Female Shark Reproductive Systems

The reproductive system of the female shark!

by Christopher N. Owen

This is part two of my series of posts on shark reproduction. The first part covered the male reproductive system. Here I cover the female reproductive system, following the egg cell from formation to maturity, and then discuss adaptations of live-bearing and egg laying sharks. r

Egg cells (but not the complete egg) form in the ovary. Depending on the species, only one ovary may be functional, and it will be expanded across the center of the shark to fill the space of the opposite ovary as well. The ovary is lodged in the epigonal organ. Egg cells leave the ovary through the front end through the ostium and into the tubular oviducts. Oviducts are bilaterally paired, even in species with only one ovary. They soon curve around to direct eggs toward the back of the shark.

There is an expansion in the oviduct called the oviductal gland. The oviductal gland is responsible for the formation of leathery shell tissue in the egg-laying species. It also stores sperm in both egg-laying and live-bearing species.

The egg cells then pass through a region of the oviduct called the isthmus, which leads to the uterus. Like the oviducts, there are two uteri, one on each side of the shark. The two uteri merge near the rear of the shark, where they lead to the cloacal chamber, which opens to the exterior of the shark. (The cloacal chamber has several tubes leading to it, including the uterine canal, rectum, and urinary papillae).

During this journey from the ovary to the outside world, the egg cell will form an embryo. In egg-laying sharks, the embryo will not develop into an animal capable of survival in the outside world until some time after the eggs are laid. However, live-bearing sharks give birth to much more developed, independent young.

There is an evolutionary tradeoff between egg-laying (oviparity) and giving birth to more developed live young (viviparity). All sharks are descended from an oviparous ancestor. Many larger species, however, later developed viviparity. Because the young of viviparous species are more developed, they are more likely to survive after being born, but a direct consequence of having more developed young is that those young are larger. This decreases the number of young that will fit in the mother's uterus, thus making viviparity an advantage only for larger species.

Eggs cases have highly specialized shapes that help to increase their survival rate. Many are flattened and tapered at the ends so that they can be easily wedged into crevices. Some also have extensive filaments projecting from the case, which the mother can tangle around various objects. A few are even threaded, like screws, so that the mother can twist them tightly into position.

This concludes the parts of shark reproduction I care about the most. Now that you know how sharks reproduce, why not form some shark babies of your own?

Source: Klimley, P. A. (2013). The Biology of Sharks and Rays. The University of Chicago Press, Chicago, IL and London, England. 

The Viral Nudibranch Jorunna parva, AKA the Sea Bunny

by Christopher Owen

A certain creature has recently gone viral. Many call it the sea bunny, but it is actually a tiny gastropod. Since it is not often that a gastropod of any size occupies a significant portion of the public consciousness, I've decided to take advantage of a felicitous situation join our little friend Jorunna parva's sudden wave of fame.

Image by crawl_ray on flickr

What are they?

You will have noticed by now that sea bunnies do not by any means belong in the order Lagomorpha, much less are they any sort of leporid. Rather, a sea bunny (more proprietously known as Jorunna parva) is actually a nudibranch (the word is a Latin/Greek mongrel meaning “nude branchia”, which is pretentious English for “naked gills”, referring to the fact that their gills are naked, but more about that in a bit). They are found throughout the coasts of the the Indian Ocean, as well as east to the central Pacific. Most individuals of J. parva are yellow with black spots, but the white ones are more famous.

Some would call nudibranchs slugs, while others prefer to refer to them as shell-less snails. Which one it really is depends on your personal views regarding the concepts of slug and snail, a timeless philosophical issue with powerfully convincing arguments on both sides. In the slug camp are those who believe that any gastropod without a shell belongs squarely in the set of slugs. However, a subtler distinction must be made when we examine the evolutionary history of these animals, for such an examination will reveal that the branching of those priapistic garden friends traditionally known as slugs occurred long after the split between the shelled snails and the nudibranchs. The issue is further complicated by the fact that larval nudibranchs retain the shells of their ancestors, while land slugs lose the shell well before they hatch. Does this mean that a nudibranch is a snail until its shell falls off, at which point it becomes a slug? Certainly further debate is necessary.

Image by crawl_ray on flickr

What are their parts?

Rather than providing an exhaustive list of structures found in J. parva, I will focus on their most bunny-like components.

The “fur” of the sea bunny is actually made of many hardened, skin-covered scaffolds called caryophyllidia. Many nudibranchs possess different versions of these structures. They are commonly assumed to play a sensory role, both because of their resemblance to known sensory organs and because of their close association with the nervous system.

The “ears”, called rhinophores, are actually more like noses. They contain a series of stacked membranes, called lamellae, which give them their feather-like appearance. The lamellae greatly increase the surface area of the rhinophores, allowing the nudibranch to detect very dilute chemicals in their watery surroundings.

Finally, the “tail” is actually J. parva's gills. If these animals were snails, the gills would be hidden inside the shell. It is the absence of this covering that gives nudibranchs their name.

Image by Christophe Cadet

What do they do?

Much like its mammalian namesake, J. parva spends most of its time eating and having sex. Fortunately, both of these behaviors happen to be pretty interesting among dorid nudibranchs, the group to which J. parva belongs. 

The dorid diet consists primarily of sea sponges. They incorporate several chemicals from the sponges into their own bodies, including various toxins and pigments, often without altering their chemical structures in any way. This makes dorids extremely toxic to almost all potential predators. Interestingly, the evolutionary loss of the shell in dorids and related groups tends to follow the ability to retain dietary toxins in the body. Even more interestingly, the sponges on which the animals feed have also lost much of their rigid skeletal structure in correlation with the ability to produce toxins.

Moving on to reproduction: J. parva are simultaneous hermaphrodites, containing both male and female reproductive systems (as opposed to serial hermaphrodites, who are able to change sexes, but belong to only one sex at any given time). The intromittent organ (equivalent to a penis) is a sharp spine located on the right side of the head. There is also a female port (equivalent to a vagina), which is located slightly left of the center line on the underside of the nudibranch. Copulation occurs between two animals, both of which fertilize each other. Sperm can be stored and used as needed. Unwanted sperm are digested. The animals lay ribbons of eggs in carefully crafted counterclockwise spirals. The larvae that hatch from the eggs are free-swimming, but will eventually settle to crawl around on their bellies, where they prefer to stay throughout their adult lives.

(Please feel free to leave corrections and questions in the comments.)

Sources:

Bouchet, P. & Rocroi, J. (2005). Classification and nomenclator of gastropod families. Malacologia, 47(1-2): 1-397. Retrieved from https://archive.org/stream/malacologia47122005inst#page/n3/mode/2up

Cardone, B. J. (2015). Sea slug courtship and reproduction. California Diving News. Retrieved from http://www.cadivingnews.com/marinelife/1204/Sea-Slug-Courtship-and-Reproduction--

DeYoung, A. (2007). Nudibranch Embryological Development. University of Oregon. Retrieved from https://scholarsbank.uoregon.edu/xmlui/bitstream/handle/1794/5332/embryology002.pdf?sequence=1

Faulkner, J. D. & Ghiselin, M. T. (1983). Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Marine Ecology – Progress Series, 13: 295-301. Retrieved from http://www.int-res.com/articles/meps/13/m013p295.pdf

Kress, A. (1981). A scanning electron microscope study of notum structures in some dorid nudibranchs (Gastropoda: Opisthobranchia). Journal of the Marine Biological Association of the United Kingdom, 61(1): 177-191. (Abstract.) Retrieved from http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=4387472&fileId=S0025315400046002

Lee, J. J. (2015). Meet the adorable “sea bunny” taking over the internet. National Geographic. Retrieved from http://news.nationalgeographic.com/2015/07/150723-sea-slug-nudibranch-sea-bunny-ocean-animals-science/?sf11266065=1

Rudman, W.B. (1999). Rhinophore in nudibranchs. Sea Slug Forum. Retrieved from http://www.seaslugforum.net/find/rhinonud

Valdés, Á. & Gosliner, T. M. (2001). Systematics and phylogeny of the caryophyllidia-bearing dorids (Mollusca, Nudibranchia), with the description of a new genus and four new species from Indo-Pacific deep waters. Zoological Journal of the Linnean Society, 133: 103-198. Exerpt retrieved from http://rfbolland.com/okislugs/caryophy.html

An Introduction to Shark Reproduction, Part I: Male Reproductive Physiology

by Christopher Owen

This is the first part of what I hope will be a series of posts related to shark reproduction. I’m starting with the male reproductive system, mainly because I read about it first. Future posts will focus on the female reproductive system, gametogenesis (i.e. the production of eggs and sperm), and reproductive behaviors. Although this article specifically concerns sharks, there are more similarities between the reproductive systems of sharks and other chondrichthyes (rays and chimaeras) than there are differences. I may make a future post about these differences if I feel like it.

The first question people often ask about an unfamiliar reproductive system is “what is the penis like?” If one wishes to be truly pedantic, sharks have no penises. Intromittent organs (made to transfer sperm into some internal part of the female) have evolved many times over the years, producing a wide variety of appendages related only in purpose. Only those intromittent organs of the mammals receive the honor of being referred to as “true penises”. Instead, the male shark has a pair of claspers. They are modified pelvic fins that penetrate the female’s cloaca, delivering sperm through an internal tube known as the dorsal grove. The main support structure of the clasper is the stem cartilage. It lends the clasper a certain stiffness that most intromittent organs require to attain any level of effectiveness. Claspers may also boast a number of appendages whose purpose is to prevent them from slipping out of the female’s cloaca during copulation. For example, the clasper of the male spiny dogfish, Squalus acanthias, contains four such appendages. The spur has a sharp tip. It rotates perpendicularly to the stem cartilage upon penetration. The claw and ventral terminal cartilage also rotate perpendicularly to the stem cartilage, but in the opposite direction of the spur, forming a “T” shape. The claw is hooked and sharpened at the end. The ventral terminal cartilage contains the distal end of the dorsal grove through which semen is transferred. A fourth appendage is called the rhipidion. It expends, fanlike, with edges anchoring into the female’s cloacal wall, further anchoring the clasper during copulation. There is significant diversity in clasper anatomy. For example, the blue shark, Prionace glauca, forgoes most of the above-listed appendages, retaining only the rhipidion.

 
Claspers of Carcharhinus brevipinna (from Wikipedia)

In evolutionary terms, the benefits of such complex adaptations are clear. Most fishes practice external fertilization, and ocean fishes tend to practice a particularly wasteful form of external fertilization known as broadcast spawning, wherein clouds upon clouds of gametes are released into the ocean in vague hopes of reproduction. By contrast, the injection of sperm directly into the female reproductive system greatly increases the chances that sperm and egg will find each other. This means that the animals do not have to waste resources producing gametes that will likely never amount to anything. In addition, the young are able to develop to highly advanced stages before leaving the safety of the womb, greatly reducing both early-life predation and starvation.

You probably weren’t wondering about the internal reproductive physiology of male sharks, which is a shame. But this article wouldn’t be complete without it, so here we go:
Sperm originate in the testes, as you may have guessed. Unlike human testes, shark testes contain seminiferous ampullae rather than seminiferous tubules. These burst upon maturation of the sperm cells (similar to the ovarian follicles in humans). The testes are nested in the epigonal organ, whose other primary purpose is to generate blood cells (remember that sharks have no bone marrow). When the seminiferous ampullae release their sperm, the sperm travel out of the testicles through the ductus efferens, a group of tubules that run through a band of connective tissue called the mesorchium. The ductus efferens transports the sperm cells to the epididymis. Some of them are stored there for a while, while others travel down the small and convoluted tubules of the epididymis. These tubules eventually all converge, forming the ductus deferens. Near its end, the ductus deferens enlarges to form the ampulla ductus deferens. Here, the sperm grouped into packages called spermatophores. A papilla from the ampulla ductus deferens projects into a chamber known as the urogenital sinus, which in turn projects into the cloaca. Normally, sperm that make it this far would end up in the open ocean, but during copulation the male lines the base of his clasper up in such a way that sperm are forced into the opening of the dorsal grove (this basal opening is called the apopyle). Sperm are forced out through the contraction of siphon sacs, bladders located just beneath the skin (but above the muscle). These sacs are filled with seawater as the male swims forward, and emptied through muscular action. This forces the sperm into the apopyle of the clasper, simultaneously breaking up the spermatophore’s membranes before they enter the female. Sperm finally exits the male and enters the female’s cloaca through an opening at the tip of the clasper called the hypopyle. An inexperienced male is unlikely to be able to perform all of these actions correctly, but with any luck, the sperm will travel through the series of tubes that form the female’s reproductive system (to be discussed in the future), where some of them will encounter eggs, and a batch of new sharks will be formed.


The reproductive system of Lamna nasus from the National Oceanic and Atmospheric Administration.

If you read through this article you probably noticed some typos, and also have questions. Please take advantage of the comment utility to share your insight.

Some sources I used for this article are:

The Biology of Sharks and Rays, by A. Peter Klimley, University of Chicago Press, 2013
Shark and Ray Reproduction, by some Unknown Author, published online at http://www.sharksavers.org/en/education/biology/shark-and-ray-reproduction/
I also used Google images to figure out what some of these things looked like.

“I'll bet this author doesn't even know how to write a bibliography in APA format!” --someone who is wrong