The IUCN/SSC Shark Specialist Group
Shark News 9: June 1997
Reproductive Strategy of White Sharks, Carcharodon carcharias
Malcolm P. Francis, NIWAS, New Zealand
Great white sharks are large, comparatively uncommon, difficult to
catch and dangerous to handle. As a result, they are difficult animals
to study. Before 1991, we knew next to nothing about the reproduction
of white sharks. The few accounts of pregnant females or embryos that
existed were largely anecdotal, second-hand, or lacked detail. Since
1991, pregnant females or aborted embryos have been caught in New
Zealand, Japan and Australia and examined by scientists. These
fortuitous captures have greatly increased our understanding of
reproduction in the species, though many important gaps remain in
our knowledge. This article is based on the reports by Uchida et al.
(1987, 1996), Uchida and Toda (1996) and Francis (1996), unless
White shark Carcharodon carcharias embryo, 145 cm. Photo: Malxolm Francis
White shark embryos are nourished by eggs ovulated from their
mother's ovary (oophagy). Intermediate-stage embryos (100-110 cm
total length) have abdomens that are enormously distended by large
quantities of ingested yolk, whereas near-term embryos (135-151 cm)
have either empty stomachs or contain smaller quantities of yolk. This
developmental pattern appears similar to that in porbeagle sharks
(Lamna nasus), in which maximum ingestion of ova occurs about half-way
through gestation. Thereafter, the ova supply dwindles, and the
embryos digest the yolk held in their stomachs and store the energy as
lipids in an enlarged liver (M. P. Francis and J. D. Stevens, unpubl.
There is no evidence that white shark embryos cannibalise their
siblings (embryophagy). In the embryophagous sand tiger shark
(Carcharias taurus), only one embryo survives in each uterus, so litter
size is never more than two embryos (Gilmore 1993). In white sharks,
maximum litter size is at least ten (see below), which makes it unlikely
that embryophagy occurs. White shark embryos have no placental
attachment to the uterus, so their reproductive mode is aplacental
viviparity, with embryos being nourished by oophagy.
Litter sizes of 2-10 embryos have been observed, with unconfirmed
reports of as many as 14 embryos. Some of the litters may have been
incomplete, because abortion of embryos during capture is known in
other shark species, and is suspected in white sharks. Average litter
size is probably 5-10 young.
Length at birth
Length at birth can be estimated from the sizes of the largest embryos
and the smallest free-living young. The largest reported embryo was
151 cm, and at least 20 embryos have been found in the length range
135-151 cm. The smallest reliably-measured free-living white sharks
appear to be three 122 cm North American animals (Casey and Pratt
1985, Klimley 1985). There have been unconfirmed reports of free-living
white sharks shorter than this, but to my knowledge none has
been accurately measured. A considerable number of free-living
white sharks in the size range 125-140 cm have been caught. Length
at birth is therefore about 120-150 cm. This range will probably be
extended at both ends as further information is obtained. There are
insufficient data to determine whether length at birth varies regionally.
Pregnant females carrying embryos longer than 127 cm have been
caught from mid-winter to summer, indicating that parturition
occurs in spring or summer. Most neo-nate white sharks (less than 155 cm) have also
been caught in spring-summer (Casey and Pratt 1985, Klimley 1985, Fergusson 1996).
However, pregnant females reputedly carrying small em-bryos have also been
caught in spring or summer. There are several possible explanations for these
observations: (1) the reported embryo
lengths and/or capture dates were incorrect; (2) the reproductive cycle
is non-synchronous, with females carrying embryos at different stages
of development during spring-summer; or (3) the gestation period is
longer than one year, resulting in two (or more) cohorts of embryos
being present in the population at any given time. The second and
third explanations seem more likely than the first.
Embryos and pregnant or post-partum white sharks have been
reported from New Zealand, Australia, Taiwan, Japan and the
Mediterranean Sea. New-born and 0+ young have been reported from
New Zealand, Australia, Japan, South Africa, the north-east Pacific,
the north-west Atlantic and the Mediterranean (Casey and Pratt 1985,
Klimley 1985, Fergusson 1996). Therefore, parturition probably occurs
in many distinct, mostly temperate, locations world-wide.
Length and age at maturity
The length at maturity of male white sharks is difficult to determine,
but is probably about 3.8 m (Pratt 1996). Most female white sharks do
not mature until 4.5-5.0 m. There have been reports of smaller mature
females, but these have not been confirmed. Based on the growth
curve provided by Cailliet et al. (1985) for north-east Pacific white
sharks, ages at maturity are tentatively estimated to be 8-9 years for
males and 12-15 years for females.
Mating of white sharks has been observed only once, in spring. Other
indirect signs can be used to infer recent mating, including semen or
spermatophores flowing from the claspers, swollen siphon sacs,
chafed claspers, and bite marks on females. For white sharks, most
such observations have been made during spring-summer. Because
parturition is also thought to occur in spring-summer, mating may
occur soon after parturition, and females may carry successive litters
of embryos with little or no resting period in between. However, this
remains to be demonstrated.
Gaps in our knowledge
Although our understanding of white shark reproduction has advanced
rapidly in the last six years, many important gaps still remain. We now
have estimates of the length at maturity of both sexes, and the length
at birth, but they are based on pooled, world-wide, data. In better-studied
species of sharks, these parameters can vary substantially
among populations. We should therefore expect regional variation
in white sharks. The same is true of age at maturity, which is poorly
estimated. Furthermore, the only available growth curve for white
sharks does not distinguish between males and females, which may
have different growth rates.
We don't have a good estimate of
average litter size, and we don't know whether litter size
varies with the size of the mother. Some or all of the reliably
reported litters (only six of them) may have been incomplete, and
reports of litter sizes greater than ten require confirmation.
More import-antly, we have no information on the
length of the gestation period, and whether females produce a litter
every year. Gestation period in the related shortfin mako (Isurus
oxyrinchus) is thought to exceed one year (H. Mollet, pers. comm.).
If the gestation period of white sharks exceeds one year, and females
have a resting period between pregnancies, they may only produce
young every 2-3 years. At present, we can only speculate on this
crucial element of the reproductive cycle.
Implications for management and conservation
Before humans began to catch white sharks, the white shark
reproductive strategy was clearly adequate to maintain their
populations. After all, it had served them well for millions of years.
Because of their large size at birth, white sharks have few natural
predators, even as juveniles. Consequently a low reproductive rate is
all that is necessary to balance a probable low rate of natural mortality.
All fish species, including white sharks, have presumably evolved
density-dependent mechanisms that compensate for natural
fluctuations in abundance. Those mechanisms might include increased
growth rate in response to reduced competition for food, reduced
natural mortality rate, and increased reproductive output. For an apex
predator with very low population density, it is difficult to imagine
how reductions in population size could provide sufficient stimulus
to initiate density-dependent changes in growth and mortality. Food
supply is presumably not limiting for white sharks (except perhaps
where humans have depleted marine mammal populations), and the
probable low natural mortality rate appears to leave little room for
Fecundity could increase through earlier maturation, increased
litter sizes or a shorter reproductive cycle. Earlier maturation would
require faster growth rates, unless social cues, such as interaction rates
with older animals, are important. There is probably little scope for
increasing litter sizes unless length at birth declines correspondingly;
the mother's body cavity can only hold so much embryonic biomass.
A shorter reproductive cycle would require one or more of the
following: faster embryonic growth; reduced length at birth; de-synchronisation
of the reproductive cycle; removal or reduction of the
resting period between pregnancies (if present).
We know virtually nothing about density-dependent responses to
fishing pressure for any chondrichthyan, let alone white sharks. Nor
do we have enough information with which to construct white shark
demographic or age-structured population models. We therefore
cannot predict whether the white shark's reproductive strategy is
sufficient to maintain recruitment in the face of human exploitation.
Intuitively, one would expect low fecundity and low natural
mortality to result in low productivity and minimal capacity for
density-dependent compensation. White shark populations are
therefore likely to be vulnerable to recruitment overfishing.
Cailliet, G.M., Natanson, L.J., Welden, B.A., and Ebert, D.A. 1985.
Preliminary studies on the age and growth of the white shark,
Carcharodon carcharias, using vertebral bands. Memoirs of the
Southern California Academy of Sciences 9: 49B60.
Casey, J.G., and Pratt, H.L. 1985. Distribution of the white shark,
Carcharodon carcharias, in the western North Atlantic. Memoirs of
the Southern California Academy of Sciences 9: 2-14.
Fergusson, I.K. 1996. Distribution and autecology of the white shark in the
eastern North Atlantic Ocean and the Mediterranean Sea. In: pp. 321-
345, A.P. Klimley and D.G. Ainley (eds), Great White Sharks. The
Biology of Carcharodon carcharias. Academic Press, San Diego.
Francis, M.P. 1996. Observations on a pregnant white shark with a review
of reproductive biology. In: pp. 157-172, A.P. Klimley and D.G.
Ainley (eds), Great White Sharks. The Biology of Carcharodon
carcharias. Academic Press, San Diego.
Gilmore, R.G. 1993. Reproductive biology of lamnoid sharks.
Environmental Biology of Fishes 38: 95-114.
Klimley, A.P. 1985. The areal distribution and autoecology of the white
shark, Carcharodon carcharias, off the west coast of North America.
Memoirs of the Southern California Academy of Sciences 9: 15-40.
Pratt, H.L. 1996. Reproduction in the male white shark. In: pp. 131-138,
A.P. Klimley and D.G. Ainley (eds), Great White Sharks. The Biology
of Carcharodon carcharias. Academic Press, San Diego.
Uchida, S., and Toda, M. 1996. Records of pregnant white sharks from
Japanese waters. Kaiyo Monthly 28: 371-379.
Uchida, S., Toda, M., Teshima, K., and Yano, K. 1996. Pregnant white
sharks and full-term embryos from Japan. In: pp. 139-155, A.P.
Klimley and D.G. Ainley (eds), Great White Sharks. The Biology of
Carcharodon carcharias. Academic Press, San Diego.
Uchida, S., Yasuzumi, F., Toda, M., and Okura, N. 1987. On the
observations of reproduction in Carcharodon carcharias and
Isurus oxyrinchus (abstract). Report of the Japanese Group for
Elasmobranch Studies 24: 5-6.
Malcolm P. Francis,
National Institute of Water and Atmospheric Research,
PO Box 14-901, Wellington, New Zealand.