. B: Mean conspecific association rate for Pacific white-sided dolphin calves. Bars = 95% CI.

Beluga whales associated with conspecifics more than the Pacific white-sided dolphin calves throughout the 30-day observation period (Figure C6; effect size: r =

0.14).

Unsuccessful beluga calf B1 showed similar rates of conspecific association to the successful beluga calves (Figure 18a). Likewise, unsuccessful Pacific white-sided dolphin calf D1 did not differ in rates of conspecific association from the successful

Pacific white-sided dolphin calves (Figure 18b).

Figure 18. Developmental progression of daily rate of conspecific association over 30 days.

A: Developmental progression of daily rate of conspecific association of the unsuccessful beluga whale calf (B1) and mean daily rate of conspecific association of successful beluga whale calves. B: Developmental progression of daily rate of conspecific association of the unsuccessful Pacific white-sided dolphin calf (D1) and mean daily rate of conspecific association of successful Pacific white-sided dolphin calves. Bars = 95% CI.

Respiration

Beluga whale respiration rates decreased outside the 95% confidence interval from Time Period 2 to Time Period 3. (Figure 19a). Variation throughout the 30-day observation period for beluga calves as a group remained relatively equal (p = 0.42).

Pacific white-sided dolphin respiration rate increased significantly throughout the 30-day observation period (Figure 19b; p = 0.049). Variation between individual calves remained relatively consistent.

Figure 19. Mean respiration rate between each 10-day time period.

A: Mean respiration rate for beluga whale calves. B: Mean respiration rate for Pacific white-sided dolphin calves. Bars = 95% CI. Beluga whales and Pacific white-sided dolphins overall showed very similar developmental trends for average respiration rate until day 22, when the Pacific white- sided dolphins displayed higher respiration rates than the beluga whale calves (Figure C7; effect size: r = 0.61).

Unsuccessful beluga calf B1 displayed lower respiration rates from the successful beluga calves falling below the 95% confidence intervals until day 24, when B1’s respiration rates increased to comparable levels. However, beginning on day 28 B1’s respiration rates increased above the 95% confidence intervals and were higher than the successful beluga whale calves (Figure 20a; effect size: r = 0.68). Unsuccessful Pacific white-sided dolphin calf D1 exhibited higher respiration rates than the successful dolphin calves (Figure 20b; effect size: r = 0.71).

Figure 20. Developmental progression of mean daily respiration rate over 30 days.

A: Developmental progression of mean daily respiration rate of the unsuccessful beluga calf (B1) and successful beluga whale calves.

B: Developmental progression of mean daily respiration rate of the unsuccessful Pacific white-sided dolphin calf (D1) and successful

Pacific white-sided dolphin calves. Bars = 95% CI.

CHAPTER IV – DISCUSSION

The aim of the present study was to identify and compare general developmental trajectories of several behaviors for the first 30 days of life in beluga whales and Pacific white-sided dolphins, two relatively understudied cetacean species. These norms were then compared to the onset and general developmental trajectories of two calves that did not survive the infancy period to determine if the early identification of specific behaviors may ultimately contribute to improving the success of future births in professional care facilities.

Developmental Norms

Hypothesis 1 predicted no significant variations between the onset and the developmental progression between the beluga whale and Pacific white-sided dolphin calves. As predicted for the study, Pacific white-sided dolphins appeared to behaviorally develop similarly to beluga whales and other cetacean species, making them a valid candidate for future comparative studies. Both beluga whales and Pacific white-sided dolphins demonstrated similar early onsets of nursing behaviors and sudden increases in nursing frequency and duration within the first 4 days of life. Nursing behaviors for both species ultimately stabilized and became more consistent throughout the remainder of the

30-day observational period, supporting previous literature on both bottlenose dolphins and beluga whales (Eastcott & Dickinson, 1987; Krasnova et al., 2009; Thomas & Taber,

1984). All nursing behaviors slightly decreased from onset to the end of the first month of life. Most likely, cetacean calves are faced with a nursing learning buffer during the first few days of life, as calves must regulate their buoyancy and coordinate their movements to

dive long enough to adequately feed from the mother’s mammary glands. Over time, calf nursing behavior becomes more efficient, thus decreasing both frequency and duration of nursing bouts. Although young beluga whale calves overall on a daily basis nursed significantly longer and more frequently than Pacific white-sided dolphins, the average duration of the nursing bouts in the current study replicated previous findings in the literature and supported the hypothesis (Krasnova et al., 2006).

Beluga whale calves and Pacific white-sided dolphin calves differed in rates of swimming in the echelon or infant position only in the first 10-day time period. As Pacific white-sided dolphins are more agile versus other cetaceans, it is likely that the calves of this species would benefit most from the extra hydrodynamic benefit of the position to be able to physically keep up with their mothers during this crucial period of behavioral and social learning. Beluga whale calves, however, may not need the hydrodynamic boost to maintain contact with their much slower conspecifics.

Maternal association rates did not vary between the two species or throughout the

30-day observational period, accounting for approximately 60-90% of all calf observation periods, as is expected for infant cetaceans (Hill, 2009). Calves of both species spent far more time interacting with their own mothers than all other individuals in the population combined (0-15% of all calf observation periods). Notably, the youngest calves for each species, B7 and D4, were the only individuals to significantly decrease in maternal association rates throughout the first 30 days of life. Cetacean mothers have been documented to alter their maternal styles as their calves age (Hill, H. M., Greer, T., Solangi,

M., & Kuczaj, S. A., 2007) and may also alter their maternal styles with more experience.

Future studies should focus on how mother-calf interactions change after multiple births.

The two species differed greatly in first occurrence and average rate of conspecific interactions, although both species in this population began interacting with conspecifics earlier than shown in the literature (Eastcott & Dickinson, 1987; Krasnova et al., 2009;

Krasnova et al. 2014). The variation between the two species might be an artifact of the calves’ social group. At the time D2 was born, no other calves were present in the population; however, for a cetacean calf other calves in its maternal group are the ideal partners for early social interactions (Hill et al., 2016). D3 and D4 were also limited in potential social partners, with D3 only having 1 potential calf partner and D4 only having

2 potential calf partners. The facility environment provides a much safer environment for calves to begin socially interacting with individuals other than their mothers far earlier than could be risked in a wild population. Further investigations need to be conducted to also determine if these findings are consistent for Pacific white-sided dolphins, as well.

The variation in rates of maternal association and conspecific association between the individual calves could also easily be explained by maternal style. It would be unreasonable to assume that all cetacean mothers allow their calves the same amount of independence at the same point of development, and so the degree to which the mother allows the calf to wander from her may be a factor affecting calf social behavior (Hill et al., 2007). Future studies could potentially focus on identifying maternal styles and how they affect calf social behaviors.

Although, beluga whales and Pacific white-sided dolphins maintained similar average respiration rates throughout the observation period, the developmental trajectory of average respiration rate differed. Beluga whale calf respiration rate decreased throughout the observation period, whereas Pacific white-sided dolphin calf respiration rate steadily increased reaching significant levels on day 22. As previously stated, Pacific white-sided dolphins are a faster and more agile species of cetaceans. As Pacific white- sided dolphins physically develop and master the task of swimming, it is reasonable to expect that they begin to swim at a faster pace than beluga whales immediately after birth.

Higher respiration rates are an indicator of higher metabolic activity, and swimming faster would necessitate more energy. Comparatively, beluga whales travel slower. It is more likely that as they physically mature and develop past the infancy stage, they do not need to surface as frequently, resulting in progressively lower average respiration rates. Future research should focus on the behavioral swim patterns of Pacific white-sided dolphin calves and specifically how those swim patterns change as the calf matures physically.

Unsuccessful Calves

Hypothesis 2 predicted significant differences between the onset and developmental progression of the successful and unsuccessful calves of both species.

Specifically, unsuccessful calves are predicted to have lower frequency and duration of nursing behaviors, higher percentages of time spent in the infant position, lower rates of associations with other animals, and higher respiration rates when compared to successful calves.

As expected, some differences were seen in the behaviors of the successful versus unsuccessful calves and the norms for development previously established in the literature.

No variation in conspecific association onset or rate were found, partially refuting the predictions of this study. The findings of this study could reflect individual differences, as only one unsuccessful calf per species was identified for comparison, limiting the statistical power to detect potential differences.

Despite these limitations, some reliable differences were identified between the unsuccessful calves and the successful calves of their respective species. For unsuccessful beluga calf B1, nursing duration varied extensively, consistently fluctuating outside the expected variability of beluga calf nursing duration behavior. B1 also nursed less frequently and for shorter durations than the successful beluga calves, though only showing a reliable difference at the end of the first 10-day time period. Most importantly, B1 significantly began nursing much later after birth than any of the successful beluga calves.

B1 appeared to struggle to begin nursing and to stabilize nursing behavior after onset, suggesting difficulty at mastering the task of nursing at a developmentally appropriate time.

Calf B1 did vary more in maternal association rates than the successful beluga whale calves. Unexpectedly, for the first half of the observation period B1 associated with its mother less than the successful beluga whale calves. It is possible that abnormal maternal association rates, whether significantly more or significantly less, may be an early behavioral indicator of an at-risk calf. Future research in the progression of maternal association behavior in unsuccessful calves is warranted for any definitive results.

As was predicted, D1 also nursed less frequently and for shorter durations relative to the successful Pacific white-sided dolphin calves. Unexpectedly, no significant differences were detected in rates of maternal association for unsuccessful Pacific white- sided dolphin calf D1.

As expected, both unsuccessful calves displayed higher respiration rates the last few days of their lives when compared to the successful calves of their respective species.

These results not only support one of the hypotheses of the current study, but also replicate previous findings in the literature (George & Noonan, 2014).

Additional limitations of the present study include the small number of subjects, as is typical of most animal behavioral studies conducted in managed care facilities. The number of subjects was limited to the calves that were born at the Shedd Aquarium between

1999 and 2016 due to constraints on availability of subjects and to attempt to reduce confounding variables in facility environments that could affect calf behavior. To limit potential threats to internal validity, randomization tests, specifically a single-case time series design, were chosen to analyze the data. Future investigations could attempt to recruit larger populations from several different facilities to obtain an adequate number of subjects for comparison.

Due to lack of access to other populations, another limiting component of this study was the inequity of beluga whale calves and Pacific white-sided dolphin calves which could not be controlled by the facility or the researcher. However, the results of this study showed vast similarities between the behavioral progression of the two species despite the unequal subject groupings making it unlikely that individual differences of the Pacific white-sided dolphin calves confounded the overall results.

Likewise, only one unsuccessful calf was identified per species group, with only 7 days of data for one of these calves. These calves were excluded from the overall analysis of the study to prevent their state of health from confounding the results of the analysis.

However, the results of this study that identified differences between the unsuccessful calves and the successful calves are only preliminary, and extensive further research is still needed before any conclusive evidence can be used to identify and predict later viability.

The randomization analysis itself was limited. The design may not have been powerful enough to detect all of the variability in this study, as 18 possible arrangements were necessary to detect significant differences in the current dataset. The subjects could not be randomly assigned to groups, and the limits for the baseline and withdrawal phases of the single-case time series design were chosen based on results from the dataset, rather than at random which could potentially increase the chance of issues with internal validity.

Overall though, the single-case time series design was the most conservative and most appropriate test to identify potential significant differences in a dataset with such a limited number of subjects (Kratochwill, 2013; Razal, Bryant, & Miller, 2017). Future research could easily be able to compensate for this limitation by extending the observational period and recruiting a larger number of subjects.

The findings of the present study have extensive practical welfare and animal management implications. Average developmental progression for the first month of life and onset of several easily identifiable behaviors in two cetacean species has been exhaustively and thoroughly described, providing previously unprecedented detail into the expected daily changes of these behaviors. Future researchers and facility staff can utilize these results to identify normal patterns of behavior in the animals housed under

their care. The findings of this study also suggest that with further research, potential differences could be identified as early as within the first 30 days of life for cetacean calves to determine if intervention is necessary to increase a calf’s chance of survival.

Conclusions

Although the field of animal development has grown extensively, several questions remain unanswered, especially those pertaining to less available species like marine mammal species. The present study is an essential preliminary investigation into the normal and abnormal developmental progression of understudied cetacean species both in managed care facilities and in the wild. This study provides unprecedented detailed information about the development of Pacific white-sided dolphins, a relatively unstudied species in the field of strictly behavioral studies, in the first month of life.

Future research using larger sample sizes across different facility environments is necessary to support the current findings of this study. The results of this study are also the first to demonstrate potential identifiable differences in the behavioral onset and progression of unsuccessful calves as early as the first month of life, although extensive further research on the topic is vital to developing any conclusive and consistent results.

The findings of this and future research can be used to hopefully increase calf survival rates in managed care facilities by providing a baseline of expected behavioral progression and normal variability of development to indicate when intervention may be necessary to increase a calf’s chance of survival.

APPENDIX A – Subjects and Ethogram

Table A1. Demographic Information of Subject Animals

Birth Date Dam Gender Belugas B1* 7/23/99 BM1 Male B2 8/3/99 BM4 Female B3 7/15/00 BM3 Male B4 7/17/06 BM1 Female B5 8/16/07 BM3 Male B6 12/14/09 BM1 Male B7 8/27/12 BM3 Female Pacific White-sided Dolphins D1* 6/3/11 DM1 Female D2 5/28/12 DM2 Male D3 6/1/15 DM2 Male D4 4/18/16 DM3 Male Note. *Indicates an animal that was unsuccessful and did not live past the 30-day infancy period.

Table A2. Operational Definitions for Coded Behaviors

Behavior Definition Nursing Bout A nursing bout begins once a calf successfully latches onto the mother’s mammary gland and ends once a calf removes its mouth Calf Respiration Respiration is considered to have occurred when the calf breaks the surface of the water and quickly submerges again. Slipstream Slipstreaming occurs when the calf is completely submerged near the mother and swimming parallel to her. The calf’s head should not be in front of the mother’s pectoral fin, and the calf’s fluke should not be past the mother’s fluke. Association An association occurs when the calf is within 1 m of another

animal. The ID of the other animal should be noted.

Note.. Adapted from Shedd Aquarium (2016).

Cetacean Calf Watch Behavioral Ethogram

Note. Reprinted from Shedd Aquarium’s Cetacean Calf Watch Manual (Shedd Aquarium, 2016). Reprinted with permission.

APPENDIX B – Results: Tables

Table B1. Descriptive Statistics for First Occurrence of Behaviors

95% Confidence

Behavior N Mean SD SE Interval for Mean

Lower Upper

Beluga Nursing 6 17.23 10.64 4.345 8.72 25.74 (hrs)

Dolphin Nursing 3 19.08 11.931 6.889 5.58 32.58 (hrs)

Beluga Association 6 2.333 2.338 0.954 0.463 4.203 (days)

Dolphin Association 3 6.00 1.732 1.000 4.04 7.96 (days)

Note. First occurrence of nursing was recorded by hours following birth. First occurrence of conspecific association was recorded by days following birth.

Table B2. Descriptive Statistics of Calf Behaviors for Successful Beluga Whales Over 30

Days

95% Confidence

Behavior N Mean SD SE Interval for Mean

Lower Upper

Nursing Bout 30 203.800 37.631 6.870 190.3 217.3

Nursing Duration (s) 30 2000.111 548.357 100.116 1804.1 2196.1

Nursing Average* 30 10.155 2.259 0.412 9.347 10.963

Slipstream Rate 30 0.083 0.020 0.003 0.075 0.090

Maternal Association 30 0.682 0.036 0.006 0.669 0.694 Rate

Conspecific 30 0.541 0.036 0.006 0.528 0.554 Association Rate

Respiration Rate 30 3.313 0.293 0.0536 3.208 3.418

Note. *Nursing average represents the average duration (s) per bout for each day.

Table B3. Descriptive Statistics of Calf Behaviors for Successful Pacific White-sided

Dolphins Over 30 Days

95% Confidence

Behavior N Mean SD SE Interval for Mean

Lower Upper

Nursing Bout 30 142.655 39.654 7.239 128.45 156.85

Nursing Duration (s) 30 647.233 240.692 43.944 561.133 733.33

Nursing Average* 30 4.555 0.803 0.146 4.268 4.842

Slipstream Rate 30 0.122 0.066 0.012 0.0984 0.146

Maternal Association 30 0.833 0.049 0.008 0.816 0.85 Rate

Conspecific 30 0.001 0.001 0.0002 0.0006 0.001 Association Rate

Respiration Rate 30 4.296 0.852 0.155 3.991 4.601

Note. *Nursing average represents the average duration (s) per bout for each day.

Table B4. Descriptive Statistics of Calf Behaviors for Unsuccessful Calves

95% Confidence

Behavior N Mean SD SE Interval for Mean

Lower Upper

Nursing Bout 30 106.53 82.742 15.11 76.93 136.13

Nursing Duration (s) 30 1597.83 1480.31 270.26 1067.83 2127.8

Nursing Average* 30 11.933 5.638 1.03 9.91 13.953

Slipstream Rate 30 0.134 0.103 0.019 0.097 0.171

Maternal Association 30 0.588 0.140 0.025 0.538 0.638 Rate

Conspecific 30 0.003 0.007 0.001 0.0005 0.005 Association Rate

Respiration Rate 30 2.610 0.450 0.082 2.449 2.771

Nursing Bout 7 31.714 69.715 26.349 69.6 69.9

Nursing Duration (s) 7 121.142 271.142 102.482 -19.886 83.314

Nursing Average* 7 2.428 2.439 0.922 0.618 4.238

Slipstream Rate 7 0.063 0.041 0.015 0.032 0.093

Maternal Association 7 0.867 0.187 0.070 0.728 1.006 Rate

Table B4 Continued

Conspecific 7 0.0001 0.0002 0.0001 -0.00004 0.0002 Association Rate

Respiration Rate 7 6.067 0.915 0.345 5.389 6.745

Note. *Nursing average represents the average duration (s) per bout for each day.

Table B5. Mean Difference Values for Behaviors in Each Time Period for Individual

Beluga Calves and Group

Behaviors B2 B3 B4 B5 B6 B7 Belugas Nursing Bout 2.00 21.50 5.20 59.70 142.80 14.30 21.02 0.10 39.20 66.10 82.00 8.40 31.40 7.73 0.29 17.70 60.90* 22.30 151.20 17.10 13.29 Nursing Duration 225.20 45.30 314.10 1230.70 343.10 626.50 334.68 (s) 449.00 499.30 486.00 444.30 346.30 361.70 283 674.20 454.00 800.10 786.40 3.20 988.20 617.68*

Average Nursing 2.40 0.60 0.70* 0.30 5.70 2.40 1.47 Duration (s) per 1.80 1.30 3.20 1.50 1.40 0.80 0.60 Bout 0.60 0.70 2.50 4.50 7.10 3.20 2.07 Slipstream Rate 0.01 0.02 0.004 0.004 0.001 0.01 0.0005 0.07 0.006 0.02 0.02 0.02 0.005 0.02 0.08 0.009 0.02 0.02 0.01 0.01 0.02* Maternal 0.02 0.02 0.07 0.03 0.12 0.67 0.01 Association Rate 0.05 0.06 0.03 0.07 0.04 0.61 0.02 0.07 0.08 0.04 0.10 0.17 0.06* 0.004 Conspecific 0.00007 0.002 0.0007 0.06 0.02 0.13 0.02 Association Rate 0.00 0.002 0.13 0.04 0.005 0.009 0.03 0.00007 0.002 0.13 0.09 0.02 0.14* 0.05 Respiration Rate 0.71 0.72 1.04 0.15 0.1 0.48 0.05 0.11 0.33 0.33 0.41 0.35 0.45 0.22 0.60 1.05 0.71 0.26 0.25 0.04 0.27

Note. Data for each calf is presented in order by each time period comparison, i.e. Time Period 1 vs. Time Period 2, Time Period 2 vs.

Time Period 3, Time Period 1 vs. Time Period 3.*Indicates p < 0.05, one-tailed

Table B6. Mean Difference Values for Behaviors in Each Time Period for Individual

Pacific White-Sided Dolphin Calves and Group

Behaviors D2 D3 D4 Pacific White-Sided Dolphins Nursing Bout 13.30 40.70 104.50 16.83 19.00 28.40 23.10 4.57 5.70 69.10 127.60 21.40 Nursing Duration 145.00 154.60 588.00 192.80 (s) 154.10 31.70 112.40 99.40 299.10 122.90 700.40 292.20* Average Nursing 0.30 1.00 0.30 0.53 Duration (s) per 0.70 1.40 0.20 0.77 Bout 0.10 2.40 0.50 1.30* Slipstream Rate 0.12 0.12 0.06 0.10 0.06 0.01 0.03 0.03 0.18 0.13 0.08 0.13

Maternal 0.06 0.05 0.05 0.06 Association Rate 0.06 0.02 0.02 0.02 0.12 0.03 0.07* 0.07

Conspecific 0.001 0.001 0.00 0.00 Association Rate 0.002 0.0002 0.0004 0.02 0.003 0.001 0.0004 0.002

Respiration Rate 0.57 1.27 0.02 0.62 0.41 0.01 0.85 0.43 0.98 1.29 0.87 1.05

Note. Data for each calf is presented in order by each time period comparison, i.e. Time Period 1 vs. Time Period 2, Time Period 2 vs.

Time Period 3, Time Period 1 vs. Time Period 3. *Indicates p < 0.05, one-tailed

APPENDIX C – Results: Figures

Figure C1. Developmental progression of mean daily nursing frequency for beluga

whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C2. Developmental progression of mean daily nursing duration for beluga whales

and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C3. Developmental progression of daily mean duration per nursing bout for

beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C4. Developmental progression of mean daily slipstream rate for beluga whales

and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C5. Developmental progression of mean daily maternal association rate for beluga

whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C6. Developmental progression of mean daily rates of conspecific association for

beluga whales and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

Figure C7. Developmental progression of mean daily respiration rate for beluga whales

and Pacific white-sided dolphins over 30 days. Bars = 95% CI.

APPENDIX D – Research Approval

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