Coital fanging in a giant cartilaginous fish

(writing in progress)

It is axiomatic that dentition and genitalia are mutually exclusive in the bodies of all vertebrates. This is because teeth are anterior whereas genitalia are posterior, and teeth function by abrasion whereas genitalia function by lubrication.

The male basking shark1 has sharp denticles on each of its two phalluses2. The largest of these are fivefold longer than any of the denticles that serve as teeth in the mouth of the same species3. Because these largest of phallic denticles are the hardest parts of the whole body4 of this cartilaginous fish they deserve to be called phallic teeth. The vagina of the basking shark is designed accordingly, with a tough pad into which a phallic tooth5 anchors during copulation. Up to 25 litres per copulation of semen67 is ejaculated via a deep, scrolled groove in the phallus. Hardening of the phallus – with its numerous small denticles, complex articulating skeleton8, and phallic tooth – works in conjunction with propulsion of sea water into the vagina via an inflatable siphon sac up to 50 cm wide9. The unusual genital abrasiveness of the basking shark is partly explained by the facts that females breed only once every few years and that the sexes are often separated. There is consequently a need for the female to store bulky semen for long periods and an incentive for the male, prior to his own ejaculation, to remove any sperm stored from a previous mate. This removal is accomplished by flushing the vagina with sea water via one of the paired siphon sacs, a mechanism which partly obviates the need for lubrication and coital thrusting. By anchoring the phallus in the vagina, the phallic tooth allows the male to propel sea water twice in succession, stimulating the female, clearing any previous semen, and injecting his own by hydraulically assisted ejaculation.

Comment stream:
This photo of a basking shark can be used in commercial sites:
http://www.flickr.com/photos/10565417@N03/6246546546/in/photostream/
Old notes:
Fish mating. Many fishes mate by methods which might, from the human point of view, seem anticlimactic. Females simply release their eggs in the water while males – which lack any form of penis and instead have a cloaca similar to that of the female - simply release their sperm in the same water. These releases are usually performed in groups so that even the thrill of coupling is short-circuited. Although the male experience is presumably erotic, it is difficult to imagine that his free-to-water ejaculation is any more orgasmic than the perfunctory ejection of eggs by the female. In line with an assumption that their nervous systems are too simple for ecstatic relationships, sex appears to be a production line for these fishes rather than a pleasurable pursuit.
Fish copulation. Various fishes perform copulation in a strict sense of the word, and therefore potentially experience a piscine eroticism. Each of these species possesses a penis, even if only in a loose sense of the word.
Comparison of mode of reproduction in basking shark and priapiumfish. The second-largest of all fishes, at up to 12 metres long, is the basking shark, which widely roams the oceans of the globe. Among the smallest, at only 1.5 centimetres long, is the priapiumfish10, which is restricted to coastal rivers in southeast Asia from Thailand to Sumatra and the Philippines. Despite their difference in body size, both these fishes eat plankton and both reproduce by means of copulation, with a delay of up to several months between insemination and actual fertilisation. The mothers of both fishes release a few progeny11 at a time into the water, although these are free-swimming in the case of the shark and in the form of eggs in the case of the priapiumfish. The main difference in their mode of reproduction is that the basking shark retains the fertilised eggs12 until they hatch within her, whereas what is retained for months in the female priapiumfish is only sperm and its packaging. (we need to state what happens to progeny in this species.ok. Do you have this information off the top of your head, Antoni, or do we need to research it?) it’s probably in our email correspondence somewhere; or the Wikipedia site probably says...
Comparison of sexual hardware in basking shark and priapiumfish. Like mammals and reptiles, both the basking shark and the priapiumfish have erectile phalluses emerging from their pelvic girdles and located close to the orifices that expel faeces and urine. In keeping with the difference in body sizes, the phallus13 of the basking shark can be up to one metre long; whereas that of the priapiumfish is at most a few millimetres long and translucent. In terms of anatomical origin, the external genitalia of both fishes are similar, being partly derived from their pelvic fins. Despite their simple origins, the genitalia of both fish are so complex and strange that – although described – they have yet to be fully interpreted by ichthyologists.
Penile multiplicity in the basking shark and priapiumfish. Unlike humans but like all other sharks14, the phallus of the basking shark is paired between left and right sides of the body. Each of these phalluses15 is a complex extension of the cartilaginous and fleshy pelvic fin on that side of the body. Although each phallus16 can be described as one-half of a paired penis in sharks, only one17 of the two phalluses is used for a given copulation. Yes, the basking shark has a ‘spare’ phallus indistinguishable from the one chosen for intromission during any particular copulation. This apparent redundancy is remarkable considering the probable cost to streamlining that comes with having two large projections, each up to one metre long, disrupting the outline of the body [refer to the shark teeth e-essay].
In the priapiumfish, the penile undercarriage18 is very complex in a different way but, as in the basking shark, the mammalian penis falls short by comparison. Firstly, the phalluses - defined without too much rigidity - include not only the genital papilla, which contains the tube of ejaculation, but also a solid finger-like projection19, a hook20, and a sucker-like disc21 that perform copulatory penetration, anchoring, or both. Secondly, these various genital components are arranged not only from front to back but also from side-to-side, making the penis of the priapiumfish an unusual example of bilateral asymmetry in vertebrates.
Although the priapiumfish lacks the left-right duplication seen in sharks, it shows penile multiplicity in a different way. As in the shark, the whole penis is far too large to be inserted into the vagina as a whole, and we do not yet know exactly which parts are inserted or how. Therefore, our use of the words ‘phallus’ and ‘penis’ in the case of the priapiumfish is somewhat arbitrary.
We can interpret this arrangement by saying that the penis of the priapiumfish, although not paired like that of sharks, contains so many moving parts that the only way to fit them all in is to boggle the line separating left from right. What the priapiumfish possesses is a multifacetted organ of simultaneous embrace and penetration, on which each of the several surfaces22 may produce its own sexual friction.
Penile articulation in the basking shark and priapiumfish. We note that the penises of both the basking shark and the priapiumfish rise above those of humans, all reptiles, and all birds in containing not just skeletal reinforcement, but an articulating skeletal system.

In the basking shark, the skeletal system contained within the penis comprises 16 rods and plates of ossified cartilage – an arrangement which is in fact simpler than in many other species of sharks. Although the entire penile undercarriage of the priapiumfish is incomparably smaller than in sharks, it too contains a bony skeleton far more complex than the solid but simple penis bone23 found in most species of mammals24.
The substantial nature of the penis of the basking shark may initially escape notice because its phalluses are normally tucked parallel with its body, pointing towards the tail tip – presumably in aid of streamlining. However, when the male becomes sexually excited, one of the two phalluses is flexed to point forwards instead of backwards, simultaneously closing the cloaca. This erection is achieved by muscles rotating the phallus at its base, where the cartilage forms a joint and the semen leaves the genital papilla25 and is channelled by the phallus. Although the channel through which semen flows out is a deep scrolled groove rather than a closed tube, this scrolling of the phallus is so complex that it seems four-dimensional compared to the simple tube of the human phallus. By this remarkably complicated route the male basking shark deposits up to 25 litres of spermatophores per copulation, in the form of a veritable transfusible tissue of semen rather than a mere coagulated liquid such as human semen. Indeed, this semen has macroscopic structure, with each spermatophore being as much as three centimetres in diameter, and containing a core, as much as one centimetre in diameter, of millions of sperm.
Penile anchoring in the basking shark and priapiumfish. In the case of the basking shark, the phallus is not only large and complex, but grips the vagina internally by means of a sharp claw – or more correctly a tooth. Indeed, when this phallus26 is fully intromitted, it unfolds partly to lodge firmly inside the vagina. Not only do flaps of hard cartilages near the tip of the phallus splay to some extent, but an articulated claw extends sideways to anchor into a corresponding pad of tough fibrous material on the vagina wall. The bone-hard tip of this claw is more than three centimetres long, composed of the same material as shark teeth, and far larger than any tooth found in the mouth of this plankton-eating species of shark.
And for its part, the penile undercarriage of the priapiumfish possesses a hook-like projection and a sucker-like disc27. We do not know exactly how these are used, but it seems that they function in both anchoring and stimulation.

Penile accessorising in the basking shark and priapiumfish The kit of the male basking shark includes a pair of inflatable siphon sacs attached to the penis and originating as part of the pelvis but extending forward for up to 1.4 metres, reaching close to the pectoral fins. These blind sacs, each up to 0.5 metres wide, lie just under the skin of the body, with their paired opening at the base of the phalluses, and are invisible until they are inflated with sea water. They form subdermal, not visceral, chambers of the genital tract.
Although the precise function of these siphon sacs remains to be described, it appears that the sac on the same side as the active phallus fills passively with sea water when its opening is reorientated by the muscular flexing of phallic erection. Then, after intromission but possibly before as well as during ejaculation, the muscles of the siphon sac themselves contract to expel the sea water forcibly. This jet is capable of clearing the vagina by flushing out the sperm of any previous mate - as we will moot after a few more paragraphs - as well as providing a medium for the male’s own ejaculation. Each siphon sac can contain many litres of sea water, in proportion with the quantity and recalcitrance of the semen to be removed.
In the case of the priapiumfish, the penile undercarriage both teases out and subsumes various anatomical structures, a paradox which can possibly be interpreted as accessorising. For obscure reasons, the various orifices contained within the cloaca of most other fishes are here separated on the surface of the penile undercarriage. At the same time the penile undercarriage of the priapiumfish incorporates not just pelvic, but also pectoral bones shifted from their original location in normal fishes.
Possible reasons for basking shark and priapiumfish penile complexity. The priapiumfish has yet to be studied thoroughly. However, one explanation for the complexity of the penile undercarriage involves a parallel function with the basking shark: namely, a hypothetical competition between males in which each suitor attempts to remove the sperm of any male with which a female has previously copulated. Although the finger-like projection28 of the penile undercarriage lacks an ejaculatory tube, this solid but otherwise phallus-like structure may possibly be inserted into the vagina for physical removal of sperm packages.
Given the similarities of their genitalia to sex-toy kits, it would be easy to imagine that the basking shark and priapiumfish are creatures of extreme eroticism compared to other fishes. Since the pelvis of the priapiumfish has been shifted to near the capital sense organs of sight, hearing, smell, and taste, it is tempting to imagine that, in some way, the sexual act is not only more complicated but also more sensually fulfilling for the priapiumfish than for humans. Indeed, the arrangement in the priapiumfish seems the more transcendent considering that its penis is located in the most unlikely of positions, under its head. Although we have no way of knowing how these fishes experience the sexual act, there is probably a more mundane reality. This is because the basic reason for copulation in both basking shark and priapiumfish appears to be ecological. Both types of fishes inhabit waters subject to great seasonal changes, and meetings between the sexes do not necessarily correspond to the time of year most suitable for reproduction. The result is what may be described as a form of delayed gratification in contrast to the sexual and parental promiscuity of many other fishes. By copulating, both species seize the temporary opportunities for fertilisation, while delaying the bearing of their offspring for a presumably more suitable time and place.  
In the basking shark, there are pronounced seasonal movements from high latitudes to the equator, each female breeds only once every few years, and the sexes are known to be segregated at the most favourable time of year when plankton blooms near the surface in cold seas. For these reasons it seems that the conditions suitable for mating are so far removed from those suitable for giving birth that fertilisation is delayed by an appropriate hiatus of several months, and each female possibly stores in her reproductive tract enough sperm to last for several years. For its part, the habitat of the priapiumfish is rivers or canals near the coast, where the water is fresh but rises and falls subject to tidal influences as well as the great seasonal ebbs and flows of the monsoons. Thus it makes sense that the priapiumfish mates during the dry season, when its populations concentrate in reduced bodies of fresh water, but lays its eggs during the wet season, when waters are so extensive that there is minimal competition for food.
Both the basking shark and the priapiumfish pose a puzzle of genital symmetry. The female genitalia are both simple and bilaterally symmetrical, yet the male genitalia are either duplicated (in the basking shark) or asymmetrical (in the priapiumfish)29. Both the basking shark and relatives of the priapiumfish have packaged sperm which can be removed as a gelatinous mass. This fact may provide some clues for understanding the complexity of their respective genitalia, especially when considering that various animals, from insects to birds, are known to have sequential mating in which each male endeavours to remove the semen or seminal plug of the previous male in order to replace his sperm. Although the mechanisms have not been documented in basking shark or priapiumfish, competition among males at this level might possibly explain the additional and complicated genitalia. In the case of the basking shark, this might explain both the doubling of the phallus and the involvement of siphon sacs. This is because each phallus risks injury in its vigorous cleansing30 of the vagina, but the other phallus can be used for the next copulation; and siphon sacs can be used both for ejaculation and for pre-ejaculatory flushing [need to double check that when we talk about this later we make a link so it does not come across as repetition]. In the case of the priapiumfish, it might explain the presence on the penile undercarriage of a ductless but skeletally reinforced finger-like projection, which might be inserted into the vagina to remove previous semen, and the accompanying sucker and hook, which might give the male extra purchase while this cleansing is being performed and while the modest genital papilla is intromitted for fresh insemination.
In both species, it seems advantageous for the female to store enough sperm, in a well-structured mass, for a whole season of breeding. This in turn may mean that a successful male needs not only to copulate but also to clear the reproductive tract of the female before doing so. And this clearing out of sperm inevitably requires a lot more extra equipment than is required for a simple insemination. Consider the different apparatus required for a slapdash spray-gunning of car versus the methodical cleaning required to remove the grime from the car. The basking shark and the priapiumfish appear to have the equivalent of the bucket, cloth, vacuum cleaner, high pressure hose and detergent compared with the paint and simple spray-gun of other animals flaunting simple penises. So in these fishes, accessory male genitalia appear to be used not as much for foreplay as for a level of competition.
Males across many taxa of animals have elaborate ways of ensuring that their sperm – as opposed to a competing male’s sperm – fertilises the female’s egg or eggs. For example, copulatory plugs are used by some mammals and many insects, reptiles, and spiders. In the case of the bumblebee31 and fruit fly32 anti-aphrodisiac chemicals are released which manipulate female behaviour and reduce her desire for mating. Male black-winged damselflies take a more physical approach, using a specially adapted penis as a scrub brush to remove the sperm other males. Males of a finch-like bird called the dunnock33 take a less sophisticated approach, simply pecking at the female's cloaca before mating to remove whatever sperm is in the orifice at the time.
Sexual pleasure in fish versus humans. As we have shown, there are plausible adaptive reasons for particularly intricate and intimate acts of coupling in the basking shark and priapiumfish. If our interpretation is correct, these fishes do not necessarily experience sex much more profoundly34 than do the fishes - mentioned at the start of this essay - which have dispensed with intercourse. The basking shark and priapiumfish certainly have ample hardware, but sexual pleasure is likely to be ultimately about software.
Perhaps the ultimate example of software in action is our own practice of sex. The human species is one of the sexiest known, in the sense that we practise copulation not only for reproduction but also for its own sake: an enjoyable and involving form of recreation. There is little evidence that any fish, including monogamous species, practises sex for its own sake as we do. Yet human genitalia, compared to those of the cold fishes to which you have been voyeur, are in physical terms something of a let-down. It is our extremely developed mind and nervous system, rather than genital complexity itself, which are likely to lay the sheets of meaning on our rich experience of sex. No pornography could do justice to what it might be like if – beyond fantasy – the human capacity for sexual software were accompanied by a penis with as much sexual hardware as that of the basking shark, let alone that of the priapiumfish.

1 Chondrichthyes: Lamniformes: Cetorhinidae: Cetorhinus maximus

2 The two phalluses, each up to 1 metre long, are symmetrically arranged on left and right, being derived from part of the pelvic fins. Only one phallus is used during a particular copulation.

3 The genital teeth are more than three centimetres long whereas the oral teeth are only 5-6 millimetres long.

4 The oral teeth of the basking shark are extremely small relative to its mature body mass of ca 5 tonnes.

5 This was called a ‘claw’ in a detailed description of the species but is more accurately described as a specialized and enlarged denticle, composed of the same type of enamel as the oral teeth of sharks. Once the phallus enters the female, it lodges by means of this genital tooth which is flexed sideways to anchor into the tough fibrous lining of the vagina. During the normal quiescence of the phallus, the genital tooth and its articulating base are folded to rest parallel to the shaft of the phallus.

6 consisting of many spermatophores, which are discrete packages of sperm surrounded by membranes, and therefore tending to form a jelly-like cohesive mass rather than flowing

7 consisting of many spermatophores, which are discrete packages of sperm surrounded by membranes, and therefore tending to form a jelly-like cohesive mass rather than flowing

8 Each phallus is reinforced by 16 rods and plates of ossified cartilage in a flexible arrangement which allows erection.

9 There is a pair of siphon sacs, consisting of one sac on the right and another on the left, which corresponds to the pair of phalluses. The sphincters of the sacs open at the base of the phallic grooves.

10 Order Atheriniformes: family Phallostethidae: Phenacostethus smithi. The family name is derived from the ancient Greek for ‘phallic erection’.

11 Even those species of cartilaginous fishes which are oviparous lay relatively few, large, carefully placed eggs; indeed the eggs of some sharks are the largest known cells.

12 The basking shark is ovoviviparous.

13 Because the external genitalia of the basking shark and the priapiumfish are so complex, we use the word ‘phallus’ to refer to a single intromittent organ, and the word ‘penis’ and ‘penile’ to refer to the whole kit including one or more phalluses.

14 We chose the basking shark mainly because it is exceptionally well-documented.

15 Usually called a clasper, a misleading term which we avoid.

16 In the basking shark each phallus corresponds to one of the two claspers.

17 Usually the one on the right-hand side in several species of sharks.

18 Or priapium.

19 Toxactinium.

20 Ctenactinium.

21 Pulvinulus.

22 Toxactinium, pulvinulus, ctenactinium, and genital papilla, in order from front to back.

23 Baculum.

24 Humans, unlike many other mammals, lack a baculum.

25 Located inside the cloaca.

26 Or clasper.

27 Ctenactinium and pulvinulus respectively.

28 Toxactinium.

29 See diagrams in Te Winkel L E (1939) The internal anatomy of two phallostethid fishes. The Biological Bulletin 76, 59-69, and Mok E Y-M & Munro A D (1997) Some anatomical and behavioural aspects of reproduction in members of an unusual teleost family: the Phallostethidae. Journal of Natural History 31 (5).

30 ‘reverse-thrusting’.

31 Scientific name to be inserted.

32 Drosophila melanogaster.

33 Prunella modularis.

34 In the sense of peaks and nuances of desire and fulfilment.

(writing in progress)

Posted on June 13, 2022 08:31 AM by milewski