Characterization of Male Killer Whale (Orcinus Orca) Sexual Maturation and Reproductive Seasonality

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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


maturity around 15–16 years of age and between 548
Killer whales, Orcinus orca, the largest member of and 610 cm in length [1,2]. In addition, Olesiuk et al.
the family Delphinidae, are found throughout the [3] defined male sexual maturity in wild killer whales
majority of oceans in the world. Despite their occurring when the male dorsal fin (height to width
widespread presence, very little is known about male ratio: HWR) could be consistently distinguished from
T.R. Robeck, S.L. Monfort/Theriogenology 66 (2006) 242–250 243
reproductive physiology and development. Wild male 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
* Corresponding author. Tel.: +1 210 523 3294; fax: sexual characteristic developed in response to
+1 210 523 3299. increased testosterone production (in association with
E-mail address: [email protected] (T.R. Robeck). puberty);
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 2.2. Animals and experiments
years before males could be distinguished from
females on the basis of the HWR of the dorsal fin. Testosterone concentrations were measured on
For captive killer whales, serum testosterone serum samples (n = 1388) collected for routine
concentrations remained <1 ng/mL until an estimated husbandry procedures from 10 male killer whales (age
age of 12 years [4]. Additionally, the absence of a 1–18 years; Table 1). These males were housed at three
consistent seasonal rhythm in testosterone secretion separate SeaWorld habitats that contained a minimum
was confirmed by preliminary data obtained from five of 20 106 L of manufactured salt water, cooled year
captive adult male killer whales [5]. Killer whale male round with temperatures ranging from 11.1 to 12.8 8C.
seasonality was consistent with female reproductive Semen samples were collected from Male 3 (body
cyclicity, which can occur throughout the year [6–8]. weight, 4090 kg) and Male 4 (body weight, 5254 kg)
However, too few animals were studied over relatively and used to characterize the effects of season on sperm
short time intervals to permit definitive conclusions production. All study animals were fed frozen-thawed
regarding the existence of reproductive seasonality in whole fish (herring, Clupea harengus,
males [4,5]. Clearly, long-term endocrine evaluations, ColumbiaRiversmelt,Thaleichthyspacificus,andpink
concurrent with assessment of growth, sexual salmon, Oncorhynchus gorbuscha) at approximately 2–
maturation and sperm production, are needed to better 3% of their body weight per day. The animals were
understand the reproductive biology of killer whales. housed in mixed male and female groups of various
The objectives of this study were to: (1) characterize age classes.
fluctuations in testosterone concentrations in
association with reproductive maturity and season; (2) 2.3. Testosterone radioimmunoassay
compare morphologic changes to estimated age of
sexual maturity based on changes in serum A double-antibody [125I] testosterone
testosterone; and (3) evaluate seasonal changes in radioimmunoassay (ICN, Costa Mesa, CA, USA) was
sperm production. validated for unextracted male killer whale serum or
heparinized plasma. The antiserum cross-reacted
2. Materials and methods 100% with testosterone, 3.4% with 5a-
dihydrotestosterone, 2.2% with 5al-androstane-3b-
2.1. Ethics of experimentation 17b-diol, 2.0% with 11-oxotestosterone, and <1%
with all other steroids tested. Individual animal peak
All samples were collected using routine husbandry serum testosterone concentrations were classified as
training and on a voluntary basis. Training of any value that exceeded 2S.D. above baseline
husbandry behavior to facilitate biological sample concentrations for that animal. Serum testosterone
collection is currently viewed as the standard of care concentration at the time of conception was estimated
for captive marine mammals. All procedures described by calculating the mean testosterone concentration for
within were reviewed and approved by the SeaWorld samples collected immediately prior to and after the
Institutional Animal Care and Use Committee and estimated conception date. The onset of puberty was
were performed in accordance with the US Animal subjectively estimated for animals with known birth
Welfare Act for the care of Marine Mammals. 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 2.5. Semen collection and processing
that T was elevated (P < 0.05) above basal
concentrations was considered the onset of puberty. The animals were trained for voluntary semen
The year of sexual maturity was defined as the 1st collection, as previously described [11,12]. Briefly,
year following pubertal onset (as described the animal was trained to present his penis while in
previously) for which median serum testosterone dorsal recumbency adjacent to the edge of the pool.
concentrations exceeded (P < 0.05) those during the Prior to training, the male was sexually stimulated by
year of pubertal onset, and where concentrations for a receptive female. Once the male appeared sexually
every sample were 1 ng/mL. Data from all males stimulated (as assessed by display of courtship
(captive born and wild caught) were combined based behavior, partial extrusion of penis from the genital
on age (or estimated age for wild-caught animals) to groove), operant conditioning using a positive
describe fluctuations in testosterone secretion relative reinforcement schedule was commenced. During
to age. training sessions, ejaculation occurred at variable
intervals before, during or after presentation of the
2.4. Age, growth, and morphometry penis. Semen was collected into a 125 mL cylindrical
plastic collection container (Nalgene 1; Nalge Nunc
Total body length and dorsal fin height and width International, Rochester, NY, USA). Semen samples
were collected from four captive-born male killer displaying gross contamination of urine or pool water
whales from January 1996 to March 2005 (Males 5– were discarded. Ejaculate concentration, volume,
8; Table 1). Total body length (cm) was assessed as color, pH (pH indicator strips; Whatman Inc., Ann
described by Norris [10], whereas the dorsal fin Arbor, MI, USA) were assessed within 30 min of
height (cm) and width (cm) were determined at least collection.
every 2 months and used to determine the HWR as
described by Olesiuk et al. [3]. 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) 242–250 245
conducted using the Student–Newman–Keuls (SNK) higher concentrations than 8 years olds (P < 0.05),
test. A level of P < 0.05 was considered significant concentrations for this group were not different from
and unless noted, data are presented as the mean S.D. 9- to 12year-old males. From these data, juvenile
animals were defined as ranging from 1 to 7 years of
3. Results age, pubertal animals from 8 to 12 years of age, and
sexually mature animals 13 years of age and older.
3.1. Serum testosterone concentrations Among-group median testosterone concentrations for
these age classifications (juvenile: median, 0.06; mean,
Parallel displacement curves were obtained by 0.13 0.20 ng/mL; pubertal: median, 2.17; mean, 2.88
comparing serial dilutions (range = undiluted–1:32) of 3.20 ng/mL; sexually mature: median, 5.15; mean, 5.57
pooled killer whale serum and testosterone standard 2.90 ng/mL) were different (P < 0.001; Fig. 1). The age
preparations. Recovery of known amounts of at which the four reproductive males in the study (one
unlabelled testosterone (range = 0.05–5.0 ng/mL) captive born and three wild caught) first sired calves
added to a pool of diluted killer whale serum was 123.4 was 11.8 2.9 years.
11.9% (y = 0.06 + 1.0x; R2 = 0.99). Based on RIA of Four males with known birth dates (Males 5–8)
elutes after HPLC [13], all immunoreactivity was exhibited transitions from juvenile (<0.4 ng/mL) to
associated with a single peak that co-eluted with
pubertal (>1 ng/mL, P < 0.05). Mean testosterone
testosterone. Killer whale serum was diluted (1:4–1:8)
concentrations and age at the onset of puberty were
and assayed (25 mL) in duplicate. Inter- and intra-
0.70 0.70 ng/mL (n = 79, range 0.05–3.40 ng/mL) and
assay variation were 8.5 and <10%, respectively,
7.8 1.0 years (range 7–9 years), respectively. The
whereas assay sensitivity was 0.05 ng/mL.
mean length and HWR for these captive born males at
puberty was 495.6 17.5 and 1.14 0.13 cm,
3.2. Reproductive maturity and seasonality
respectively. Of these four males, only three reached
an HWR of 1.4 during the sampling period (mean of 13
Median testosterone concentrations first became
2 years; range 11–15 years). The interval from puberty
elevated and sustained above baseline (P < 0.05) at 8
to first achieving a HWR of 1.4 was 4.3 2.5 years
years of age. Median testosterone concentrations for all
(range 2–7 years). Males 5, 6 and 8 reached sexual

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).
maturity during the sampling period. Mean testosterone
older males (8–24 years) remained elevated (P < concentrations, age, length and HWR at sexual
0.05) above median concentrations for 1–7-year-old maturity were 6.0 3.3 ng/mL, 11.6 2.1 years, 548 20
males. Whereas 13–24-year-old males always had 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 animals within the group exhibited cyclic variations
concentrations were detected in juvenile males. Peak in testosterone concentration, annual within- and
concentrations occurred from March to July and among-animal differences were observed in the
February to June for pubertal and sexually mature monthly zenith of testosterone concentration. Thus,
animals, respectively (Fig. 2). For pubertal animals, while annual patterns of testosterone concentrations
the months of March to June (mean, 4.2 3.4 ng/mL) could be clearly defined for each individual, variation
had higher (P < 0.05) median T (3.28 ng/mL) values from year-to-year resulted in a more blunted,
than the nadir months of December to February prolonged period of peak testosterone in the
(median, 0.43 ng/mL; mean, 1.4 2.6 ng/mL). In population as a whole (Figs. 2 and 3). For males (n =
sexually animals, the months of March to June (mean, 4) that sired calves during the sampling interval,
7.2 3.3 ng/mL) had higher (P < 0.05) median serum testosterone concentrations at the estimated
testosterone concentrations (6.5 ng/mL) than the nadir time of conception (n = 13 samples) were below peak
months of September to December (median, 3.6 concentrations (>baseline + 2S.D.). Mean testosterone
ng/mL; mean, 4.0 2.0 ng/mL; Fig. 2). Conceptions at conception and baseline for each male,
occurred throughout the year. Although individual respectively, were: Male 1,
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 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) 242–250 249
4. Discussion consistent with observations collected from wild and
captive killer whale pods that demonstrated diffuse
Population management of both captive and wild seasonal reproduction, with conceptions peaking from
species requires an understanding of basic spring to fall, but occurring throughout the year
reproductive biology. For killer whales, most research [3,6,7]. For captive males in this study, conceptions

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).
occurred during periods characterized by low and
has been focused on defining female reproductive high testosterone concentrations, but males had little
physiology [6,9,14]. While equally important for the competition for access to estrus females. Since
development of effective reproductive management increased libido caused by elevated testosterone may
plans, little information has been collected on male be important for establishing dominance over
reproduction. The present study provides new, potential competitors, seasonal variations in
extensive information on serially collected serum testosterone may reflect a situation in the wild where
testosterone concentrations from multiple maturing elevated concentrations are associated with seasonal
and adult males, and seasonal semen production. In variations in the geographic availability of females.
contrast to patterns of testosterone secretion with Recent evidence suggested that cortisol increases in
prolonged nadir concentrations and clear periods of response to seasonal environmental stressors (i.e.,
peak elevation observed in seasonally reproductive reduced air and/or water temperatures) may be
delphinids (spinner dolphin, Stenella longirostris associated with mild seasonal changes in reproductive
[15]; Pacific white-sided dolphin, Lagenorhynchus hormone concentrations [17].
obliquidens; Robeck unpublished), and similar to Olesiuk et al. [3] predicted that the beginning of
those with less defined seasonal testosterone secretion testosterone production (initiation of puberty)
that produce spermatozoa throughout the year responsible for the increase in HWR of the dorsal fin
(bottlenose dolphin, Tursiops truncatus [16]), probably occurred 2–3 years prior to sexual maturity
testosterone concentrations from adult male killer (and HWR of 1.4). Using this assumption, their
whales (>13 years) always remained above 1 ng/mL predicted age of puberty for killer whales (range 7.5–
and demonstrated periods of elevation (spring to fall). 14.5 years) was similar to our estimations based on
Despite these apparent seasonal rhythms in serum testosterone concentrations (range 8–12 years).
testosterone secretion (particularly within each Males were reported to attain sexual maturity at a mean
animal), sperm production did not exhibit an obvious age of 14.5 years [3], which is approximately 1.5 years
seasonal change. Thus, it appears that even during older than when known age animals attained the HWR
periods of relatively low testosterone secretion, of 1.4 in the present study. When classifying males as
spermatogenesis is maintained. These findings were 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 for semen collection. We thank Dr. J.K. O’Brien for
not always observed. In fact, one male had an HWR of editorial comments and Steve Clark for growth data.
1.4 as early as 2 years after the onset of puberty, We also recognize the technical support provided by
corresponding to 2 years prior to sexual maturity Karen Steinman and Kendall Mashburn in conducting
(based on serum testosterone). Although HWR may be endocrine analyses. We thank Brad Andrews, Jim
useful for generalizations about a population, one must McBain and Thad Lacinak for their consistent support
consider that dorsal fin growth rate may vary among for this research. This project was funded by SeaWorld
individuals prior to the influence of serum testosterone. Corporation and is a SeaWorld Technical contribution
Potential factors influencing the age at which an Number 2004-01-T.
animal reaches HWR of 1.4 include genetic differences
in growth rate, the final adult size of the body and References
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