Whale Shark Reproduction

Written By Simon J Pierce

< Guide to whale sharks

This article is based on information from Whale Sharks: Biology, Ecology, and Conservation, the first scientific textbook on whale sharks, co-authored by Marine Megafauna Foundation co-founder and Principal Scientist Dr. Simon J Pierce.

 

As the largest shark species, whale sharks face numerous threats that impact their global population. Gaining a deeper understanding of their reproduction is crucial for developing effective conservation strategies. By studying their reproductive biology, researchers can estimate population growth and assess the success of management efforts. Recent groundbreaking technologies have shed light on whale shark reproduction, providing invaluable insights that will help protect these magnificent creatures for future generations.

Diversity of Shark Reproduction

Sharks employ a wide range of reproductive strategies to maximize their evolutionary success. These strategies are influenced by various factors, such as habitat, ecological niche, and body form. With over 500 species of sharks, researchers continue to be amazed by their reproductive diversity, from oviparity (egg-laying) to adelphophagy (sibling cannibalism) and even parthenogenesis (asexual reproduction). The study of shark reproduction remains a favorite among reproductive and evolutionary biologists, as sharks continue to surprise scientists with their incredible capabilities and adaptability.

Unlike most bony fishes that use external fertilization, sharks use internal fertilization, where fetal development occurs at least partially inside the mother's body. This approach varies from egg-laying species, where embryos develop within egg cases on the seafloor, to viviparous species, where embryos develop entirely inside the mother before being born as free-swimming pups. Yolk-sac viviparity, as seen in whale sharks, involves the yolk-sac providing the main source of nutrition for the developing embryos. This approach, however, limits the size of the offspring due to the finite resources provided by the yolk-sac.

The Groundbreaking Discovery of a Pregnant Whale Shark

For a long time, whale shark reproduction remained a mystery, with many researchers believing them to be egg-laying due to the discovery of a large egg case containing a live whale shark embryo in the Gulf of Mexico in 1953. The embryo still had an attached external yolk-sac, and its gut cavity was full of yolk, leading to the belief that whale sharks were egg-layers. However, the thin, light-colored egg case suggested that it may have been aborted, leaving researchers uncertain about the reproductive mode of whale sharks.

In a pivotal moment for the understanding of whale shark reproduction, a 10.6-meter-long, 16-ton pregnant female whale shark was caught off Taiwan. Dubbed "megamamma", this extraordinary specimen carried around 300 embryos in various stages of embryonic development in her twin uteri.

Among the contents of her uteri, researchers found empty egg cases from embryos that had already hatched. They measured 24 of these egg cases, which had an average length of 21 cm. Additionally, some embryos were still present inside their egg cases, with their yolk-sac attached. However, most embryos had already left their eggs and were nearly ready for birth.

The largest size-class of embryos, measuring between 58 and 64 cm in total length, had clear vitelline scars at the prior attachment point of their now fully absorbed yolk-sacs. The sex ratio of all the inspected embryos was 123:114 (female:male), which was not significantly different from 1:1.

This litter, containing slightly over 300 embryos is the largest ever recorded in a shark, surpassing the next largest litter of 135 from a blue shark, Prionace glauca. It's important to note, however, that the average litter size for blue sharks is only around 30.

The discovery of this pregnant whale shark provided groundbreaking insights into their reproductive mode, confirming that whale sharks are yolk-sac viviparous, with embryos "hatching" inside the mother and being born as free-swimming and independent individuals.

Rare Observations and Anecdotal Accounts of Whale Shark Reproduction

While the pregnant whale shark from Taiwan remains the most informative finding to date, other observations and anecdotal accounts have provided glimpses into the elusive reproductive life of whale sharks. In 1910, a shark identified as a whale shark was caught with a "very ripe ovary" and numerous egg cases, but later investigations suggested it was likely a misidentification of another species. In 1996, a group of 16 juveniles was reported to be swimming alongside a whale shark off India, but this observation has been questioned by researchers, who considered it more likely to be an unrelated species.

Perhaps the most credible account of whale shark reproduction comes from Geoff Taylor, a pioneering whale shark researcher from Western Australia. Taylor witnessed a whale shark giving birth during an aerial survey of the Ningaloo Reef, with 14 newborn whale sharks emerging at the surface alongside the mother. This rare observation appears to be the only record of a whale shark giving birth. However, it is important to note that no postpartum maternal care has been recorded in any shark species to date, so any association between the mother and her offspring is expected to be brief.

Female Whale Sharks Reproductive Anatomy, Maturity, Cycle, and Seasonality

Sharks have developed specialized anatomical adaptations for internal fertilization. Female sharks possess a pair of reproductive tracts and a single or paired ovary located in the anterior body cavity. Only one ovary, usually the right, is typically developed in orectolobiform sharks. In whale sharks, either the right or left ovary may develop, as observed in dissections of three immature animals.

The ovary creates early-stage egg cells, known as oocytes, through a process called oogenesis. As these egg cells mature, they start making and releasing hormones, grow larger, and begin to form yolk in a process called vitellogenesis. Once they are fully developed, these egg cells, now called ova, travel through small openings called ostia into tubes known as oviducts, and then into a special gland called the oviducal gland. If the shark has mated, the ova are fertilized in this gland. The oviducal gland also creates a protective covering for the fertilized egg, which then moves into the uterus where the baby shark, or embryo, continues to develop.

Determining Maturity in Female Whale Sharks

The onset of maturity in individual sharks can be determined by examining anatomical changes in the reproductive tract. In females, the diameter and presence of visible yolk in the largest ovarian follicles, the developmental state of the oviducal gland, and the width and structure of the uterus are common characters used to determine maturity.

Although knowledge about whale shark reproduction is limited, their reproductive mode appears to be most similar to that of the nurse shark G. cirratum. Both species produce relatively large litters and have a variation of "normal" yolk-sac viviparity, referred to as serial yolk-sac viviparity. Ovulation is a prolonged process that lasts at least 2-3 weeks in nurse sharks and may last far longer in whale sharks due to their much larger litter size.

Maturity in female whale sharks is assumed to occur at 9-10 meters total length. Recent technological advances, such as waterproofed ultrasound units, have allowed researchers to examine the reproductive anatomy of whale sharks in their natural habitats, which can help gather data on maturity in wild sharks.

Ultrasound Imaging and Maturity Estimation

Ultrasound imaging helps estimate the largest size of follicles (egg-producing structures) in whale sharks by comparing them to well-known species. On average, mature whale sharks have follicles about 102 mm in diameter.

Ultrasound has also helped researchers study ovarian follicles in two female sharks thought to be 11-12 meters long. The largest follicle sizes in both Galapagos whale sharks were within the expected range, showing they were mature. Continuing to use ultrasound on large sharks (over 8 meters) can help gather information needed to better understand their maturity.

Hormone Levels and Maturity Assessment

New methods for taking blood samples from free-swimming whale sharks are now available. This allows us to study the reproductive hormone levels in the blood. Once we have baseline hormone measurements for mature sharks, these techniques will greatly improve our ability to gather information on whale shark reproduction and maturity in the wild with minimal disturbance.

It's crucial to understand whale shark reproduction and maturity to create effective conservation plans. Progress in ultrasound technology and in-water blood sampling offers new research opportunities, giving us important insights into their reproductive systems and maturity of these mysterious animals.

The Female Reproductive Cycle and Seasonality in Whale Sharks

Female viviparous sharks undergo a reproductive process involving ovulation, fertilization, embryonic development, and birth of free-swimming pups. The duration of each stage varies among species. Some sharks can retain sperm for fertilization over extended periods, like the brown-banded bamboo shark. Some species minimize the time between litters by having a new ovarian cycle concurrently with embryonic development from the previous cycle, allowing for annual or multiple litters. The length of the ovarian cycle is the main factor affecting the reproductive interval, which can be over 3 years in some species. Some sharks also include a resting period to prepare for the next cycle of vitellogenesis, resulting in varying reproductive intervals within a population.

For female whale sharks, follicle development and embryonic development don't seem to be concurrent, and a biennial or longer reproductive interval is most likely. Different shark species can have synchronized seasonal reproductive cycles, continuous mating throughout the year, or a combination of both. Diapause, the delay of embryonic development to regulate parturition time, can also occur.

Male Whale Sharks Reproductive Anatomy, Maturity, Cycle, and Seasonality

Male sharks have developed reproductive adaptations that focus on producing sperm and transferring it to the female. Although specific information on male whale sharks is limited, their internal organization is believed to be similar to other sharks. The paired testes function in sperm production and steroid hormone secretion. Sperm travels through the efferent ductules and into the epididymis before being stored in the seminal vesicle, ready for mating.

Copulatory Organs and Maturity Indicators

Adult male sharks have external "claspers" that extend from each pelvic fin and function as copulatory organs. At maturity, these structures are rigid and calcified, allowing for movement at the base. Siphon sacs under the skin hold seawater to flush sperm into the female's oviduct. Many species have hooks or claws on the clasper tip to maintain contact during mating.

Claspers are visible in free-swimming male sharks and are the most common way to determine maturity. Immature whale sharks have small, thin claspers, while mature males have thick claspers extending past the pelvic fins. Clasper length and appearance data have shown that maturity length differs among locations.

Size at Maturity and Geographic Variation

The size at maturity for whale sharks varies by location. In eastern Africa, the mean length of maturity is 9.2 meters, while in Qatar, Western Australia, the Philippines, and the Mexican Atlantic, it ranges from 6.8 to 8.1 meters. Differences in measurement techniques and observer biases may account for some variation, but real differences exist.

Larger sizes at maturity have been associated with higher latitudes and lower water temperatures. This phenomenon, called James's rule, is typically observed in endothermic species. For ectotherms like sharks and rays, faster growth in warmer water could explain the pattern.

Observations of Maturation in Captivity

Jinta, a male whale shark at the Okinawa Churaumi Aquarium, provides a unique opportunity to observe the maturation process. Clasper elongation occurred over 11 months, and mating display behaviors began in April 2012. Sperm were collected from Jinta's claspers in 2016, revealing a similar structure to other sharks' sperm. Testosterone levels increased during clasper elongation and remained high once the shark was mature, suggesting a role in reproductive functions like mating behavior, spermiogenesis, and clasper elongation.

Male Reproductive Cycle and Seasonality in Whale Sharks

Sperm production in male sharks can be continuous or seasonal, often with a peak associated with a specific mating season. Most studied elasmobranchs match their sperm production to the female's reproductive cycle, but sperm storage can also make a synchronous cycle unnecessary. Seasonal variation in sperm production can be associated with observable changes in clasper shape, with swollen claspers corresponding to mating season.

Courtship and mating behaviors have been observed in whale sharks in specific locations and times, with some instances of misdirected mating displays. Female whale sharks with presumed bite marks from mating have been seen at these locations. Mating observations are seasonal in Atlantic nurse sharks, which are similar to whale sharks in reproduction. Mature male nurse sharks visit mating locations yearly, while mature females return biennially or less frequently.

Reproductive seasonality in male whale sharks may be resolved by collecting field data on testosterone levels or assessing seasonal variation in mature clasper morphology. However, mature males may be seasonal visitors to specific locations for reasons other than mating, such as food availability. Sampling for such work may need to take place in multiple locations to test for seasonal variation.

Conservation Implications

Understanding the reproductive strategies of whale sharks and other shark species is crucial for their conservation. As slow-growing, long-lived animals with low reproductive rates, sharks are particularly vulnerable to overfishing and habitat degradation. Comprehensive knowledge of their reproductive biology and behavior will enable the development of effective conservation and management strategies to protect these incredible animals for future generations.

Simon J Pierce

Dr. Simon Pierce is a co-founder and Principal Scientist at the Marine Megafauna Foundation, where he leads the Global Whale Shark Program.

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