VOCAL BEHAVIOR OF CAPTIVE ATLANTIC BOTTLENOSE

DOLPHINS IN A SWIM PROGRAM

by

Deborah D. Boege

A Thesis Submitted to the Faculty of

The College of Science

in Partial Fulfillment of the Requirements for the Degree of

Master of Science

Florida Atlantic University

Boca Raton, Florida

April 1994 For My Father, Harald, In Loving Memory VOCAL BEHAVIOR OF CAPTIVE A1LANTIC BOITLENOSE

DOLPHINS IN A SWIM PROORAM

by

Deborah D. Boege

This thesis was prepared under the direction of the candidate's thesis advisor, Dr. Godfrey R. Bourne, Department of Biological Sciences and has been approved by the members of her supervisory committee. It was submitted to the faculty of the College of Science and was accepted in partial fulfillment of the requirements for the degree of Master of Science.

SUPERVISORY COMMITIEE:

Chairman

Dr. Daniel F. Austin ~u_ ~~ Dr. Michael Salmon

Date

ii ACKNOWLEDGEMENTS

I thank Drs. Daniel F. Austin, Godfrey R. Bourne, and Michael Salmon for

providing helpful comments about experimental design, and on early drafts of the thesis. I

am particularly grateful to G. R. Bourne for his continuous support and invaluable advice

throughout this project. The generous permission to conduct this research was granted by

Lloyd and Rick Borguss of Dolphins Plus to whom I am greatly indebted. I appreciate the staff of Dolphins Plus, particularly Wendy Kellam, for their cooperation and hospitality. I also thank Scott Spitz for all his help, and Annika Woehr for fieldwork assistance. Special gratitude is owed to Judy Hicklin and Sue Schmidt for their statistical advice and assistance when Dr. Bourne was out of the country. Finally, I especially thank Ingeburg Boege and

Michael Schmidt for their continuous encouragement and enthusiastic support. A Marine

Biology Research Grant through the Department of Biological Sciences, Florida Atlantic

University, equipment loans from G. R. Bourne, Ed Gerstein, and M. Salmon, and contributions from Joe Scandroli, Judy Fuchs, and the Spitz family made it possible for me to conduct this research.

ill ABSTRACT

Author: Deborah D. Boege

Title: Vocal Behavior of Captive

Atlantic Bottlenose Dolphins

in a Swim Program

Institution: Florida Atlantic University

Thesis Advisor: Dr. Godfrey R. Bourne

Degree: Master of Science

Year: 1994

Dolphins emit distinct vocalizations in the contexts of stressful situations, such as when captured in nets. It has been assumed among animal rights groups that the presence of human swimmers causes stress in captive Atlantic bottlenose dolphins (Tursiops truncatus). Stress may be expressed in dolphin vocalizations and the associated visual behaviors before, during, and after swim sessions with humans. Thus, these behaviors were recorded to elucidate quantitative vocal patterns suggestive of conspecific stress.

Significant differences among vocalization types within sample sessions were found only for whistles between During II and After sessions. Other comparisons indicated no significant differences for vocalization production frequencies between the presence or absence of human swimmers. Additionally, correlations found among the seven vocalization types and all five sample sessions indicated only that one variable, i.e. the presence or absence of human swimmers, was being measured in several different ways

(by the different vocalization type production frequencies). Thus, conspecific stress, if indeed it can be measured by vocalization production frequency, does not appear to occur more often in the presence of human swimmers.

IV TABLE OF CONTENTS

ACKNOWLEDGEMENTS ...... iii

ABSTRACT ...... iv

LIST OF TABLES ...... vi

LIST OF FIGURES ...... vii

INTRODUCTION ...... 1

MATERIALS AND METHODS ...... 3

Study Site and Animals ...... 3

Recording Procedures ...... 3

Vocalization Categories ...... 4

Behavioral Categories ...... 5

Statistical Analyses ...... 6

RESULTS ...... ?

Vocalizations ...... 7

Vocal Behavior...... 7

DISCUSSION ...... 15

Sample Sessions and Vocal Behavior ...... 15

Conclusions ...... 16

LITERATURE CITED ...... 18

v LIST OFTABLES

1. Vocalization parameters used to distinguish between

vocalization types (N = 70) ...... 9

2. Mean numbers and standard errors of vocalization

totals by session (N = 276) ...... 11

3. Results of analysis of variance for seven vocalization

types among five sample sessions employing square root

transformed data [DF = 4 (session types), 271 (sessions);

N = 276 (total number of sessions sampled)] ...... 12

4. Matrix of significant differences (P values) among pairwise

sample session comparisons within each vocalization type

at Dolphins Plus estimated using a one-way ANOV A model,

after square root transformations, followed with pairwise

post-hoc Fisher's Protected LSD tests (Nscss ion s = 276) ...... 13

VI LIST OF FIGURES

1. Audiospectrograms and waveforms of dolphin vocalization types ...... 8

2 . Frequencies of seven audible behavior types emitted by dolphins

during the five sample sessions ...... lO

Vll INTRODUCTION

Many cetaceans, including Atlantic bottlenose dolphins (Tursiops truncatus

Montagu), exhibit highly developed auditory and sound producing systems, and are among the most vocal of the nonhuman mammals (Herman and Tavolga, 1980). Little is known about the social contexts in which captive and free-living dolphins vocalize (Herman and

Tavolga, 1980; Herman, 1991; Tyack, 1991). However, Caldwell and Caldwell (1965) contend that bottlenose dolphins might emit more, louder, and faster whistles when stressed. Some sounds produced by dolphins are coordinated with a visible display. For example, the jaw clap is a sound produced by the snapping together of the jaws, and is usually emitted in conjunction with an agonistic, open mouth display (Wood 1954).

Moreover, according to Caldwell et a!. (1962), Pryor (1973), Norris and Dohl (1980),

Ralston and Herman (1989), and Pryor and Schallenberger (1991) certain visual displays, such as tail slaps, jaw claps, and tail swishes, as well as high-energy vocalizations, including repetitive whistling bouts, and rapid burst-pulse sounds (referred to as "barks" in this study) appear to be indications of agitation and stress among both captive and wild dolphins.

There is concern among animal rights groups that stress may be induced in captive dolphins by the presence of human swimmers that are without escape routes (DeGeorge,

1989; Linden, 1989). Only two studies (Ostman, 1991; Spitz, 1993) have quantitatively analyzed the social behavior of captive dolphins in association with humans. To study the impact human presence has upon captive dolphins, the frequencies of vocalizations, their social contexts, and the associated visual behaviors in which these vocalizations are produced must be examined. An evaluation of auditory emissions is of vital importance in the study of dolphin

social behavior. Dolphins have remarkable auditory information processing skills and

apparently communicate most often by auditory means (Herman, 1991). Many dolphins

are able to detect signals above 100 kHz, thereby suggesting a very specialized hearing

apparatus (Schevill and Lawrence, 1952; Popper, 1980; Norris, 1991). The reliance on the

auditory rather than the visual system is not surprising, given the short visibility of light in

the murky water where some dolphins live. In contrast, nonhuman primates tend to be

more visually oriented (D 'Amato, 1973; D 'Amato and Colombo, 1986).

Presently there are four Swim-with-the-Dolphins (SWTD) programs in the United

States. Each SWTD program is authorized by the Marine Mammal Commission on a

"probationary basis" due to the assumption that "undesirable modifications of the dolphin's

behavior," including stress and agitation, may result as a consequence of swimming with

humans. An examination of vocalizations, with special reference to agonistic emissions, the behavioral contexts in which vocalizations are produced, and the presence or absence of human swimmers may aid in determining whether swimming with humans causes adverse effects on captive dolphins.

In this study I compare dolphin vocalizations and their frequency of occurrence between sample sessions when humans are present and absent. I do so to elucidate the effect human swimmers have on vocal and visual behavior. The following hypothesis was tested: there is an increase in the number of agonistic emissions produced by dolphins during sessions when human swimmers are present.

2 MATERIALS AND METHODS

Study Site and Animals.- Ten Atlantic bottlenose dolphins at Dolphins Plus in Key

Largo, Florida were held in two pens (27 m x 40 m). Pen depth ranged from 4 to 5 m.

The pens lie in two basins on the north and south sides of a canal open on both ends to the

Atlantic Ocean, allowing exposure to natural tidal patterns. A portion of each pen is

sectioned off as an "escape" area where human swimmers are excluded.

Five adult females were maintained in the north pen; four females and one male

were housed in the south pen. At the time of the study, seven of the nine females were

between 8 and 10 yr old, while the two remaining females and the two males were between

15 and 16 yr. All animals were captured in the Gulf of Mexico between Tampa Bay and

Fort Meyers, Florida (L. Borguss, pers. comm.). Individuals were identified by

coloration, rostral scars, and by general shape and notches of their flukes (Taylor and

Saayman, 1973; Wtirsig, 1979). Such marks appear to change little over many years, and

thus serve as useful individual identification markers (Scott et al., 1990). For the last 6

years all of the dolphins have been actively swimming with humans (L. Borguss, pers.

comm.).

Four swim sessions with a duration of 0.5 h each are held daily in both pens:

two in the morning and two in the afternoon. Each set of two is separated by a 30 min

break. A 2 h break separates the morning and afternoon sets, when the animals are fed (L.

Borguss, pers. comm.).

Recording Procedures.- Observation sessions (N = 276) were recorded between 6

June, 1992 through 11 April, 1993. Underwater vocalizations and corresponding behavior

were observed during 28 min time blocks as follows: (1) for 14 min before the beginning

3 of a swim session ("Before"), and extending 14 min into the session ("During I"); (2) beginning 14 min before the end of a swim session ("During II") and extending 14 min after its completion ("After"). Control sessions were 14 min time blocks when swimmers and other humans were absent. These sessions were separated from a swim session by at least 45 min. Fifty-three Before, 53 During I, 73 During II, 73 After, and 24 Control observation sessions were recorded. Forty-four percent of these sampling observations were made during the morning, with the other 56 percent recorded in the afternoon.

Vocalizations were detected using an Atlantic Research Corporation hydrophone

(LC-57; ± 2 db from 20 Hz to 20 kHz). These signals were simultaneously recorded on both channels of a cassette recorder (Marantz Superscope CD-330; ± 2 db from 35Hz to

16kHz). I monitored all recordings and noted when sounds occurred, the vocalization type (described below), dolphin nearest the hydrophone, and associated visual behavior.

Sessions were also recorded on video from a platform about 7 m above the water surface to document and clarify behavioral contexts, and to identify the dolphin closest to the hydrophone by matching the videotape to audiotape (Tyack, 1991 ). Location varied depending upon the position of the sun. I used polarizing glasses to clearly see underwater displays.

Vocalizations and their corresponding behavioral contexts were aurally and visually inspected during tape playback for comparison to field notes. Spectrograms of taped vocalizations were made using a Macintosh IIci using appropriate software (MacRecorder

SoundEdit Pro, Canary 1.1).

Vocalization Categories.- Vocalizations and other audible emissions produced by the dolphins were placed into the following behaviorally defined categories as follows: (1) whistles-frequency-modulated, narrow-band sounds which may identify the individual

(Schevill and Lawrence, 1956; Caldwell and Caldwell, 1965); (2) jaw claps-short, broad­ band emissions often emitted in conjunction with gapping, head nodding, and jaw shaking

4 (McBride, 1940; Lawrence and Schevill, 1954; Wood, 1954); (3) tail slaps-sounds

produced when slapping the peduncle and tail flukes against the water surface (Pryor,

1973); (4) tail swishes-sounds caused by a sudden movement of the flukes through the

water, creating swirls of bubbles (Pryor, 1973; T. Hankins, pers. comm.); (5)

grunts-long, low frequency, burst-pulse sounds (D. D. Boege, pers. observ.); (6)

barks-short, burst-pulse sounds (also referred to as squawks and yelps; Caldwell and

Caldwell, 1967); and (7) other-emissions heard rarely and not in any of the above

categories. The most common was a "giggle" (D. D. Boege, pers. observ.). The "giggle"

was produced when the dolphins were excited, swimming rapidly, and leaping

occasionally. This sound was heard most often when trainers approached with food

buckets.

Vocalizations were also quantitatively defined by inspection of spectrogram

contours, which varied in dominant frequency, frequency pattern, and duration (Dreher,

1961; Tyack, 1991). I randomly selected ten vocalizations of each type from randomly

selected audio tapes and constructed a vocalization parameters table (Table 1). This table

was utilized in defining the type of individual calls by comparing spectrogram

characteristics. Additionally, categorization depended on aural inspection of the sounds

during tape playback accompanied by examination of notes and video taken during

sessiOns.

Behavioral Categories.- Dolphin behavior when humans were present and absent

was categorized as follows: (1) strong agonistic behavior: jaw clapping, tail slapping, tail

swatting, hitting or ramming, biting, and ag&rressive teeth raking (McBride, 1940; McBride

and Hebb, 1948; Lawrence and Schevill, 1954; Tavolga and Essapian, 1957; Essapian,

1963; Wtirsig, 1979); (2) mild agonistic behavior: tail swishing, tail flicking, flipper

slapping, and open mouth approach/chase (Wtirsig, 1979; Shane, 1990; T. Hankins, pers. comm.); (3) sexual behavior: attempted copulation, successful copulation, ventral rubbing,

5 and erection (McBride and Kritzler, 1951; Tavolga and Essapian, 1957; Saayman et al. ,

1973; T. Hankins, pers. comm.); and (4) non-aggressive displays: side-by-side swimming and "play" (Taylor and Saayman, 1973; Wiirsig, 1979; Connor and Smolker, 1985; T.

Hankins, pers. comm.).

Statistical Analyses.- For each of the five sample periods total counts of the seven vocalization categories were recorded (Table 2). Data were square root transformed to permit analysis by parametric statistics (Sokal and Rohlf, 1981 ). A one-way ANOVA with pairwise post-hoc Fisher's Protected LSD tests was used to test the hypothesis of no difference in number of vocalizations produced between "Before" and "During I" sessions, between "During II" and "After" sessions, and among "Control" and the other four sessions. Comparisons were made only between close temporal sessions, eliminating as much as possible factors perhaps due to time/activity pattern changes. Therefore, in these two sets of comparisons, changes in vocalization production frequencies would only be attributable to the presence or absence of people in the water. Comparisons were also made among the Control sessions and all four other sessions to examine if changes in vocalization production frequencies varied in complete absence of people (swimmers and staff). These variations, however, would not be attributable solely to the absence of humans because changes in time/activity patterns are known to occur in vocal and visual behaviors of both captive and wild dolphins (Kellogg, 1961; Lilly, 1962; Powell, 1966;

Saayman et a!., 1973; Herman and Tavolga, 1980).

Finally, I used a Wilk's Lambda MANOVA test to determine whether there were significant correlations between vocalization types and session samples. The P ~ 0.05 significance level was used in all statistical tests.

6 RESULTS

Vocalizations.- Examples of the seven vocalizations and their distinguishing

parameters are presented as audiospectrograms and waveforms (Figure 1, Table 1). The

data used to define vocalization parameters was taken from ten randomly selected emissions

of each type of vocalization category. These graphs were used to confirm my

categorization of the seven sounds or vocalization types by ear.

Quantitative Analysis of Vocalizations.- While mean and percent occurrences of

five of the seven auditory emissions produced by bottlenose dolphins increased after swim

sessions with humans (Figure 2, Table 2), a one-way ANOVA [Table 3; N = 276; DF = 4

(session type), 271 (sessions)] with pairwise comparisons (Table 4) suggested that

statistically significant differences were present for whistles, jaw claps, tail swishes, barks,

and other emissions only among Control and the four other sample sessions, and only for

whistles between During II and After. For example, whistles were emitted less often

during the Control session than during all other sessions, and the number of whistles

produced in During II sessions were significantly fewer than those produced during After.

However, the difference in number of whistles produced between Before and During I was

insignificant. In four of the remaining six vocalization types Uaw claps, tail swishes, barks

and other) significantly fewer emissions were produced during Control than during one of

the other four sample sessions. None of the remaining six vocalization types were significantly different when the two session sample pairs, indicating immediate temporal differences due to human presence or absence (i.e. Before vs. During I, and During II vs.

After) were compared (Tables 2 and 4). Tables 3 and 4 also suggested that there were no significant differences between any of the session comparisons for tail slaps or grunts.

7 FIGURE 1.- Audiospectrograms and waveforms of dolphin vocalizations. A. Whistles B. Jaw Claps

1 0 1 0 5 5 kHz kHz mS 0 0.0 0.5 1. 0 s 1000 1000 0 0 mV m'l mS 0 s 0.0 0.5 1. 0

c. Tail Slaps D. Tail Swishes E. Grunts

1 0 10 5 5 kHz kHz KHZ s 0.0 s 0.0 mS 0 200 1000 1000 0 0 100qH H ~ ~t· t mV mV ~v s 0.0 s 0.0 mS 0 200

F. Barks G. Other 1 0 1 5 kHz l

8 Table 1.- Vocalization parameters used to distinguish among vocalization types. Data was taken from ten randomly selected vocalizations of each type.

Vocalization Duration (Sec) Frequency Frequency Type Mean SD Range Range (kHz) Pattern

Whistles 0.94 0.52 0.22 - 1.71 2.4 - 11.8 modulated

Jaw Claps 0.05 0.01 0.04- 0.07 0.3 - 12.5 pulsed, irregular

Tail Slaps 0.98 0.18 0.87- 1.19 0.3- 8.2 irregular

Tail Swishes 0.49 0.10 0.42- 0.60 0.3- 9.3 irregular

Grunts 0.29 0.07 0.21 - 0.43 0.3 - 10.9 pulsed, regular

Barks 0.24 0.03 0.21 - 0.29 0.3- 9.1 pulsed, irregular

Other 0.66 0.35 0.46 - 1.06 1.5 - 11.1 modulated

9 FIGURE 2.- Frequencies of seven audible behavior types emitted by dolphins during the five sample sessions. Vocalization Frequencies (Percentage) ...... N W ~ ~ ~ -...) 00 0 0 0 0 0 0 0 0 0

n liD • o r::::nma• 0 ··------894 ::l Ot::tlCl-l-l~~ 263 ~~§~~~g 1 ..,Cil~(/)~oc. [ •..;.. : .. "h:·:·:·:·.·:·:·:·:·:·:·:·:-:· .·· .· · 324 ~ ., ., C> c;; · "' "'0 l',ll ::>""' "' ~

t:O 4387 (1) ~!111·------· 0' 1000 @ . 1149 -0

~(j !;fj c 4957 ~- :::::1. ~~------0 ::l :I (Jq J 1 862 !;fj - 0~ 836

(j u 10683 c ::l. ::l (Jq I 2222 1::::1 k

OA 14900

~"1 ~ I 2125 Table 2.- Mean number and standard error of vocalization totals per session. For all sessions, sample sizes were as follows: Control, N = 24; Before, 53; During I, 53; During

II, 73; and After, 73.

Vocalization Type Control Before During I During II After

Whistles 37 .2 ± 8.0 82.8 ± 7.2 92.8 ± 6.3 145.6 ± 9.8 204.1 ± 14.5

Jaw Claps 3.5 ± 1.1 5.2 ± 1.5 4.2 ± 1.2 6.4 ± 1.3 9.6 ± 1.7 Tail Slaps 0.2 ± 0.2 0.1 ± 0.1 0.2 ± 0.1 0.1 ± 0.0 0.1 ± 0.0

Tail Swishes 3.0± 0.8 2.5 ± 0.7 1.2 ± 0.4 1.2 ± 0.2 1.8 ± 0.3

Grunts 11.0±3.2 18.9 ± 3.1 16.3±3.3 15.9 ± 2.3 17.1 ± 2.1

Barks 13.5 ± 5.6 21.7±6.2 15.8 ± 3.8 29.5 ± 5.7 29.1±4.3

Other 0.4 ± 0.3 1.4 ± 0.8 0.7 ± 0.2 1.5 ± 0.3 1.5±0.3

11 Table 3.- Results of analysis of variance for seven vocalization types among five sample

sessions employing square root transformed data [DF = 4 (session types), 271 (sessions); N = 276 (total number of sessions sampled)].

All Sessions

Variable Sum of Squares Mean Square F-Value Probability

Whistles 1637.85 409.46 32.03 0.001

Jaw Claps 43.43 10.86 2.98 0.02

Tail Slaps 0.04 0.01 0.09 0.98

Tail Swishes 12.26 3.06 2.90 0.02

Grunts 22.78 5.70 1.11 0.35

Barks 128.48 32.12 2.68 0.03

Other 8.90 2.23 2.54 0.04

12 Table 4.- Matrix of significant differences (P values) among pairwise sample session

comparisons within each vocalization type at Dolphins Plus estimated using a one-way

ANOV A model, after square root transformations, followed with pairwise post-hoc

Fisher's Protected LSD tests (Nscssions = 276).

Pairwise Session Comparisons

Vocalization Control vs Before vs During II vs Type Before During I During II After During I After

Whistles <0.01 <0.01 <0.01 < 0.01 0.33 <0.01

Jaw Claps 0.90 0.98 0.34 0.03 0.85 0.08

Tail Slaps 0.88 0.92 0.84 0.87 0.75 0.61

Tail Swishes 0.13 <0.01 0.01 0.14 0.07 0.12

Grunts 0.06 0.20 0.22 0.07 0.41 0.42

Barks 0.67 0.74 0.09 0.03 0.90 0.49

Other 0.22 0.50 0.02 0.02 0.48 0.92

13 Since most dependent variables (vocal behavior categories) were significantly different (Tables 2 and 4) with regard to sample sessions (effect), a MANOVA model was employed to see if the means of two of more variables (vocalization types) measured for several samples (sessions) were equal (Sokal and Rohlf, 1981 ). The Wilk's Lambda test indicated that all vocalization types, whistles, jaw claps, tail slaps, tail swishes, grunts, barks, and other, were positively correlated among the five sample blocks (F-Value =

5.881; DF = 28; P-Value = 0.0001).

14 DISCUSSION

Sample Sessions and Vocal Behavior.- Quantitative comparisons between sample session pairs closely linked temporally (Before and During I, and During II and After), suggested no evidence of effects of stress in dolphins participating in the Swim-with-the

Dolphins program at Dolphins Plus (Table 3). The only vocalization type which showed significant difference between the presence (During II) and absence (After) of human swimmers was whistles. While whistles have been found in other studies to be possible indicators of stress, I did not find this to be the case. In fact, during agonistic displays, whistle emissions were heard much less than other typical agonistic vocalizations, i.e. barks, grunts, jaw claps, tail slaps, and tail swishes. For this reason, whistles were not included in agonistic type vocalizations, and because whistles were the only vocalization type produced in frequencies significantly different during the presence and absence of human swimmers, they were not taken as suggestive evidence of stress. No significant differences were found between any of the seven vocalization types between Before and

During I sessions. Therefore, conspecific stress, if indeed it can be measured by vocalization production frequency, did not increase when captive dolphins were in the presence of human swimmers.

While many significant differences were found between the Control sample session and the other four sample sessions, perhaps this is because Control sample sessions were almost always early in the morning, before the facility opened, or late in the evening, after

Dolphins Plus closed. During these times humans (swimmers and staff) were absent, and frequencies of activity budgets of all dolphins were low. At the onset of this experiment it was assumed that monitoring dolphin vocal behavior in complete absence of humans would

15 not be dependent on what time of day it was. However, time of day is known to influence

rates of vocal and visual behaviors in dolphins (Kellogg, 1961; Lilly, 1962; Powell, 1966;

Saayman et al., 1973; Herman and Tavolga, 1980). Therefore, the low frequencies of

vocal emissions during Control periods may have been due to time effects and scheduling

rather than to the presence or absence of humans. Captive dolphins utilized in a scheduled

pattern of daily events, such as that present at Dolphins Plus, may learn when feedings and

swim sessions are scheduled, therefore reserving their energy to be used for vocal and

visual behavior demonstrations in the presence of humans. A separate study is needed to

address time/activity patterns of captive dolphins in a swim program.

The highly significant result of the Wilks' Lambda test indicated a strong

dependence among the five sample sessions and vocalization types. This dependence

suggested that the presence of one underlying factor among the sample sessions was

measured in several different ways (Ambrose and Ambrose, 1987; Gagnon et al., 1991).

Since the primary variable that was altered and monitored in this study was the presence or absence of human swimmers, this variable was probably the underlying factor that accounted for the strong relationship between the five sample sessions and the seven vocalization types.

Humans show a time lag in acting out behaviors indicative of stress (W. Tollefson, pers. conun.). Since five of the seven vocalization types increased after human swimmers left the water, perhaps dolphins are also exhibiting similar delayed stress behaviors. Spitz

(1993) found a similar pattern when he examined visual behaviors relative to the presence or absence of human swimmers. Further study is needed to examine delayed stress behaviors in dolphins participating in swim programs.

Conclusions.- This study revealed that while dolphin vocalizations increased slightly after human swimmers exited the water, no significant evidence of effects of stress in dolphins were found to be due to the presence or absence of human swimmers. The

16 staff at Dolphins Plus assumes that the dolphins view human swimmers as "toys and

possessions." Only in a few extreme situations have dolphins aggressively interacted over

a human swimmer "possession," whereby the tension and stress among individual

dolphins grew in the presence of human swimmers (D. D. Boege, pers. observ.). People

may simply provide a distraction for the dolphins as is suggested by the fact that

vocalization type frequencies decreased while human swimmers were in the water, and then

increased upon their exit. Or the dolphins may be like humans, having exhibiting delayed

behavioral and vocal expressions of stress after the proximate source of stress was

removed (W. Tollefson, pers. comm.).

Theoretically, a study such as this one intending to measure stress-induced

behavior in dolphins as a function of swimming with humans would need to be conducted immediately after removing dolphins from their free-ranging environment and social

groups, and on individuals placed in swim programs from the onset. Since the dolphins

used in this study had already been participating in Swim-with-the-Dolphin programs for the past six years, the possible factors of learned adjustments made according to time/activity schedules could not be eliminated. Ideally, such a study group should also be comprised of individuals forming a proper social structure (adults, subadults, and juveniles of both sexes, as is seen in free-ranging dolphins). Additional studies, primarily in the disciplines of physiology and psychology are needed to determine if stress levels, as indicated by biochemical markers and cognition, detectably increase when captive dolphins swim with people.

17 LITERATURE CITED

Ambrose, III, H. W., and K. P. Ambrose. 1987. A handbook of biological investigation. 4th ed. Hunter Textbooks, Inc., Winston-Salem, N.C.

Caldwell, M. C., and D. K. Caldwell. 1965. Individualized whistle contours in bottlenosed dolphins (Tursiops truncatus). Nature 207: 434.

Caldwell, M. C., and D. K. Caldwell. 1967. Intraspecific transfer of information via the pulsed sound in captive odontocete cetaceans. In Les Systemes Sonars Animaux, Biologie et Bionique (ed. R. C. Busnel), Laboratoire de Physiologie Acoustique, Jony-en-Jonas, France.

Caldwell, M. C., R. M. Haugen, and D. K. Caldwell. 1962. High-energy sound associated with fright in the dolphin. Science 138: 907-908.

Connor, R. C., and R. S. Smolker. 1985. Habituated dolphins (Tursiops spp.) in Western Australia. J. Mamm. 66: 398-400.

D' Amato, M. R. 1973. Delayed matching and short-term memory in monkeys. In The Psychology of Learning and Motivation: Advances in Research and Theory (ed. G. H. Bower), pp. 227-269, Academic Press, New York.

D ' Amato, M. R., and M. Colombo. 1986. Auditory delayed matching-to-sample in monkeys (Cebus apella). Anim. Lear. and Behav. 13: 375-382.

DeGeorge, D. 1989. Close encounters of the dolphin kind. Business Week 10 April: 101.

Dreher, J. J. 1961. Linguistic considerations of porpoise sounds. J. Acoust. Soc. Am. 33: 1799-1800.

Essapian, F. S. 1963. Observations on abnormalities of parturition in captive bottle-nosed dolphins, Tursiops truncatus, and concurrent behavior of other porpoises. J. Mamm. 44: 405-414.

Gagnon, J., J. Roth, B. Finzer, R. Hofmann, K. Haycock, J. Simpson, and D. Feldman. 1991. SuperANOVA v. 1.11. Abacus Concepts, Inc. , Berkeley.

Herman, L. M. 1991. What the dolphin knows, or might know, in its natural world. In Dolphin Societies (ed. K . Pryor and K. S. Norris), pp. 349-363, University of California Press, Berkeley.

Herman, L. M. and W. N. Tavolga. 1980. The communication systems of cetaceans. In Cetacean Behavior. Mechanisms and Functions (ed. L. M. Herman), pp. 149-209,

18 Wiley-Interscience, New York.

Kellogg, W. N. 1961. Porpoises and Sonar. University of Chicago Press, Chicago.

Lawrence, B. and W. E. Schevill. 1954. Tursiops as an experimental subject. J. of Mamm. 35: 225-232.

Lilly, J. C. 1962. Vocal behavior of the bottlenose dolphin. Proc. Amer. Phil. Soc. 106: 520-529.

Linden, E. 1989. An uneasy dip with the dolphins. Time 27 Nov: 80-81.

McBride, A. F. 1940. Meet Mister porpoise. Nat. Hist. 45: 16-29.

McBride, A. F. , and D. 0. Hebb. 1948. Behavior of the captive bottlenose dolphin, Tursiops truncatus. J. Comp. Physiol. Psycho!. 41: 111-123.

McBride, A. F., and H. Kritzler. 1951. Observations on pregnancy, parturition, and post-natal behavior in the bottlenose dolphin. J. Mamm. 32: 251-266.

Norris, K. S. 1991. Looking at captive dolphins. In Dolphin Societies (ed. K. Pryor and K. S. Norris), pp. 349-363, University of California Press, Berkeley.

Norris, K. S., and T. P. Doh!. 1980. The structure and functions of cetacean schools. In Cetacean Behavior: Mechanisms and Functions (ed. L. M. Herman), pp. 211-262, John Wiley and Sons, New York.

Norris, K. S., and T. P. Dohl. 1980a. Behavior of the Hawaiian spinner dolphin, Stenella longirostris. Fish. Bull. 77: 821 -847.

Ostman, J. 1991. Changes in aggressive and sexual behavior between two male bottlenose dolphins (Tursiops truncatus) in a captive colony. In Dolphin Societies (ed. K. Pryor and K. S. Norris), pp. 304-317, University of California Press, Berkeley.

Popper, A. N. 1980. Sound emission and detection by delphinids. In Cetacean Behavior: Mechanisms and Functions (ed. L. M. Herman), pp. 1-52, John Wiley and Sons, New York.

Powell, B. A. 1966. Periodicity of vocal activity of captive Atlantic bottlenose dolphins: (Tursiops truncatus). Bull. Sth. Calif. Acad. Sci. 65: 237-244.

Pryor, K. 1973. Behavior and learning in porpoises and whales. Naturwissenschaften 60: 412.

Pryor, K. W. and I. R. Schallenberger. 1991. Social structure in spotted dolphins (Stenella attenuata) in the tuna purse seine fishery in the eastern tropical Pacific. In Dolphin Societies (ed. K. Pryor and K. S. Norris), pp. 160-196, University of California Press, Berkeley.

Ralston, J. V., and L. M. Herman. 1989. Dolphin auditory perception. In The Comparative Psychology of Audition: Perceiving Complex Sounds (eds. R. J.

19 Dooling and S. H. Hulse), pp. 295-328, Lawrence Erlbaum Associates, Hillsdale.

Saayman, G. S., C. K. Tayler, and D. Bower. 1973. Diurnal activity cycles in captive and free-ranging Indian Ocean bottlenose dolphins (Tursiops aduncus Ehrenburg). Behaviour 44: 212-233.

Schevill, W. E., and B. Lawrence. 1952. Ketophonics. Woods Hole Ocean. Inst. Ref.: 52-80.

Schevill, W. E., and B. Lawrence. 1956. Food-finding by a captive porpoise (Tursiops truncatus). Breviora 53: 1-15.

Scott, M. D., R. S. Wells, A. B. Irvine, and B. R. Mate. 1990. Tagging and marking studies on small cetaceans. In The Bottlenose Dolphin (eds. S. Leatherwood and R. R. Reeves), pp. 489-514, Academic Press, San Diego.

Shane, S. H. 1990. Behavior and ecology of the bottlenose dolphin at Sanibel Island, Florida. In The Bottlenose Dolphin (eds. S. Leatherwood and R. R. Reeves), pp. 245-265, Academic Press, San Diego.

Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman and Company, New York.

Spitz, S. S. 1993. Patterns of association in captive Atlantic bottlenose dolphins in a swim program. Unpublished Masters Thesis. Florida Atlantic University, Boca Raton.

Tavolga, M. C., and F. S. Essapian. 1957. The behavior of the bottle-nosed dolphin (Tursiops truncatus): mating, pregnancy, parturition and mother-infant behavior. Zoologica 42: 11-31.

Taylor, C. R. and G. S. Saayman. 1973. Imitative behavior by Indian Ocean bottlenose dolphins (Tursiops aduncus) in captivity. Behaviour 44: 286-298.

Tyack, P. 1991. Use of a telemetry device to identify which dolphin produces a sound. In Dolphin Societies (eds. K. Pryor and K. S. Norris), pp. 319-344, University of California Press, Berkeley.

Wood, F. G., Jr. 1954. Underwater sound production and concurrent behavior of captive porpoises, Tursiops truncatus and Stenella placiodon. Bull. Mar. Scien. Gulf Carr. 3: 120-133.

Wiirsig, B. 1979. Dolphins. Scient. Amer. 240: 136-147.

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