So far this year, visitors on Jim Abernethy's Shearwater were able to take pictures of a very pregnant Emma the Shark, the charismatic star of This is your Ocean: Sharks. I was curious to learn more about Emma's pregnancy and about tiger shark gestation in general. I spoke to Jim about Emma's pregnancy as well as his observations of tiger sharks over the years. To help me learn more about the science behind tiger shark reproduction, Jim introduced me to Dr. Neil Hammerschlag of the R.J. Dunlap Marine Conservation Program (RJD) at the University of Miami, who directed me to some of the resources listed at the end of this article. Here's what I learned.

Emma's pregnancy

Emma's current pregnancy began as early as June, 2010 when Jim started observing (and photographing) Emma's mating wounds, which accumulated over a 10-week period. Nobody has seen tiger sharks mating or been able to follow an individual tiger shark from first mating through parturition (birth). There also appears to be no scientific documentation on how frequently a single female tiger shark mates during her breeding season, but judging from the multiple mating wounds observed on many of the female tiger sharks, it happens quite frequently. Jim has also observed that it is mainly the larger females who have mating wounds, not their smaller sisters. This is typical for most shark species. The sexually mature females are the largest in the area, and they seem to mate with even barely mature males [1].

When mating, the male shark uses his teeth to hold the female, grasping her fins or body, while inserting one of his claspers into her genital opening (a vent below the pelvic fins), inflicting wounds that quickly scar over. Female sharks have thicker denticles (the tiny tooth-like scales that cover the skin of sharks) than males, so most mating wounds heal quickly and leave no lasting damage.

Given a working knowledge of shark anatomy, and the location of some of the mating wounds, Jim believes that many wounds are the result of unsuccessful mating attempts by inexperienced males. For example, on July 31, 2010 Emma showed up with a severe injury to her dorsal fin, as you can see in this photo, which was taken while the wound was still raw 100731-DorsalDamage.jpg.jpg. Because of the dorsal fin's proximity to the genital opening, is unlikely that the male shark could compress himself into the requisite "U" shape to insert his claspers and make it work, so this hapless male may have bitten off a chunk of her dorsal fin in a failed attempt.

Earlier photographs from June 17 show damage to her anal fin, also from an unsuccessful mating attempt 100617-AnalFinDamage.jpg, and damage to her gills 1000617-GillDamage.jpg, which likely represents a successful mating. By biting her gills, the smaller male shark wouldn't have to contort himself to insert his claspers.

Most of Emma's mating wounds healed quickly, but the gill wound was still present on July 31 when the dorsal fin wound was documented 100731-101948-0065.jpg and also in September when her pregnancy started to show 100916-bothWounds.jpg.

Tiger sharks: The Science

Tiger sharks are members of the shark family Carcharhinidae, which has more than 54 species. Aside from being larger than most members of their family, they also have several unique features such as nostril flaps, a labial furrow or lip groove, uniquely shaped teeth, and a special gill slit (spiracle) behind the eyes that provides oxygen directly to the eyes and brain. Mature female tiger sharks normally range in size from 8 to 11.5 feet with average males slightly smaller, from 7.5 to10 feet. However, individual tiger sharks can be considerably larger. The record for largest tiger shark appears to be a female caught off Indo-China in 1957. She was reported to be 24 feet in length, and to weigh 6,860 pounds. Emma is estimated to be 14 feet in length.

Tiger shark reproduction

What really sets tiger sharks apart is that they reproduce using aplacental viviparity, also known as ovoviviparity. Most sharks reproduce using viviparity, which is giving birth to live young that have developed in a yolksac placenta.[2] Aplacental viviparity (ovoviviparity) means that tiger shark pups hatch from eggs that develop inside of the mother's body. There is no placenta to nourish the pups. Instead, the tiger mom produces uterine milk. Intrauterine cannibalism, in which developing embryos feed on unfertilized eggs or on each other, has not been documented in in tiger sharks. 

According to research on Hawaiian tiger sharks,[3] tiger sharks reproduce every three years, with litters that range from10-83 pups, with an average litter size of 35 to 55 pups. The gestation period ranges from 13 to 16 months, and females take a rest period of over a year before mating again. The tiger shark's triennial reproductive cycle means that if female tiger sharks reach reproductive maturity at 9 years and live to a maximum of 28 years, they can reproduce on average only 6.3 times per lifespan. [3] The maximum life span for tiger sharks in the Bahamas is not known, and it seems that the tiger sharks in the Indo-Pacific region are the record holders in the size category. Emma and the other large female tiger sharks that Jim has observed in the Bahamas over the last seven years have not grown appreciably in size.

Jim has observed that Emma has been pregnant 3 times in the last seven years, so the estimates for Hawaiian tiger sharks may need to be revised for regional populations, or as additional observational data is gathered on living sharks elsewhere in the world. Tiger sharks are found throughout the world's temperate and tropical waters except for the Mediterranean. Regional differences in migration patterns, the availability of food, and other environmental factors would appear to be the most likely explanation for these variations.

Much of the scientific knowledge about tiger shark gestation has been collected from dead specimens, which are often obtained through commercial and recreational fisheries. However, determining reproductive timing and maturity requires samplings of all developmental stages and all months of the year for both sexes. Commercial and recreational fishery catches often reflect a small portion of the year (due to regulations or migratory patterns). They only include a limited sampling of the length and age distributions, and are often sex-biased [4]. Pregnant female tiger sharks are prized for fishing tournaments because they are larger and heavier, so there is an additional incentive to catch them, potentially destroying not merely one shark, but future generations as well. Currently Shark Savers is working to protect Florida's tiger sharks and hammerheads. You can read about our work and the upcoming Commission hearings in Florida Fish and Wildlife Commission Workshop Report https://mckenziewestmore.com/en/blogs/763-florida-shark-workshop-report.html

Parturition

It is difficult to determine from photographs when Emma will give birth, although one can estimate roughly fifteen months from the time her mating scars first showed up last June. It's impossible to judge from mating scars alone which mating attempts were successful, or how many different sires Emma's pups are likely to have. In some shark species, litters have multiple fathers, and in others, a form of genetic monogamy occurs where one male shark's sperm out-competes the rest. As of this writing, I was unable to locate any studies of paternal DNA testing in tiger shark litters.

Jim noted that Emma’s previous pregnancies would end with her leaving the area where she interacts with divers for 3 weeks, and then returning much slimmed down in size. When it comes time to give birth, she will probably swim to a shallow, protected area in the Bahamas, affording her pups a better chance of survival.

Perrine_tigerpup.jpg When tiger sharks are born, their small size and awkward swimming style make them easy prey for other marine predators. Juvenile tiger sharks are exceedingly slender and delicately built, with over-sized fins and an elongated upper caudal lobe with a low thrust angle. This tail structure condemns new-born tiger sharks to an eel-like wriggle, an inefficient swimming style that renders them extremely susceptible to predators. To counteract this vulnerability, newborns grow very quickly. In fact, tiger shark pups typically double their length within their first year. But tiger sharks do not outgrow their ‘awkward stage’ until they reach a length of about 8 feet at about four years of age. [5] We don’t know how many pups from each litter survive, on average, to reproductive age. MaryO-juvenile.jpg

Learning more: The future of shark tagging

With the increase of shark satellite tagging over the past decade, scientists have been able to describe previously unknown migration patterns and diving behavior, as well as depth and temperature preferences for a variety of species. [6] Some tagging methods have a high rate of failure due to tags being dislodged or malfunctioning in various ways. Tags can also cause physiological or behavioral consequences that potentially alter a shark's natural behavior. Tagging has been able to answer many questions about where sharks go once they are tagged and head out to open ocean, although the reasons why sharks spend their time in certain areas and not in others remain mysterious. To answer these questions, scientists are working on a variety of tools and developing new satellite tagging technologies. [6] Tagging a pregnant tiger shark would tell us where she goes to give birth, so that we can ensure that those areas are protected.

Following tagged sharks

Although Emma is not tagged, you can follow other tiger sharks that have been tagged as part of the R.J. Dunlap Marine Conservation Program. Navigate to http://www.rjd.miami.edu/learning-tools/follow-sharks/. Click on Tiger Sharks, and click on the name of one of the sharks listed. A time slider tool at the top of the map shows you the date of each transmission, and the tools at the right allow you to navigate and zoom in and out. There is a description of each tagged shark under the map which gives you more information about that individual shark.

Conclusions

As apex predators, tiger sharks’ reproductive strategy of infrequent litters evolved to avoid overpopulation. But that strategy broke down when humans came along and started over-harvesting sharks for their fins. Since many female tiger sharks are killed for sport fishing tournaments when they are at their largest, i.e., pregnant, their triennial reproductive cycle makes it difficult for populations to recover.

The observational data collected by photographers like Jim, who interact with individual tiger sharks over many years, can help fill in some of the gaps in our knowledge. More work needs to be done to incorporate the data collected by citizen scientists (non-scientific observers) into current paradigms of shark behavior. More work is also needed in the area of non-invasive tracking technologies that do not interfere with a shark's natural behavior and do not injure the shark. Scientific knowledge is constantly evolving and so is our understanding of the grave need to save sharks from extinction.

Mary Chipman
Shark Savers
Visit Emma on her Facebook page https://www.facebook.com/EmmaTheShark

References

[1] Kajiura, S. M., Tyminski, J. P., Forni, J. B., and Summers, A.P. 2005.  The sexually dimorphic cephalofoil of Bonnethead sharks, Sphyrna tiburo. The Biological Bulletin, 209(1) 1-5.

[2] Medd, Hannah. Reproduction of Sharks and Rays. https://mckenziewestmore.com/en/education/shark-biology-behavior/620-reproduction-sharks-rays.html

[3] Whitney N, Crow G. Reproductive biology of the tiger shark in Hawaii. Mar Biol (2007) 151:63–70 DOI 10.1007/s00227-006-0476-0

[4] Hammerschlag N, Sulikowski J. 2011. Killing for Conservation: The Need for Alternatives to Lethal Sampling of Apex Predatory Sharks. Endangered Species Research 14: 135-140 http://www.rjd.miami.edu/scientific-publications/pdf/n014p135.pdf

[5] Martin RA. Biology of Sharks and Rays http://elasmo-research.org/education/ecology/coral-tiger.htm