Theriogenology 66 (2006) 242–250

www.journals.elsevierhealth.com/periodicals/the

Characterization of male killer whale (Orcinus orca) sexual

maturation and reproductive seasonality T.R. Robeck
a,
*, S.L. Monfort b
a
Sea World and Busch Gardens’ Reproductive Research Center, 500 SeaWorld Drive,
San Diego, CA 92019, USA
b
Conservation and Research Center, National Zoological Park, Smithsonian Institution, Front
Royal, VA 22630, USA
Received 17 August 2005; accepted 3 November 2005

Abstract

Longitudinal serum testosterone concentrations (n = 10 males) and semen production (n = 2 males) in killer whales were
evaluated to: (1) characterize fluctuations in serum testosterone concentrations with respect to reproductive maturity and season;
(2) compare morphologic changes to estimated age of sexual maturity, based on changes in serum testosterone concentrations;
and (3) evaluate seasonal changes in sperm production. Classification of reproductive status and age class was based on
differences (P< 0.05) in serum testosterone concentrations according to age; juvenile males ranged from 1 to 7 years (mean S.D.
testosterone, 0.13 0.20 ng/mL), pubertal males from 8 to 12 years (2.88 3.20 ng/mL), and sexually mature animals were 13
years and older (5.57 2.90 ng/mL). For captive-born males, serum testosterone concentrations, total body length and height to
width ratio of the dorsal fin were 0.7 0.7 ng/mL, 495.6 17.5 cm and 1.14 0.13 cm, respectively, at puberty; at sexual maturity,
these end points were 6.0 3.3 ng/mL, 548 20 cm and 1.36 0.1 cm. Serum testosterone concentrations were higher (P< 0.05)
from March to June than from December to February in pubertal animals (4.2 3.4 ng/mL versus 1.4 2.6 ng/mL) and than from
September to December in sexually mature animals (7.2 3.3 ng/mL versus 4.0 2.0 ng/mL). Ejaculates (n = 90) collected from
two males had similar (P> 0.05) sperm concentrations across all months. These data represent the first comprehensive study on
male testosterone concentrations during and after sexual maturation, and on reproductive seasonality in the killer whale.
# 2005 Elsevier Inc. All rights reserved.

Keywords: Delphinidae; Cetacean; Reproductive endocrinology; Sperm production; Sexual maturation

1. Introduction killer whales have been estimated to reach sexual

Killer whales, Orcinus orca, the largest member of
the family Delphinidae, are found throughout the
majority of oceans in the world. Despite their
widespread presence, very little is known about male
maturity around 15–16 years of age and between 548
and 610 cm in length [1,2]. In addition, Olesiuk et al.
[3] defined male sexual maturity in wild killer whales
occurring when the male dorsal fin (height to width
ratio: HWR) could be consistently distinguished from
 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
reproductive physiology and development. Wild male
* Corresponding author. Tel.: +1 210 523 3294; fax:
+1 210 523 3299.
E-mail address: Todd.Robeck@SeaWorld.com (T.R. Robeck).
0093-691X/$ – see front matter # 2005 Elsevier Inc. All rights reserved.
doi:10.1016/j.theriogenology.2005.11.007
furthermore, they estimated that puberty occurred 2–3
years before males could be distinguished from
females on the basis of the HWR of the dorsal fin.
For captive killer whales, serum testosterone
concentrations remained <1 ng/mL until an estimated
age of 12 years [4]. Additionally, the absence of a
consistent seasonal rhythm in testosterone secretion
was confirmed by preliminary data obtained from five
captive adult male killer whales [5]. Killer whale male
seasonality was consistent with female reproductive
cyclicity, which can occur throughout the year [6–8].
However, too few animals were studied over relatively
short time intervals to permit definitive conclusions
regarding the existence of reproductive seasonality in
males [4,5]. Clearly, long-term endocrine evaluations,
concurrent with assessment of growth, sexual
maturation and sperm production, are needed to better
understand the reproductive biology of killer whales.
The objectives of this study were to: (1) characterize
fluctuations in testosterone concentrations in
association with reproductive maturity and season; (2)
compare morphologic changes to estimated age of
sexual maturity based on changes in serum
testosterone; and (3) evaluate seasonal changes in
sperm production.
2. Materials and methods
2.1. Ethics of experimentation
All samples were collected using routine husbandry
training and on a voluntary basis. Training of
husbandry behavior to facilitate biological sample
collection is currently viewed as the standard of care
for captive marine mammals. All procedures described
within were reviewed and approved by the SeaWorld
Institutional Animal Care and Use Committee and
were performed in accordance with the US Animal
Welfare Act for the care of Marine Mammals.
243
that of the female. More specifically, a HWR ratio of
1.4 or greater was indicative of a sexually mature male
(first detected in wild males between 11 and 17 years
of age).
Olesiuk et al. [3] hypothesized that this secondary
sexual characteristic developed in response to
increased testosterone production (in association with
puberty);
2.2. Animals and experiments
Testosterone concentrations were measured on
serum samples (n = 1388) collected for routine
husbandry procedures from 10 male killer whales (age
1–18 years; Table 1). These males were housed at three
separate SeaWorld habitats that contained a minimum
of 20 106 L of manufactured salt water, cooled year
round with temperatures ranging from 11.1 to 12.8 8C.
Semen samples were collected from Male 3 (body
weight, 4090 kg) and Male 4 (body weight, 5254 kg)
and used to characterize the effects of season on sperm
production. All study animals were fed frozen-thawed
whole fish (herring, Clupea harengus,
ColumbiaRiversmelt,Thaleichthyspacificus,andpink
salmon, Oncorhynchus gorbuscha) at approximately 2–
3% of their body weight per day. The animals were
housed in mixed male and female groups of various
age classes.
2.3. Testosterone radioimmunoassay
A double-antibody [125I] testosterone
radioimmunoassay (ICN, Costa Mesa, CA, USA) was
validated for unextracted male killer whale serum or
heparinized plasma. The antiserum cross-reacted
100% with testosterone, 3.4% with 5a-
dihydrotestosterone, 2.2% with 5al-androstane-3b-
17b-diol, 2.0% with 11-oxotestosterone, and <1%
with all other steroids tested. Individual animal peak
serum testosterone concentrations were classified as
any value that exceeded 2S.D. above baseline
concentrations for that animal. Serum testosterone
concentration at the time of conception was estimated
by calculating the mean testosterone concentration for
samples collected immediately prior to and after the
estimated conception date. The onset of puberty was
subjectively estimated for animals with known birth
dates (no samples were collected from wild caught
males prior to puberty) by comparing all data
collected during Year 2 (24–36 months of age) to
244 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
every successive 12-months increment. The first year
that T was elevated (P < 0.05) above basal
concentrations was considered the onset of puberty.
The year of sexual maturity was defined as the 1st
year following pubertal onset (as described
previously) for which median serum testosterone
concentrations exceeded (P < 0.05) those during the
year of pubertal onset, and where concentrations for
every sample were 1 ng/mL. Data from all males
(captive born and wild caught) were combined based
on age (or estimated age for wild-caught animals) to
describe fluctuations in testosterone secretion relative
to age.
2.4. Age, growth, and morphometry
Total body length and dorsal fin height and width
were collected from four captive-born male killer
whales from January 1996 to March 2005 (Males 5–
8; Table 1). Total body length (cm) was assessed as
described by Norris [10], whereas the dorsal fin
height (cm) and width (cm) were determined at least
every 2 months and used to determine the HWR as
described by Olesiuk et al. [3].
2.5. Semen collection and processing
The animals were trained for voluntary semen
collection, as previously described [11,12]. Briefly,
the animal was trained to present his penis while in
dorsal recumbency adjacent to the edge of the pool.
Prior to training, the male was sexually stimulated by
a receptive female. Once the male appeared sexually
stimulated (as assessed by display of courtship
behavior, partial extrusion of penis from the genital
groove), operant conditioning using a positive
reinforcement schedule was commenced. During
training sessions, ejaculation occurred at variable
intervals before, during or after presentation of the
penis. Semen was collected into a 125 mL cylindrical
plastic collection container (Nalgene 1; Nalge Nunc
International, Rochester, NY, USA). Semen samples
displaying gross contamination of urine or pool water
were discarded. Ejaculate concentration, volume,
color, pH (pH indicator strips; Whatman Inc., Ann
Arbor, MI, USA) were assessed within 30 min of
collection.
2.6. Statistical analysis

Table 1
Description of male killer whales used and samples collected
Male DOBa Location Date range for No. samples Age at first No. calves
serum samples conception (years) sired

1 1974b SWC 10/76 to 10/85 n = 84 15 2

2 1976b SWSAf 02/88 to 04/95 n = 129 13 3
3 1977b SWSDe 02/94 to 01/01 n = 107 – –
01/04 to 10/05d n = 28

4 1982b SWOc 01/92 to 12/00 n = 208 8 8

09/98 to 10/05d n = 62

5 8/89g SWC 04/92 to 4/2004 n = 253 – –

6 12/91g SWT 01/93 to 4/2004 n = 157 – –
7 2/93g SWT 11/93 to 4/2004 n = 194 11 1
8 9/93g SWC 09/94 to 4/2004 n = 216 – –
9 6/95g SWO 04/99 to 4/00 n = 22 – –
10 5/98g SWO 01/00 to 12/00 n = 18 – –

a
Date of birth. Non-parametric monthly median serum
b
Estimated age for wild-caught whales. c
SeaWorld testosterone concentrations and sperm concentrations
Orlando. were compared using Kruskal–Wallis ANOVA on
d
Date range for collection of semen samples. ranks, and Dunn’s multiple comparison test
e
SeaWorld San Diego. f
SeaWorld San (SigmaStat, Version
g
Antonio. Captive born. 2.0; SSPS, Inc., San Rafael, CA, USA). All pair-wise
multiple-comparison procedures between means were
 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
conducted using the Student–Newman–Keuls (SNK)
test. A level of P < 0.05 was considered significant
and unless noted, data are presented as the mean S.D.
3. Results
3.1. Serum testosterone concentrations
Parallel displacement curves were obtained by
comparing serial dilutions (range = undiluted–1:32) of
pooled killer whale serum and testosterone standard
preparations. Recovery of known amounts of
unlabelled testosterone (range = 0.05–5.0 ng/mL)
added to a pool of diluted killer whale serum was 123.4
11.9% (y = 0.06 + 1.0x; R2 = 0.99). Based on RIA of
elutes after HPLC [13], all immunoreactivity was
associated with a single peak that co-eluted with
testosterone. Killer whale serum was diluted (1:4–1:8)
and assayed (25 mL) in duplicate. Inter- and intra-
assay variation were 8.5 and <10%, respectively,
whereas assay sensitivity was 0.05 ng/mL.
3.2. Reproductive maturity and seasonality
Median testosterone concentrations first became
elevated and sustained above baseline (P < 0.05) at 8
years of age. Median testosterone concentrations for all
Fig. 1. Mean (S.D.) monthly serum testosterone concentrations from all killer whale males combined (n = 10), based on known (n = 6) or
estimated age (n = 4). Months under different brackets are different (P < 0.05).
older males (8–24 years) remained elevated (P <
0.05) above median concentrations for 1–7-year-old
males. Whereas 13–24-year-old males always had
245
higher concentrations than 8 years olds (P < 0.05),
concentrations for this group were not different from
9- to 12year-old males. From these data, juvenile
animals were defined as ranging from 1 to 7 years of
age, pubertal animals from 8 to 12 years of age, and
sexually mature animals 13 years of age and older.
Among-group median testosterone concentrations for
these age classifications (juvenile: median, 0.06; mean,
0.13 0.20 ng/mL; pubertal: median, 2.17; mean, 2.88
3.20 ng/mL; sexually mature: median, 5.15; mean, 5.57
2.90 ng/mL) were different (P < 0.001; Fig. 1). The age
at which the four reproductive males in the study (one
captive born and three wild caught) first sired calves
was 11.8 2.9 years.
Four males with known birth dates (Males 5–8)
exhibited transitions from juvenile (<0.4 ng/mL) to
pubertal (>1 ng/mL, P < 0.05). Mean testosterone
concentrations and age at the onset of puberty were
0.70 0.70 ng/mL (n = 79, range 0.05–3.40 ng/mL) and
7.8 1.0 years (range 7–9 years), respectively. The
mean length and HWR for these captive born males at
puberty was 495.6 17.5 and 1.14 0.13 cm,
respectively. Of these four males, only three reached
an HWR of 1.4 during the sampling period (mean of 13
2 years; range 11–15 years). The interval from puberty
to first achieving a HWR of 1.4 was 4.3 2.5 years
(range 2–7 years). Males 5, 6 and 8 reached sexual
maturity during the sampling period. Mean testosterone
concentrations, age, length and HWR at sexual
maturity were 6.0 3.3 ng/mL, 11.6 2.1 years, 548 20
cm, and 1.36 0.1 cm, respectively (Table 2).
246 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
No differences in median monthly testosterone
concentrations were detected in juvenile males. Peak
concentrations occurred from March to July and
February to June for pubertal and sexually mature
animals, respectively (Fig. 2). For pubertal animals,
the months of March to June (mean, 4.2 3.4 ng/mL)
had higher (P < 0.05) median T (3.28 ng/mL) values
than the nadir months of December to February
(median, 0.43 ng/mL; mean, 1.4 2.6 ng/mL). In
sexually animals, the months of March to June (mean,
7.2 3.3 ng/mL) had higher (P < 0.05) median
testosterone concentrations (6.5 ng/mL) than the nadir
months of September to December (median, 3.6
ng/mL; mean, 4.0 2.0 ng/mL; Fig. 2). Conceptions
occurred throughout the year. Although individual
Table 2
Mean (S.D.) serum testosterone concentration, body length and dorsal fin height to width ratio (HWR a) from puberty to sexual maturity in four
captive-born male killer whales
Male 5
animals within the group exhibited cyclic variations
in testosterone concentration, annual within- and
among-animal differences were observed in the
monthly zenith of testosterone concentration. Thus,
while annual patterns of testosterone concentrations
could be clearly defined for each individual, variation
from year-to-year resulted in a more blunted,
prolonged period of peak testosterone in the
population as a whole (Figs. 2 and 3). For males (n =
4) that sired calves during the sampling interval,
serum testosterone concentrations at the estimated
time of conception (n = 13 samples) were below peak
concentrations (>baseline + 2S.D.). Mean testosterone
at conception and baseline for each male,
respectively, were: Male 1,
Male 6 Male 7 Male 8 Overall

Date of birth 08/15/1989 12/24/1991 02/02/1993 09/09/1993

Puberty Age
(years) 8 9 7 7 7.8 1.0
Testosterone (ng/mL)
Mean 1.1 1.0 0.8 0.8 0.3 0.4 0.5 0.5 0.7 0.7
Range 0.05–3.4 (n = 15) 0.05–2.2 (n = 16) 0.05–1.2 (n = 14) 0.05–2.4 (n = 34) 0.05–3.4 (n = 79)
Length (cm) 515 8 (n = 25) 501 15 (n = 8) 474 10 (n = 18) 491 9 (n = 25) 496 19 (n = 76)
HWR (cm) 1.03 0.05 (n = 21) 1.13 0.07 (n = 25) 1.23 0.07 (n = 21) 1.05 0.09 (n = 26) 1.11 0.10 (n = 93)
Sexual maturity
Age (years) 14 – 11 10 11.6 2.1
Testosterone (ng/mL)
Mean 5.5 2.2 – 4.7 3.6 7.0 3.5 6.0 3.3
Range 1.2–8.0 (n = 8) – 1.2–10.0 (n = 9) 1.5–13.9 (n = 15) 1.2–13.9 (n = 32)
Length (cm) 561 8 (n = 10) – 522 6 (n = 10) 559 12 (n = 10) 548 20 (n = 30)
HWR (cm) 1.34 0.08 (n = 12) – 1.43 0.11 (n = 7) 1.21 0.08 (n = 7) 1.36 0.1 (n = 26)
HWR 1.4
Age (years) 15 13 9 – 13.0 2.0
Testosterone (ng/mL)
Mean No samples No samples 0.8 0.9 – –
Range 0.05–3.0 (n = 23) – –

Length (cm) 568 9 (n = 6) 568 8 (n = 6) 500 10 (n = 24) – 522 34 (n = 36)

n = number of serum samples or measurements used to determine the respective values.
a
HWR 1.4 is the proposed size of the dorsal fin at sexual maturity in wild killer whales [3].
 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250 247

Fig. 2. Mean (S.D.) monthly serum testosterone concentrations for juvenile (~), pubertal (*) and sexually mature (&) male killer whales. For
pubertal animals, the months of March to June (mean 4.2 3.4 ng/mL) had higher (P < 0.05) higher median T (3.28 ng/mL) values than the nadir
months of December to February (median, 0.43 ng/mL; mean, 1.4 2.6 ng/mL). In sexually mature animals, the months of March to June (mean
7.2 3.3 ng/mL) had higher (P < 0.05) median testosterone concentrations (6.5 ng/mL) than the nadir months of September to December
(median,
3.6 ng/mL; mean, 4.0 2.0 ng/mL). Conceptions per month are represented by grey vertical bars.
248 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250

Fig. 3. Mean (S.D.) serum testosterone concentrations values from three male adult killer whales (Male 2: top graph; Male 3: middle graph;
Male
4: bottom graph) over a 4-year interval. Peak testosterone values are located above the horizontal line (baseline 2S.D.). Each grey vertical bar
represents one conception. 2005)
frombothmales.Themeanspermconcentrationandtotal
sperm/ejaculate from Males 3 and 4 was 54.7
7.7 1.5 and 4.8 2.1 ng/mL; Male 2, 6.4 3.2 and 4.1
1.5 ng/mL; Male 4, 6.7 2.2 and 5.9 2.0 ng/ mL; Male 36.7 107 sperm/mL; 46.7 52.9 108 total sperm/
7, 0.98 0.4 and 1.7 1.6 ng/mL. Whereas testosterone ejaculate and 72.1 51.4 107 sperm/mL; 55.9 92.2 108
concentrations in pubertal animals sometimes sperm/ejaculate, respectively. Monthly ejaculate
decreased to < 1 ng/mL, concentrations in sexually sperm concentration for Males 3 or 4 did not change
mature animals were consistently > 1 ng/mL (P > 0.05), thus there was no apparent relationship
throughout the year (Figs. 2 and 3). between this end point (or total spermatozoa per
ejaculate, data not shown) and monthly serum
3.3. Sperm concentrations testosterone concentration (Fig. 4).

Sperm concentrations were determined from 90

ejaculates (Male 3, n = 28; Male 4, n = 62) collected
over a maximum of 7 years (April 1998 to October
 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
4. Discussion
Population management of both captive and wild
species requires an understanding of basic
reproductive biology. For killer whales, most research
Fig. 4. Mean (S.D.) monthly serum testosterone (*) and sperm concentrations (vertical grey bars) from killer whale Male 3 (n = 107 serum
testosterone samples; n = 28 ejaculates) Male 4 (n = 208 serum testosterone samples; n = 62 ejaculates).
has been focused on defining female reproductive
physiology [6,9,14]. While equally important for the
development of effective reproductive management
plans, little information has been collected on male
reproduction. The present study provides new,
extensive information on serially collected serum
testosterone concentrations from multiple maturing
and adult males, and seasonal semen production. In
contrast to patterns of testosterone secretion with
prolonged nadir concentrations and clear periods of
peak elevation observed in seasonally reproductive
delphinids (spinner dolphin, Stenella longirostris
[15]; Pacific white-sided dolphin, Lagenorhynchus
obliquidens; Robeck unpublished), and similar to
those with less defined seasonal testosterone secretion
that produce spermatozoa throughout the year
(bottlenose dolphin, Tursiops truncatus [16]),
testosterone concentrations from adult male killer
whales (>13 years) always remained above 1 ng/mL
and demonstrated periods of elevation (spring to fall).
Despite these apparent seasonal rhythms in
testosterone secretion (particularly within each
animal), sperm production did not exhibit an obvious
seasonal change. Thus, it appears that even during
periods of relatively low testosterone secretion,
spermatogenesis is maintained. These findings were
249
consistent with observations collected from wild and
captive killer whale pods that demonstrated diffuse
seasonal reproduction, with conceptions peaking from
spring to fall, but occurring throughout the year
[3,6,7]. For captive males in this study, conceptions
occurred during periods characterized by low and
high testosterone concentrations, but males had little
competition for access to estrus females. Since
increased libido caused by elevated testosterone may
be important for establishing dominance over
potential competitors, seasonal variations in
testosterone may reflect a situation in the wild where
elevated concentrations are associated with seasonal
variations in the geographic availability of females.
Recent evidence suggested that cortisol increases in
response to seasonal environmental stressors (i.e.,
reduced air and/or water temperatures) may be
associated with mild seasonal changes in reproductive
hormone concentrations [17].
Olesiuk et al. [3] predicted that the beginning of
testosterone production (initiation of puberty)
responsible for the increase in HWR of the dorsal fin
probably occurred 2–3 years prior to sexual maturity
(and HWR of 1.4). Using this assumption, their
predicted age of puberty for killer whales (range 7.5–
14.5 years) was similar to our estimations based on
serum testosterone concentrations (range 8–12 years).
Males were reported to attain sexual maturity at a mean
age of 14.5 years [3], which is approximately 1.5 years
older than when known age animals attained the HWR
of 1.4 in the present study. When classifying males as
sexually mature in this study using serum testosterone
250 T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250
data, a concurrent dorsal fin HWR of at least 1.4 was
not always observed. In fact, one male had an HWR of
1.4 as early as 2 years after the onset of puberty,
corresponding to 2 years prior to sexual maturity
(based on serum testosterone). Although HWR may be
useful for generalizations about a population, one must
consider that dorsal fin growth rate may vary among
individuals prior to the influence of serum testosterone.
Potential factors influencing the age at which an
animal reaches HWR of 1.4 include genetic differences
in growth rate, the final adult size of the body and
dorsal fin, social status, and responsiveness to the
influences of testosterone.
Other reports of killer whale sexual maturation have
relied on post-mortem analysis of testis to describe
spermatogenesis, combined with age estimations
(based on tooth and total length). Substantial elevations
in testosterone production first occurred at a mean
body length of 496 cm in males of known birth date in
this study (n = 4). In contrast, Johnsgard and Lyshoel
[18] estimated spermatogenesis occurred around 580
cm
bodylength,whereasBigg[1]notedthesharpestincrease in
testes weight occurred around 550 cm body length.
Using Christensen’s [2] growth curves, Olesiuk et al.
[3] estimated the age associated with the lengths
reported in those studies was a mean of 19.8 years.
Although our males reached sexual maturity at the
lower end of length (548
cm)previouslydescribed[1],thecorrespondingage was
demonstrably lower at 11.6 years. Whether this
disparityinagedataatsexualmaturityisareflectionofan
increased and consistently higher plane of nutrition for
captive animals, small sample size, inaccurate
estimations of wild animal age, or some combination
offactors, remains unknown. Regardless, the data
presented herein, both in terms of sperm production
and fertility, provided clear evidence that killer whale
reproductive potential begins earlier in life than
previously reported.
Acknowledgements
We thank the veterinary, animal laboratory, animal
care and animal training staff at SeaWorld Orlando,
San Antonio and San Diego for their consistent
support, and sample collection necessary to make this
research possible. We especially thank Laura Surovik,
Matt Fripp and Brian Rokeach and the animal training
staff at SeaWorld Orlando and SeaWorld San Diego
for semen collection. We thank Dr. J.K. O’Brien for
editorial comments and Steve Clark for growth data.
We also recognize the technical support provided by
Karen Steinman and Kendall Mashburn in conducting
endocrine analyses. We thank Brad Andrews, Jim
McBain and Thad Lacinak for their consistent support
for this research. This project was funded by SeaWorld
Corporation and is a SeaWorld Technical contribution
Number 2004-01-T.
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