Animal Reproduction Science 124 (2011) 184–193

Contents lists available at ScienceDirect

Animal Reproduction Science

journal homepage: www.elsevier.com/locate/anireprosci

Reproductive cycles of marine mammals夽

P. Pomeroy
NERC Sea Mammal Research Unit, University of St Andrews, St Andrews KY16 8LB, UK

a r t i c l e i n f o a b s t r a c t

Article history: Marine mammals conform to the general mammalian reproductive system centered on
Available online 24 September 2010 the hypothalamic–pituitary–gonadal axis. Most marine mammals are long-lived and of
large body size with lesser reproductive rates than many other animals, a consequence of
Keywords: their interaction with the marine environment where the demands of acquiring resources
Marine mammal from the ocean must be balanced with the need for bearing offspring in a suitable place
Seals
for survival. The degree of spatial and temporal separation of these life history phases in
Whales
many species is a key feature of their ecology. The reproductive physiology of pinnipeds,
Dolphins
Reproductive cycles cetaceans, sirenians, sea otters and polar bears has been more thoroughly characterized for
the more accessible species.
Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.

1. Introduction as of ecological imperatives. This review includes a com-

plex and varied group of species (Table 1). Thus while an
Current knowledge of the reproductive cycles of marine obvious difference among the subjects under consideration
mammals has been acquired necessarily from relatively is whether they are totally or partially aquatic, reproduc-
few species, sometimes from few individuals and conse- tive similarities between the pinnipeds, polar bears and sea
quently descriptive generalizations are the norm. However, otters betray their carnivore origin, while the major life his-
there are important differences in comparative anatomy tory differences between the toothed and baleen whales
and physiology even in quite closely related species. The reflect at least to some extent whether or not reproduc-
group conforms to the general mammalian reproduc- tion is tied intimately to seasonal or annual migrations.
tive system of the hypothalamic–pituitary–gonadal axis. Similarly, reproductive differences between manatees and
A reproductive cycle is defined as the normal time for a dugongs are partially explained by the ways in which they
female to reproduce, i.e. to complete the processes associ- interact with their environments. The fact that most marine
ated with a fertile oestrus, ovulation, conception, gestation, mammals are long-lived and of large body size with lesser
birth and lactation. Environmental, nutritional or social reproductive rates than many other species is also linked
influences may affect the timing of this cycle, such that to the need to balance the demands of acquiring resources
the consequences of one breeding episode may be appar- from the ocean with the need for bearing offspring in a suit-
ent subsequently (Arnbom et al., 1997; Boyd et al., 1999; able place for survival. The degree of spatial and temporal
Pomeroy et al., 1999; Reijnders et al., 2010). separation of these life history phases in many species is a
It is impossible to separate a reproductive cycle from key feature of their ecology (Table 1).
its context, therefore, the issues of when, where and how
much breeding occurs is as much a function of phylogeny 2. Pinniped reproductive cycles

Pinniped female reproductive cycles are characterised

夽 This paper is part of the special issue entitled: Reproductive Cycles of by a period of delayed implantation, during which devel-
Animals, Guest Edited by Michael G Diskin and Alexander Evans. opment of the blastocyst is either very slow or negligible.
E-mail address: pp6@st-andrews.ac.uk In pinnipeds, as in ursids and mustelids, delayed implanta-

0378-4320/$ – see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.anireprosci.2010.08.021
 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193 185

Table 1 and behavioural components. The following description is

Classification and examples of marine mammals.
based on pinnipeds for which most information is avail-
Order Family Examples able (Table 2), obvious contrasts with other groups are
Carnivora
highlighted. Greater maternal plasma concentrations of
Pinnipedia Phocidae Earless seals, e.g. oestrogens at parturition (>30 pg/mL in northern fur seals)
elephant, hooded, grey, decrease rapidly and then increase rapidly, as cells in the
harbour seals ovary secrete oestrogens, which together with decreas-
Otariidae Eared seals, e.g.
ing concentrations of progesterone are likely the stimulus
northern fur seals,
Steller sea lions for hypothalamic GnRH secretion, LH and FSH production,
Odobenidae Walrus allowing an ovarian follicle to mature. While phocids such
Ursidae Polar bear as grey seals begin follicular recruitment from the pool
Mustelidae Sea otter of immature ovarian follicles around parturition, taking
Cetacea
Mysticeti Balaenopteridae Blue, fin, minke
around 14 days to mature, northern fur seals Callorhinus
Eschrichtiidae Gray whale ursinus may take 5 months for a similar process to occur.
Balaenidae Southern right whale This difference is probably directly related to the rela-
Neobalaenidae Pygmy right whale tive functional activity of phocid and otariid corpora lutea.
Odontoceti Delphinidae Orca, beluga
Rapid follicular growth ends with follicle maturation and
Phocoenidae Porpoises
Monodontidae Narwhal, beluga ovulation as the epithelium of the ovary thins and rup-
Pontoporidae Franciscana tures. The process of follicular maturation and the secretion
Liptotidae Baiji of large quantities of oestrogen by the theca interna sur-
Iniidae Boto rounding the mature follicle marks the onset of oestrous
Plantanistidae Indian river dolphin
Ziphidae Beaked whales
behaviour in the female. The ovum is released and col-
Kogiidae Pygmy sperm whale lected by the fimbria into the oviduct where fertilization
Physeteridae Sperm whale normally occurs. A conceptus migrates around the uterine
Sirenia horn before implantation and placentation occurs, but once
Trichechidae Manatees
implanted, active gestation begins. The follicle that pro-
Dugongidae Dugongs
duced the ovum released at ovulation continues to develop
tion appears to be obligate. It has been suggested that the into a corpus luteum. The lining of granulosa cells in the
period of delayed implantation confers flexibility of tim- matured follicle secretes steroid precursors of the hor-
ing of parturition on females and is most closely controlled mones produced by the corpus luteum. The empty vacuole
by photoperiod. Neurological transduction of stimuli in the of the ruptured follicle is quickly filled by expanding luteal
brain appears to be centered in the hypothalamus, but the cells. Progesterone produced by the corpus luteum, which
physiology of delayed implantation is less clear (for further may eventually occupy a large portion of the ovary, is nec-
details see Boyd et al., 1999). essary in controlling pregnancy along with placental and
Most species are thought to implant during a decreasing pituitary hormones (but see below). Hilar rete glands have
photoperiod. Photoperiodic response may be controlled by been observed in grey and ringed seal ovaries and although
periods of receptivity when exposure to light or dark may most abundant during delayed implantation, their function
define endocrine response. Pinnipeds are thought to be par- is not known (Boyd, 1984).
ticularly receptive to blastocyst reactivation when they are Ovulation tends to occur in pinnipeds from alternate
exposed to a particular day length, during decreasing day ovaries at successive oestrous episodes. Follicular growth
length (Temte, 1991). Harbour seals showed a decreased in the ovary from which ovulation does not occur may
pituitary sensitivity to LH during winter and spring, con- be inhibited by local or paracrine activity from the adja-
sistent with photoperiod control (Gardiner et al., 1999). cent uterine horn containing the current pregnancy. Thus
Nutritional state is also an important factor which may ovulation and implantation tend to occur contralaterally,
impact reproductive patterns (Boyd et al., 1999). although this is not always the case. In contrast, in most
odontocetes ovulations occur more frequently from the left
2.1. Oestrus ovary until later in life when ovulation from the right ovary
predominates (Slijper, 1949).
Oestrus is the state of receptivity to mating that a female Most pinnipeds that have been studied are function-
enters during the reproductive cycle. It has physiological ally monoestrus. Oestrus occurs postpartum either during

Table 2
Reproductive Characteristics of three species of Pinnipeds.

Reproductive characteristics Harbor seal (Phoca vitulina) California sea lion (Zalophus californianus) Walrus (Odobenus rosmarus)

Pupping period Early May Late may, early June Mid-April to mid-June, peak May
Timing of ovulation End of lactation Approx. 28 days postpartum Mid-lactation
Conception June Late June, early July January–March (peak February)
Duration of lactation 21–42 days 6–12 months 24+ months
Delayed implantation period July–August July–September March–July
Delayed implantation 1.5–3 months 3 months 4–5 months
Postimplantation gestation September–May October–May August–May
Total gestation interval 11 months 11 Months 15 months
 186
Table 3
Breeding characteristics for major cetacean species (adapted after tables 6-9, 6-10 in Boyd et al., 1999).

Species Location Peak month(s) of Gestation Peak months of birth and Lactation Length at Mean lengths (m) and ages at sexual maturity
conception period length of neonate (m) duration weaning (m)
(months) (months)

Male Female Age (year)

Blue Antarctic + South June/July 11 May; 7.0 7 12.8 22.6 24.0 5

Africa
Pygmy Blue Antarctic Two seasons; <12? Main: March–April ? ? Ca. 18.9 19.2 Ca. 5–6
main:
February–April
Compl.: Compl.:

P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193

October–January? November–January? 6.3
Fin Antarctic (all June/July 11 May; 6.4 7 11.5 19.0 20.0 10 ⇒ 6 or 7
areas) + south
Africa
North Atlantic December? 11? November? ?6–7 ? 16.8–17.6 17.7–19.1 11 ⇒ 8
North Pacific. December 11–12 November/December; 6.4 ? ? 17.6–17.7 18.3–18.6 8–12
Sei Antarctic (all July >10.75 June; 4.5 6 8.0 13.6 14.0 11 ⇒ 8
areas) + South
Africa
North Atlantic November–February >10.5 November/December; ? ?6 ? 12.9 13.3 8
North Pacific:
(West) October–November 12–13 November/December; ? 7 ? 12.8 13.3 10 ⇒ 6
(East) October–November 10 November; 4.4 9 9.0 12.9 13.4 10
Minke Antarctic + South August/September 10 May/June; 2.8 4 4.5 7.2 8.0 14 ⇒ 6 or 7
Africa + Brazil
North Atlantic February 10 December; 2.6 <6 Ca.4.5–5.5 6.9 7.3–7.45 7.3
North Pacific February/March 10 December/January; 2.8 ?6 ?4.6 6.9 7.3 ?
Huanghai Sea July–September 10–11 May–July; 2.5–2.7 ? ? ? 6.6–7.0 ?
Bryde South Africa
(Inshore) Year-round 12 Year-round; 3.96 6? Ca. 7.1 12.0
(Offshore) March 12 February/March; 3.96 6? Ca. 7.1 (13.0) 12.5 Ca. 10
North Pacific (12.0) 8–11
(Costal Japan) Mainly December ?12 ?November but protracted; ? Ca. 7.1 11.9 12.0 9
but protracted. 3.95
(Pelagic) Protracted ? Protracted; >3.95 ? ? 11.9 12.0 10 and 8
South Pacific (two Protracted ? Protracted; <4.15 ? ? 11.6–12.4 12.2–12.8 10
stocks)
Humpback Antarctic + Australia July/August 11.5 July/August; 4.3 10.5–11 8.8 11.5 12.0 4 or 5 (x2)
North Pacific:
(West) February 10–11 January; 4.1 10–11 or 12 Ca. 8.0 11.6 11.7 8
(East) Ca. 12
Grey North-eastern December 13.75 January–February; 4.6 7 8.5 11.1 12.2–14.0 4
Pacific
Table 3 (Continued )

Species Location Peak month(s) of Gestation Peak months of birth and Lactation Length at Mean lengths (m) and ages at sexual maturity
conception period length of neonate (m) duration weaning (m)
(months) (months)

Male Female Age (year)

Bowhead Arctic May Ca. 12–13 April/May; 4.5 5–6 6.1 11.6 ? ?
Pygmy Right Southern ?Probably Ca. 12 Probably extended? ?5–6 Ca. 3.2–3.6 13.0–16.0 13.0–16.0 ?
Hemisphere extended
Ca. 1.6–2.2
Right Southern August/October 10 May/July; 5.5 ? ?
Hemisphere, south
Africa + South
America

P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193

Northern ? 10 August; 6.1
Hemisphere
?; 4.4–4.8
Sperm Whale Southern October–December 15–16 February–March; 400 >2 670–760 12.5–13.7 8.7 19 male; 9
Hemisphere female
White Whale W. Greenland May–June >11 April–May; 160 ? ? 3.9 3.45 6–7 male; 4–7
(Beluga) male
Pilot Whale Northeast Atlantic June 12 May–August; 177 3.67 ? 4.94 3.75 14.3 male; 8.7
(long-finned) (May–September) female
Pilot Whale Northeast Pacific August–January 14.5–16 December–January 185 2–2.78 ? 5.6 3.95 16.5 male; 8.5
(short-finned) female
Killer Whale Northern Japan
Northeast Pacific ? 17; (12–15) October–March; 246 Ca. 1.0 ? 5.8 4.6–4.9 14–15 (both)
Northeast Atlantic October–December 17; (12–15) December–?; 208–220 <3.0? ? 5.8 4.6-4.9 15 male; 8
female
False Killer Northeast Atlantic ? 15.5 ?; 193 1.5 ? 5.32 4.47 16 male; 17
Whale female
Bottlenose Northwest Atlantic Spring through 12 March–June; 115 1.6 ? 2.58 2.39 10–15 male; ca.
Dolphins June 10 female
Striped Northwest Pacific Two Peaks: 12 Summer and winter; 100 0.67–1.67 ? 2.27 2.2 14 (both)
Dolphin Summer and
Winter
Harbour Bay of Fundy June–August 10.6 Mid-May; 78 0.65–0.75 Ca. 115–118 ? 1.43 3.15–3.44
Porpoise Canada (both)
Northwest USA, June–August Ca. 10 May–July; 80–86 ? ? 1.3–1.49 1.42–1.52 4.6 (both)
California
British Isles June–August 10–11 June–July; ca. 70 ? ? >1.30 >1.40 3–4 (both)
West Baltic July–August 11 June–July; 75 0.67 ? ? ? ?
Norway ? Ca. 10 May–July; 75–86 0.67 ? ? ? ?
Dall’s Porpoise Costal Japan Mid-August–late- 11.4 August–September; 99.7 0.5–3.5 (av. ? 1.76–1.87
October peaking in 2.07)
September
North July and August 11 Late-August; 100 Ca. 2.0 ? ? ? ?
Pacific + Bering Sea

187
188 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193

(grey and elephant seals) or after lactation (harbour seals). 3. Cetacea

Many otariids have a relatively early postpartum oestrus
4–14 days after birth, but a few species including the Cetaceans can be classified either as baleen whales (all
Steller sea lion – Eumatopias jubatus, Galapagos fur seals large bodied filter feeders) or odontocetes (toothed whales
– Arctocephalus galapagoensis and California sea lions – ranging in size from large sperm whales to small por-
Zalophus californianus do not enter oestrus until mater- poises).
nal foraging trips begin. In the case of California sea lions, Much of the early basic biology available came from
this means around 4 weeks after giving birth. Walrus – commercially caught species and the efforts of biologists
Odobenus marinus – are unusual in that they have two to clarify the reproductive cycles and life history character-
oestrus periods within a year. Walrus gestation is around 15 istics provided crucial data for regulatory purposes. More
months. Mothers have an initial oestrus around 4 months recently, long term mark-recapture studies and work with
after giving birth when relatively few reproductively active captive animals has begun to yield data on the smaller
males are present, followed by a second oestrus about 6 species. The difference in sources of data is important for
months later, coinciding with the peak of male mating interpretative purposes (Murphy et al., 2009). As with pin-
activity. It is not known what function the early oestrus nipeds, the relationships of species with their environment,
event serves or whether animals are fertile at this time. particularly the need for food and the movements they
Hawaiian monk seals exhibit polyoestrus activity (Iwasa make to find food, defines much of their ecology (Table 3).
and Atkinson, 1997), possibly related to their sub-tropical Because of the range of strategies seen throughout the
habitat and less well defined seasonal reproductive cycles. group, large variations exist even within families. Infor-
Phocid seal species tend to exhibit oestrus in late lac- mation for general patterns may serve only as guidelines.
tation, but as lactation varies in duration from as little as Structural and size variations are also huge – even though
4 days in hooded seals – Cystophora cristata – to 5 months whales tend to be thought of as very large mammals, the
in Mediterranean monk seals – Monachus monachus, there ovaries of the baleen whales are relatively small, weigh-
is considerable variation in the occurrence of oestrus ing several kilograms, while those of a porpoise may weigh
(Table 2). The literature is equivocal on the exact relation- several grams (Lockyer, 1984a).
ship between the timing of birth and oestrus in pinnipeds. Cetacean oestrous cycles vary greatly. In odontocetes, an
The timing and duration of oestrus defines the males ovarian follicle matures, releasing an ovum from the ovary
that are candidates for paternity of the next offspring. On and the corpus luteum develops at the site of ovulation.
average, selective pressures ensure that male competition The corpus luteum regresses gradually if fertilization does
and/or female choice should be maximized at oestrus. The not take place, but maintains its progesterone-secreting
duration of oestrus is difficult to measure in wild animals, function if a viable pregnancy is established. Irrespective
but by observing copulations it has been estimated to vary of fertilization, the corpus luteum eventually regresses to
from hours in some otariids to up 2 weeks in the north- form a small white or grey area called the corpus albicans.
ern elephant seal – Mirounga angustirostris. It is unclear At the site of each ovulation, a permanent scar develops at
whether females remain fertile within these longer periods the site from where ovulation occurred, normally visible
of oestrus or if there are other behavioural complications on the surface of the ovary. A number of pieces of evidence
which make females receptive during this time. suggest that these bodies remain throughout the animal’s
It is notoriously difficult to estimate the serial reduc- life and thus the total number of ovulations, most of which
tion in percentage of previously parous females implanting, result in pregnancies, should be apparent by careful inspec-
pregnant at various stages and eventually giving birth, for a tion of cetacean ovaries (Laws, 1961; Ivashin, 1984; Marsh
wild population particularly in marine mammals. A recent and Kasuya, 1984). Cetacean corpora albicantia are thus
development has seen the use of ultrasonic examination of unusual as in most other mammals they are gradually
female northern fur seals around the time of implantation, resorbed. It has been suggested that corpus albicans regres-
along with serum hormone measurements to determine sion slows during active pregnancy because of the effects of
pregnancy and timing of implantation with a greater accu- hormones, although it is not clear why these structures fail
racy than possible previously (Adams et al., 2007; Testa to regress fully as in other mammals. Accessory corpora
et al., 2010). lutea may be found in the ovary ipsilateral to pregnancy.
Sea otters Enhydra lutris are thought to have oestrous Ovaries may also contain other structures such as corpora
periods following weaning, of several days, based on mat- atretica, corpora aberrantia, and cystic follicles, as well as
ing observations. It has been suggested that ovulation is cysts of unknown aetiology (Laws, 1961; Perrin and Myrick,
induced by mating in this species, as it is in mustelids. There 1981; Kasuya and Marsh, 1984; Lockyer, 1984a, 1987b;
is also evidence that sea otters are polyoestrus – females Lockyer and Smellie, 1985; Boyd et al., 1999). As many
that fail to conceive initially return to oestrus until they cetaceans have regular seasonal ovulations this provides a
become pregnant. method for estimating an animal’s age (after maturation).
Less is known about oestrus in polar bears – Ursus This is especially true of baleen whales. Observations from
maritimis. They are seasonal breeders and females enter animals stranded or trapped provide compelling evidence
oestrus during this time (March–May). Observations sug- that for those species at least ovulation is spontaneous
gest that “courtship behaviour” may be necessary for (minke whale, Marsh, 1985).
ovulation and that oestrus occurs over a period of days. Examination of the larger cetacean species’ ovaries is
Individual females tend to bear young at intervals of 2 or 3 helped by their size: a blue whale corpus lutem in preg-
years. nancy may average 137 mm in diameter and weigh several
 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193 189

hundred grams, while that of the minke whale may aver- tive tissue on either side of the ventral midline. Offspring
age 66 mm in diameter and weigh 156 g (Lockyer, 1984b). are suckled at two mammary slits positioned ventrally on
Using the minke whale as an example, a short time after either side of the midline just forward of the vulva, each of
parturition the corpus luteum may have diminished to which contains a nipple. Cetacean milk is thick and creamy,
less than 40% of its original size during pregnancy. It will may appear yellowish and has a high fat content ranging
then continue to regress to about 25% of its original size from 14 to 53% (Lockyer, 1984a, 1987a, 1993). Lactation
within a few years of pregnancy (Lockyer, 1987b). Some and suckling together will suppress oestrus in cetaceans
whale species may be long-lived (>100 years) and although but not in pinnipeds (Robeck, 1996; Robeck et al., 2001).
the ovaries may remain active throughout the lifetime of
the female, there is evidence that in some species such 3.1. Hormonal evidence of pregnancy in cetaceans
as short-finned pilot whales (Globicephala macrorhynchus)
reproductive senescence may occur in females older than In a study of belugas Delphinapterus leucas, circulat-
50 years (Marsh and Kasuya, 1984). Social factors have been ing concentrations of testosterone, progesterone, estrogen,
implicated in such phenomena. and prolactin were measured as well as in urine (Hoier
In baleen whales the left and right ovaries appear to be and Heide-Jorgensen, 1994). Mature males typically had
fully functional from the onset of maturity with little or over four times the concentrations of testosterone as
no evidence of biased activity of one side compared to the immature males (4.14 nmol/L compared to 0.96 nmol/L
other (Lockyer, 1987b). However many odontocetes have testosterone). Pregnant females had concentrations of
distinct bias in ovarian activity, with the left ovary show- progesterone that were 15 times greater than juveniles
ing most ovulatory activity at least in the early stages of or non-pregnant individuals (29.1 nmol/L compared to
reproductive life and activity in the right ovary becom- 1.76 nmol/L progesterone). Concentrations of oestrogen
ing apparent only after a number of ovulations have taken in pregnant females were similarly elevated (2.43 nmol/L
place (Slijper, 1949) or the left ovary becomes dysfunc- compared to 0.37 nmol/L in non-pregnant females and
tional through damage or disease (e.g., short-finned pilot juveniles). Concentrations of prolactin were also greater
whales, Marsh and Kasuya, 1984). in lactating females compared to in non-lactating females
Endometrial development occurs in parallel with ovar- (4.35 and 1.97 nmol/L respectively). Recent hormone mea-
ian development, and is greatest during ovulation and surements have been made on minke whales captured
pregnancy (Lockyer and Smellie, 1985). The endometrium in the Antarctic comparing information from direct ovar-
and myometrium decrease in thickness and glandular ian and gross inspection with blood hormone assays to
activity during lactation. Hormonal effects on the devel- determine the reproductive status of females (Iga et al.,
opment of the cetacean endometrium are well defined 1996). Concentrations of progesterone were 4.3–4.5 ng/mL
and cyclical (Mathews, 1948). The stratum spongiosum of in pregnant and ovulating females, and concentrations
the mature, ovulating, and subsequently pregnant female of oestradiol were 8.7 pg/mL in pregnant and 13.8 pg/mL
have an increase in glandular presence, size, and activ- in anestrous females. Juveniles had no detectable pro-
ity which is clearly different to immature and anestrous gesterone and their concentrations of oestradiol were
females (Lockyer and Smellie, 1985). The overlying stra- about 7.4 pg/mL. Measurements of progesterone concen-
tum compactum becomes increasingly vascularised and trations in blubber samples from by-caught dolphin species
the surface develops numerous frond-like projections as were able to distinguish pregnant (elevated concentra-
pregnancy proceeds. In lactating females, the endometrium tions; mean 261 ng/g) from non-pregnant animals (mean
becomes thin, less glandular, and has a smoother and less 15.2 ng/g) and thus biopsy samples were suggested as
perfused stratum compactum (Lockyer and Smellie, 1985). viable indicators of pregnancy state (Kellar et al., 2006).
During pregnancy the developing embryo attaches via In captivity, it is possible to perform longitudinal mea-
the placenta and umbilical cord both of which are com- surements of circulating hormones in a non-destructive
pletely lost during parturition. At parturition the uterus manner. Robeck et al. (1994) found that when serum
collapses, while myometrial constriction of blood vessels concentrations of progesterone in bottlenose dolphins
and clotting arrests bleeding. No further bleeding or uter- (Tursiops truncates) decreased from more than 3 to
ine shedding occurs. Placental scars have not been found in <1 ng/mL within 1 month, ovulation had occurred and
the cetacean uterus, consequently these are not available that subsequently if concentrations >3 ng/mL were sus-
to indicate or estimate frequency of previous pregnancies. tained, pregnancy had occurred. “Noncycling” female
Observations of cetacean births had been few in the wild bottlenose dolphins averaged circulating concentrations of
but are increasingly frequent from advanced observational 0.286 ng/mL progesterone and 25 pg/mL oestrogen. In the
and tracking studies as well as from captive groups. Partu- same study, Robeck et al. (1994) suggested that bottlenose
rition is signaled by a period of uterine contractions, which dolphins were spontaneous ovulators, whose oestrous
have been observed in captive dolphins, and enlargement cycle spanned 21–42 days. However, there is evidence
of the vulval opening. Most offspring are born tail first that ovulatory cycles may occur at irregular periods and
(Slijper, 1949) and the mother often flexes her body during a seasonal reproductive component may be present. Sea-
the birth process. sonal polyoestrus and 1–2 years of anoestrus followed by
Lactation in cetaceans may be an extended process. polyoestrus may also occur. Female bottlenose dolphins
Bottlenose dolphins and beluga may nurse offspring for also show evidence that some cycles are associated with
up to 36 months. Cetacean mammary glands are elongate a lack of fertility, this is consistent with a lesser than aver-
narrow flat organs extending in the subcutaneous connec- age pregnancy rate in the younger age classes of mature
190 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193

females. Studies that relate known reproductive histories Wild dugongs probably mature several years later than
to histology, eg in captive animals, indicate that while cor- Florida manatees. The youngest female dugong with cor-
pus albicantia may correspond with known pregnancies, pora lutea or corpora albicantia present was a 0.5-year-old
number of ovulations is much more difficult to discern nulliparous female from Townsville, Australia. All females
(Brook et al., 2002). A female’s first births can often result in aged 10 years or older were parous with at least one pla-
early offspring mortality. The calf may die as a result of the cental scar present (Marsh et al., 1984a,b). However, age
parent’s inexperience and/or difficulties during parturition at primiparity varied widely, three females from Morning-
(Bryden and Harrison, 1986). ton Island, Australia were still nulliparous at 15–17 years,
although two of these animals had corpora lutea or corpora
albicantia (Marsh et al., 1984b).
4. Sirenia The gestation period of Florida manatees is estimated
to be 12–14 months for captive animals (Odell et al.,
Sirenians have a gestation period of 12–14 months, with 1995) Field observations also suggested gestation periods
an extended lactation period that can last at least 1.5 years. of between 12 and 14 months. Marsh’s (1995) estimate
In dugongs, ovulation may not be suppressed by lactation. of the dugong gestation period (13.9 months) relied on
Similar to sea otters, after weaning offspring, females show a number of assumptions but remains the most reliable
evidence of a polyoestrous cycle. There is also evidence estimate available. Dugongs and manatees are large, long-
that fecundity rates may be poor. No evidence of pregnancy lived animals with maximum estimated life spans of 73
or lactation was found in 33 and 56% of ovaries examined years for dugongs (Marsh, 1995) and 59 years for mana-
from manatees and dugongs, respectively. The duration of tees (Marmontel et al., 1996). There is currently no strong
oestrus has been inferred from behavioural evidence, as evidence of reproductive senescence in either female and
being likely to be prolonged and possibly induced. male sirenians (Marsh and Kasuya, 1986).
Reproductive information for the four extant species Sirenians do not breed continuously. Interbirth intervals
of sirenians is minimal, but summarized in Table 4 (after have been estimated between 2.5 and 5 years for man-
Boyd et al., 1999). The Florida manatee (Trichechus mana- atees, with a larger upper limit of 6.8 years for dugongs
tus latirostris), is the best studied sirenian and data come and there is some evidence that reproductive cycles may
from captive studies, observations in the wild and post- be condition-dependent (Boyd et al., 1999). Mature folli-
mortem examinations. Information on dugongs has been cles and/or corpora lutea were absent from ovaries in 9 of
assembled mostly from postmortem studies supplemented 27 mature manatees and 13 of 25 mature female dugongs
by behavioural observations. whose ovaries were examined histologically and that were
Sirenian testes are permanently situated in the abdom- neither pregnant nor lactating. While female reproductive
inal body cavity. Reproductive gross morphology of activity in a population is not closely synchronised, some
male dugongs and manatees has more in common with evidence of seasonality has been recorded. The ovaries of
cetaceans than elephants and hyraxes (Marsh et al., 1984a). Australasian female dugongs were more likely to contain
However, the reproductive anatomies of female sireni- follicles or corpora lutea in winter/spring than in sum-
ans and African elephants (Loxodonta africana) have many mer/autumn (Marsh et al., 1984b; Marsh, 1995).
similarities, including typical corpora lutea and corpora Captive Florida manatees showed mating behaviour
albicantia counts, a zonary placenta that scars the uterus throughout pregnancy, suggesting that females mate even
conspicuously in dugongs but unreliably in manatees, the when they are not fertile (Odell et al., 1995). Although such
gross uterine morphology, and the nature of histological behaviour may be an artifact of captivity, similar observa-
changes in the endometrium. tions have been recorded of mating in herds in winter when
In Sirenians ovulation scars are generally small and at least some males are probably not spermatogenic. Obser-
difficult to detect. Luteinised (non-ovulated) follicles are vations of free-ranging and captive animals and necropsy
generally easier to distinguish from corpora lutea in studies indicate that very few calves are born to free-
cetaceans than in sirenians (Marsh, 1984). As a result, it ranging or captive Florida manatees in the winter months
is extremely difficult to assess sexual maturity in sirenians (Odell et al., 1995). Births have been recorded throughout
based on inspection of ovaries. Dugongs and manatees have the remainder of the year in Florida, but calving peaks in
been described as polyovular (Marsh et al., 1984a) such that spring and early summer, similar to that for the dugong in
associated with each pregnancy is a large and variable num- Australasia.
ber of presumed corpora lutea. These presumed corpora
lutea also vary in size (Marsh et al., 1984a). In dugongs, 5. Pregnancy and pseudopregnancy
only some of the “corpora lutea” show stigmata suggest-
ing follicular rupture. As bodies classed as corpora lutea or 5.1. Pinnipeds
corpora albicantia may include luteinised follicles and asso-
ciated scars, ovulation is difficult to confirm from ovarian Pinniped pregnancies comprise five important steps;
examination in non-pregnant, nulliparous female sireni- conception, delayed implantation, embryo reactivation and
ans. Nulliparous Florida manatees and dugongs may have implantation, foetal development and parturition. Otariids
several oestrous cycles before they first conceive. Although appear to have an obligate pseudopregnancy after ovula-
the normal litter size is one, many instances of twins have tion, irrespective of the presence of a normal blastocyst
been recorded in wild and captive manatees (Boyd et al., (Boyd, 1991a,b; Atkinson, 1997). Nevertheless, the changes
1999). associated with an actual pregnancy including placental
 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193 191

Table 4
Characteristics of the ovaries, uteri, and mammary glands of female sirenians in different stages of reproduction.

Stage Ovaries Uterus Mammary

glands

Immature, prepubescent Smooth and flattened surface with Glands undeveloped, lumen small, Inactive
numerous small follicles blood supply underdeveloped
Immature, maturing Several LGF Early proliferation endometrium, Inactive
size inter-mediate between
juvenile and adult
Sexually mature, nulliparous CL and/or CA present may have Adult sized, no PS Inactive
several LGF
Parous CA present, may have LGF or CL At least one PS (dugong only) Active or
inactive
Ovulating Luteal: LGF and CL Secretory endometrium with or Inactive or
without PS. Not pregnant active
Pregnant CL present, may have CA Embryo or fetus present, secretor Usually
endometrium inactive but
may be active
Lactating Recent CA Secretory endometrium. Recent PS Active
present
Resting CA but no LGF or CL Involving endometrial glands, PS Inactive
present or absent

CA, corpora albicantia; CL, corpora lutea; LGF, large Graafian follicle; PS, placental scar.

formation which occur after the 4 month delayed implan- inter-specific variation in these mechanisms will provide
tation period are dependent on the presence of a viable interesting information in the future.
blastocyst. It is not known at what point maternal recogni-
tion of pregnancy occurs. 5.2. Cetacea
The fetal–placental unit’s role in hormonal control
of pregnancy has been questioned. Previously, it has Pseudopregnancy has been observed in several species
been thought that placental gonadotrophin functions of delphinids. Killer whales, in captivity, tend to exhibit this
through fetal gonads to stimulate placental production after have several oestrous cycles without conceiving and
of oestrogens and progesterone, maintaining pregnancy it is thought that this route to pseudopregnancy would be
and eventually initiating parturition. Fetal adrenals and unlikely to occur in the wild (Robeck et al., 2001). Pseu-
gonads are often of a similar size at birth to the adult dopregnancy generally occurs after early embryonic loss
organs because of hormonal hypertrophy. However, lon- when maternal recognition of pregnancy has occurred.
gitudinal monitoring of serum hormone concentrations in
captive northern fur seals over 2 years showed that pro- 6. Male reproductive cycles
gesterone concentrations for non-pregnant animals cycled
similarly to those of pregnant animals. Greater concentra- 6.1. Pinnipeds
tions of progesterone (20–30 ng/mL) in July are reflective
of ovulation, dropping to 5–10 ng/mL in August–October Pinniped breeding seasons are typified by being short,
during delayed implantation, before increasing again to synchronous and seasonal, but there is evidence that this
25–35 ng/mL in November (Kiyota et al., 1999). These pro- is a consequence of synchrony with female reproductive
files matched those seen in wild animals, but only two patterns. Gross measures of male reproductive capacity
of the seven profiles were accompanied by a pregnancy, such as testicular mass, plasma concentrations of testos-
suggesting that the obligatory pseudopregnancy extends terone and the presence of sperm in testes or epididymides
beyond the period of normal implantation. In effect this have indicated that potentially fertile male grey and south-
means that maintenance of the corpus luteum, in northern ern elephant seals may reside in the presence of females
fur seals at least, is not dependent on maternal recognition over a much longer period than the apparent breeding
of pregnancy or an embryonic-derived component. The season. However, there is also some indication that an
presence of circulating progesterone may also indicate that additional behavioural component is important for mat-
the corpus luteum is still active in late gestation. However, ing and successful fertilization in these species (in Boyd,
in a phocid seal (Phoca vitulina; Reijnders, 1990; Atkinson, 2009). Elevated circulating concentrations of testosterone
1997) hormonal data suggest that pseudopregnancy, as are associated with increases in diameter of seminiferous
indicated by circulating concentrations of progesterone, tubules and epididymis, although spermatogenesis tends
only occurs up to the end of delayed implantation in to occur 1–3 months after increases in concentrations of
non-pregnant seals. Non-pregnant walrus have also have testosterone. Reductions in gonad mass and activity are
increased concentrations of progesterone (>3 ng/mL) over thought to be produced by concurrent reductions in the
long periods in captivity. Hobson and Boyd (1984) sug- anterior pituitary cells responsible for gonadotrohpin pro-
gested that placental gonadotrophins were required for duction. Significant seasonal decreases in pituitary release
corpus luteum function in some seal species. It is likely that of LH in response to experimental GnRH administration
192 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193

in harbour seals supports this hypotheses (Gardiner et al., Bryden, M.M., Harrison, R.J., 1986. Gonads and reproduction. In: Bryden,
1999). M.M., Harrison, R.J. (Eds.), Research on Dolphins. Clarenden Press,
Oxford, pp. 149–159.
Gardiner, K.J., Boyd, I.L., Follett, B.K., Racey, P.A., Reijnders, P.J.H., 1999.
6.2. Cetaceans Changes in pituitary, ovarian, and testicular activity in harbour seals
(Phoca vitulina) in relation to season and sexual maturity. Can. J. Zool.
77, 211–221.
Males that are reproductively mature are thought to Hobson, B.M., Boyd, I.L., 1984. Concentrations of placenta gonadotrophin,
produce sperm, at least in quantity, only seasonally. Some placental progesterone and maternal plasma progesterone during
species have seasonal growth, hypertrophy, followed by pregnancy in the grey seal (Halichoerus grypus). J. Reprod. Fert. 72,
637–644.
atrophy of the testes. In a study of a captive colony of Hogg, C.J., Rogers, T.L., Shorter, A., Barton, K., Miller, P.J.O., Nowacek, D.,
Hawaiian spinner dolphins (Stenella longirostirs), a seasonal 2009. Determination of steroid hormones in whale blow: it is possible.
peak in circulating concentrations of testosterone in males Mar. Mammal Sci. 3, 605–618.
Hoier, R., Heide-Jorgensen, M.P., 1994. Steroid hormones and prolactin in
was reported by Wells (1984). More recently, measure-
white whales (Delphinapterus leucas) from West Greenland. Meddr.
ment of steroid hormones from blubber and even lung Grønland: Biosci. 39, 227–238.
mucosa exhaled in cetacean blows has been demonstated, Iga, K., Fukui, Y., Miyamoto, A., 1996. Endocrinological observations of
in attempts to gain information on reproductive status female minke whales (Balaenoptera acutorostrata). Mar. Mammal Sci.
12, 296–301.
from free-ranging individuals (Kellar et al., 2009; Hogg Ivashin, M.V., 1984. Characteristics of ovarian sorpora in dolphins and
et al., 2009). whales as described by Soviet scientists. Rep. Int. Whaling Commis-
sion (Special Issue 6), 433–444.
Iwasa, M., Atkinson, S., 1997. Analysis of corpora lutea to estimate repro-
6.3. Sirenia ductive cycles of wild Hawaiian monk seals (Monachus schauinslandi).
Mar. Mammal. Sci. 12, 182–198.
Mature male sirenian reproductive status has been Kasuya, T., Marsh, H., 1984. Life history and reproductive biology of
the short-finned pilot whale, Globicephala macrorhynchus, off the
assessed mainly from histological examination of the testes pacific coast of Japan. Rep. Int. Whaling Commission (Special Issue
and /or epididymides. Such studies suggest that not all of 6), 259–310.
the mature males in a population of Florida manatees or Kellar, N.M., Trego, M.L., Marks, C.I., Dizon, A.E., 2006. Determining preg-
nancy from blubber in three species of delphinids. Mar. Mammal Sci.
dugongs are producing spermatozoa continuously. Thus, 22, 1–16.
more than half of the pubertal and mature males from north Kellar, N.M., Marisa, L., Trego, C.I., Marks, S.J., Chivers, K.D., Archer, F.I.,
Queensland (n = 41) and mature male dugongs from Papua 2009. Blubber testosterone: a potential marker of male reproduc-
tive status in short-beaked common dolphins. Mar. Mammal Sci. 25,
New Guinea (n = 141) were infertile at the time of sampling.
507–522.
Spermatogenesis was asynchronous within a population Kiyota, M., Yamaguchi, Y., Nishikawa, F., Kohymama, K., 1999. Cytological
(Marsh et al., 1984a). Marsh et al. (1984b) suggest that indi- changes in vaginal smear and epithelium associated with the repro-
vidual males have periods of sexual inactivity followed by ductive cycle in northern fur seal, Callorhinus ursinus. Bull. Nat. Resour.
Inst. Far Seas Fish. 36, 17–25.
periods of sexual recrudescence and activity, and that some Laws, R.M., 1961. Southern fin whales. Discov. Rep. 31, 327–486.
males may be reproductively sterile either permanently or Lockyer, C., 1984a. Review of baleen whale (Mysticeti) reproduction and
over long periods. implications for management. Rep. Int. Whaling Commission (Special
Issue 6), 27–50.
Lockyer, C., 1984b. age determination by means of the earplug in baleen
Conflict of interest statement
whales. Rep. Int. Whaling Commission 34, 692–696.
Lockyer, C., 1987a. Evaluation of the role of fat reserves in relation to the
The author has no conflict of interest in publishing this ecology of North Atlantic fin and sei whales. In: Huntley, A.C., Costa,
review. D.P., Worthy, G.A.J., Castellini, M.A. (Eds.), Approaches to Marine Mam-
mal Energetics. Society for Marine Mammalogy, Special Publication
No. 1, Lawrence, KS, pp. 183–203.
References
Lockyer, C., 1987b. Observations of the ovary of the southern minke whale.
Sci. Rep. Whales Res. Inst. 38, 75–89.
Adams, G.P., Testa, J.W., Goertz, C.E.C., Ream, R.R., 2007. Ultrasonographic Lockyer, C., 1993. Seasonal changes in body fat condition of northeast
characterisation of reproductive anatomy and early embryonic detec- Atlantic pilot whales, and their biological significance. Rep. Int. Whal-
tion in the Northern Fur Seal (Callorhinus ursinus) in the field. Mar. ing Commission (Special Issue 14), 323–350.
Mammal Sci. 23, 445–452. Lockyer, C., Smellie, C.G., 1985. Assessment of reproductive status of
Arnbom, T.R., Fedak, M.A., Boyd, I.L., 1997. Factors affecting maternal female fin and sei whales taken off Iceland, from a histological exam-
expenditure in southern elephant seals during lactation. Ecology 78, ination of the uterine mucosa. Rep. Int. Whaling Commission 35, 343.
471–483. Marmontel, M., O’Shea, T.J., Kochman, H., Humphrey, S., 1996. Age deter-
Atkinson, S., 1997. Reproductive biology of seals. Rev. Reprod. 2, 175–194. mination in manatees using growth-layer-group counts in bone. Mar.
Boyd, I.L., 1984. Occurrence of hilar rete glands in the ovaries of grey seals Mammal Sci. 12, 54–88.
(Halichoerus grypus). J. Zool. (Lond.) 204, 585–588. Marsh, H., 1984. Terminology of reproductive morphology and physiology.
Boyd, I.L., 1991a. Changes in plasma progesterone and prolactin con- Rep. Int. Whaling Commission (Special Issue 3), 18–22.
centrations during the annual cycle and the role of prolactin in the Marsh, H., 1985. Observations on the ovaries of an isolated minke whale:
maintenance of lactation and luteal development in the Antarctic fur evidence for spontaneous sterile ovulation and structure of the resul-
seal (Arctocephalus gazella). J. Reprod. Fert. 91 (2), 637–647. tant corpus. Sci. Rep. Whales Research Inst. 36, 35–39.
Boyd, I.L., 1991b. Environmental and physiological factors controlling the Marsh, H., 1995. The life history, pattern of breeding and population
reproductive cycles of pinnipeds. Can. J. Zool. 69, 1135–1148. dynamics of the dugong. In: O’Shea, T.J., Ackerman, B.B., Percival, H.F.
Boyd, I.L., Lockyer, C., Marsh, H.D., 1999. Reproduction in marine mam- (Eds.), Population Biology of the Florida Manatee. U.S. Department of
mals. In: Reynolds III, JE., Rommel, S.A. (Eds.), Biology of Marine the Interior, National Biological Service, Information and Technology
Mammals. , pp. 218–286. Report 1, pp. 75–83.
Boyd, I.L., 2009. In: Perrin, W.F., Wursig, B., Thewissen, J.G.M. (Eds.), Pin- Marsh, H., Kasuya, T., 1984. Changes in the ovaries of the short-finned
niped Life History in Encyclopedia of marine mammals. , 2nd ed. pilot whale, Globicephala macrorhynchus, with age and reproductive
Elsevier, Burlington MA. activity. Rep. Int. Whaling Commission (Special Issue 6), 331–335.
Brook, F.M., Kinoshita, R., Benirschke, K., 2002. Histology of the ovaries of a Marsh, H., Kasuya, T., 1986. Evidence for reproductive senescence in
bottlenose dolphin, Tursiops aduncus, of known reproductive history. female cetaceans. Rep. Int. Whaling Commission (Special Issue 8),
Mar. Mammal Sci. 18 (2), 540–544. 57–74.
 P. Pomeroy / Animal Reproduction Science 124 (2011) 184–193 193

Marsh, H., Heinsohn, G.E., Channells, P.W., 1984a. changes in the ovaries Reijnders, P.J.H., Brasseur, S.M.J.M., Meesters, E.H.W.G., 2010. Earlier pup-
and uterus of the dugong, dugong dugon (Sirenia: Dugongidae) with ping in harbour seals, Phoca vitulina. Biol. Lett. June, doi:10.1098/rsbl.
age and reproductive activity. Aust. J. Zool. 32, 743–766. 2010.2010.0468.
Marsh, H., Heinsohn, G.E., Marsh, L.M., 1984b. Breeding cycle, life his- Robeck, T.R., 1996. Defining Basic Reproductive Physiology Includ-
tory and population dynamics of the dugong, Dugong Dugon (Sirenia: ing Reproductive Anatomy, Reproductive Endocrinology and Estrus
Dugongidae). Aust. J. Zool. 32, 767–785. Induction in Captive Delphinids. Dissertation, Texas A&M University
Mathews, L.H., 1948. Cyclic changes in the uterine mucosa of bal- UMI Dissertation Services 89-166.
aenopterid whales. J. Anat. 82, 207–232. Robeck, T.R., Curry, B.E., McBain, J.F., Kraemer, D.C., 1994. Reproductive
Murphy, S., Winship, A., Dabin, W., Jepson, P.D., Deaville, R., Reid, R.J., biology of the bottle nose dolphin (Tursiops truncatus) and the poten-
Spurrier, C., Rogan, E., Lopez, A., Gonzalez, A.F., Read, F.L., Addink, tial application of advanced reproductive technologies. J. Zoo Wildl.
M., Silva, M., Ridoux, V., Learmonth, J.A., Pierce, G.J., Northridge, S.P., Med. 25, 321–336.
2009. Importance of biological parameters in assessing the status of Robeck, T.R., Atkinson, S.K.C., Brook, F., 2001. Reproduction. In: Dier-
Delphinus delphis. Mar. Ecol.: Prog. Ser. 388, 273–291. auf, L.A., Gulland, F.M.D. (Eds.), CRC Handbook of Marine Mammal
Odell, D.K., Bossart, G.D., Lowe, M.T., Hopkins, T.D., 1995. Reproduction of Medicine. CRC Press, Boca Raton, Florida, 1063 pp.
the West Indian manatee in captivity. In: O’Shea, T.J., Ackerman, B.B., Slijper, E.J., 1949. On some phenomena concerning pregnancy and
Percival, H.F. (Eds.), Population Biology of the Florida Manatee. U.S. parturition of the Cetacea. Bijdragon tot de Dierkunde 28,
Department of the Interior, National Biological Service, Information 416–448.
and Technology Report 1, pp. 192–193. Temte, L.J., 1991. Precise birth timing in captive harbour seals (Phoca vit-
Perrin, W.F., Myrick, A.C., 1981. Report of the workshop. Age determina- ulina) and California sea lions (Zalophus californianus). Mar. Mammal
tion of toothed whales and sirenians. Rep. Int. Whaling Commission Sci. 7, 145–156.
(Special Issue 3), 1–50. Testa, J.W., Adams, G., Bergfelt, D., Johnson, D., Ream, R., Gelatt T, 2010.
Pomeroy, P.P., Fedak, M.A., Anderson, S.S., Rothery, P., 1999. Consequences Replicating necropsy data without lethal collections: using ultra-
of maternal size for reproductive expenditure and pupping success of sonography to estimate early term pregnancy rate in northern fur
grey seals at North Rona, Scotland. J. Anim. Ecol. 68, 235–253. seals. J. Appl. Ecol. (in press).
Reijnders, P.J., 1990. Progesterone and oestradiol – 17beta concentration Wells, R.S., 1984. Reproductive behaviour and hormonal correlates in
profiles throught the reproductive cycles in harbour seals (Phoca vit- Hawaiian spinner dolphins, Stenella longirostris. Rep. Int. Whaling
ulina). J. Reprod. Fert. 90, 403–409. Commission (Special Issue 6), 465–472.