The Sensual Sea
Story and Photographs by Doug Perrine
In the game of evolution, the winner is the organism that dies with the most copies of its genetic code replicated in successive generations. Nearly all creatures more advanced than 
bacteria use sex as the most effective method of accomplishing this goal, although some utilize other methods of reproduction as well. Sex is the most important progress in life on earth since the advent of multi-cellular organisms. Sex is the means by which genes are reshuffled, creating the variability upon which natural selection acts. Without sex, the only source of variability is mutation, which occurs naturally at a rate of one in every million or so replications - way too slow to produce the explosive adaptive radiation that covered the continents with dinosaurs, and later mammals, and filled the seas with 25,000 species of fish, plus marine mammals, marine reptiles, and innumerable species of sexually-reproducing invertebrates.
Sex creates variation from which nature can “choose” the fittest combinations. This allows a species to become fitter, and adapt to changing environments. Sex is more important than survival. Survival without reproduction is a genetic dead end, while reproduction followed by death leaves offspring to continue the genetic line.
It is no wonder then, that many animals will abandon their normal caution in pursuit of sex. It is also no surprise that predators, including humans, have learned to take advantage of this indiscretion. Three-spot damselfish rarely leave the shelter of the reef, except in early morning when they may dance a meter above the reef at the peak of a spawning loop. This is the moment when they are most likely to vanish into the jaws of a trumpet fish. Male sea turtles are so reluctant to abandon a female, once they have mounted, that they will endure severe injury by other males attempting to displace them. Knowing this, fishermen capture pairs of turtles by swimming to a mating couple and tying a line around the female’s flipper. The male holds on tight as she is pulled over to the fishing boat.
Predators may target eggs rather than parents. Whale sharks appear during mass spawnings of fish and corals to vacuum up eggs and egg-eating plankton. For some organisms, including salmon and most octopus and squid, sexual reproduction is soon followed by death, allowing the parent to put all of its resources into the survival of the offspring. After mating, with certain death on the way, a female octopus has no further use for a male, and may have one for her last meal, to give her additional strength to see the eggs through to hatching.
Some species, like humans, have adapted sex to purposes other than reproduction. Dolphins use sex to reinforce social bonds, establish dominance, and for recreation. They do not restrict their sexual activities to those approved by humans. Typical dolphin activities, if performed by humans, would be classed as gang rape, child molestation, incest, sodomy, bestiality, homosexuality, and promiscuity. Sex is so casual, scientists quip, that to a dolphin, “It’s like a handshake.”
This broad spectrum of sexual modes and partners is common among marine mammals, including manatees, sea lions, and seals. Among the most mysterious is the humpback whale. Humpbacks migrate to breeding grounds where they give birth, and presumably mate. However, there is not a single reliable recorded observation of humpbacks mating. I have perhaps come as close as anybody to witnessing this arcane event. I have often seen humpback whales engaged in what appears to be courtship. On three occasions, I have seen couples where one member had the penis extended 2-3 metres outside the body (it is normally hidden). In two of these cases, however, both partners turned out to be male.
Given the many different organisms that reproduce sexually, we should not be surprised that evolution has produced many variations on the sexual process. In many marine organisms, gender is not as clearly defined as in our own kind. In turtles, crocodiles, and some shrimp, there are no X and Y chromosomes that determine the sex of the offspring. Instead, gender is determined by environmental factors. In sea turtles for example, sex is determined by the temperature of the nest. High temperatures produce all females, low temperatures produce all males, and median temperatures produce mixed nests. By our tampering, such as removing shoreline vegetation or moving nests to shaded or unshaded hatcheries, we may be skewing the sex ratios of populations. Certain beaches in Florida where eggs were collected and incubated in Styrofoam coolers may have produced only males for years. Climate change may eliminate males from some populations altogether.
Other creatures change gender during their lives, or may be both male and female at the same time. Nudibranchs are simultaneous hermaphrodites. During sex, they perform male duties at one end, and female duties at the other. Afterwards, both partners crawl off to lay a ribbon of eggs. Some flatworms, also simultaneous hermaphrodites, have reproductive dynamics that give males the edge in producing more offspring. When two meet, both rear up, evert their dagger-like penises and stab at each other. The winner of the duel punctures the loser’s body wall and injects sperm, fertilizing the loser’s eggs.
Some hermaphrodites are less simultaneous than others. Hamlets (small seabasses) play one sexual role at a time. A spawning pair circles around until one member releases eggs, and the other sperm. Then they reverse direction, and roles.
Many larger basses, such as Nassau groupers, are sequential hermaphrodites, changing from one sex to the other during their lives. Most sex-changing groupers are protogynous i.e. maturing first as females, and later becoming male. However some females never change sex, and some males may not pass through a female stage. Nassau groupers are normally solitary. Annually, they swim many miles to join spawning aggregations. They spend days to weeks preparing for the main event, gathering in tens of thousands, flashing different colour patterns at each other. On the final evening, males abandon their normal diagonal brown stripes in favour of a black & white “tuxedo”. Clusters of males surround individual females, which dash to the surface, releasing their eggs into a cloud of sperm.
Some groupers are simultaneous hermaphrodites when young, but switch to male later in life. In some cases, the males maintain harems of hermaphrodites. The hermaphrodites mate only as females with the harem master, but may also mate as males with each other. In other cases, the harem master is also a hermaphrodite, and mates only as a male with its concubines, but may mate as a female with the harem master in another territory.
Many parrotfishes and wrasses are also protogynous sequential hermaphrodites. The terminal phase is often a “supermale” that is larger, more colourful, and more dominant than initial phase fish, which may also include males. Sexual dynamics vary between species. Supermales are often sex-reversed females, but in some species, initial phase males may also progress to terminal phase. Some species have several alternative life history patterns.
In the Caribbean blue-headed wrasse, only terminal-phase males have blue heads, while initial phase males and females and juveniles are all yellow. Supermales dominate spawning, as they are able to maintain spawning territories along the perimeter of the reef, which attract females. Initial phase males participate in group spawning and also sometimes spawn as “sneakers” or “streakers” - dashing in to release sperm just as a female is spawning with a supermale. Initial phase males, however, have lower reproductive success than terminal males. The number of available territories is a function of the circumference of the reef, and the number of terminal males is in direct proportion to that figure. The overall ratio of males to females in each population is also a function of the size of the reef, and can be mathematically shown to optimize the reproductive potential of the population. The mechanism by which the gender of each fish is determined is unknown. In other wrasse species, gender is socially determined - it depends upon the sex ratio already present in the population.
In anemonefishes and in the parasitic isopod Anilocra (segmented “bugs” that attach to the heads of reef fish), sex determination is by chemical control. Both are protrandrous (male first) hermaphrodites. The largest and most dominant fish in an anemone is the female. There is usually one male, and some smaller non-reproductive fish. The female exudes a pheromone that prevents the male from changing sex. If the female dies or leaves, the male becomes a female, and one of the juveniles becomes a male. Likewise in Anilocra, the large visible individual is a female, which exerts chemical dominance over much smaller males which also live on the host fish. If something happens to the female, one of the males takes her place.
In some organisms, the two sexes start out as different individuals, but merge into one body. In deep-sea anglerfish, spoon worms and parasitic barnacles, the male starts out life as a free-swimming larva, follows a chemical trail to the female, enters her body, and is absorbed, becoming little more than a clump of sperm-producing cells. Spoon worms boast the animal kingdom’s greatest disparity in male and female body sizes. An eight-centimetre female can contain a male only one to three millimetres long. By contrast, most angelfish and butterflyfish lead boringly conventional sex lives. Both sexes look alike; most mate for life and are rarely seen more than a few metres from their mate.
Some sea creatures maintain conventional sexual identities, but reverse the normal parental roles. In most damselfish, jawfish, cardinalfish and seahorses, the eggs are brooded by the male (in the mouth for jawfish and cardinalfish). In one species of frogfish, the female lays eggs on the side of the male’s body, where he cares for them until they hatch. Male seahorses have a ventral pouch where the female deposits the eggs for brooding. A different type of role reversal occurs in one type of mantis shrimp, where females aggressively pursue males, sometimes injuring them as they strike them with their claws.
Some brine shrimp have dispensed with males altogether, and form all female “Amazon” populations. Sponge shrimp colonies are mostly female, but, like bees and ants, produce a few drone males to fertilize the queen’s eggs. As with social insects, the queen shrimp is the only one that reproduces. The worker castes are all sterile females.
Many sea creatures ensure successful mating through elaborate behavioural rituals, costume changes, and communication via visual, audible, chemical, and electrical signals. Neon-like colour patterns shift over the bodies of unicornfish, squid, and cuttlefish during courtship. The foghorn-like booming of toadfish trying to attract a mate and the songs of male humpbacks in breeding season can be deafening underwater. Small reef fish often swim ritualized “dance” patterns and/or flash bright patterns hidden under their fins. Stone crabs scratch the striated “fingerprints” on their claws to “telegraph” the opposite sex, while fiddler crabs raise a brightly coloured claw and wave it around. Flashlight fish, like fireflies, blink lights to coordinate their night time reproductive activities. Deep-sea fishes most likely use bioluminescence for sexual communication - some skates can apparently signal each other in the dark for sexual purposes using electrical impulses. Females of many species release pheromones that attract males. Whales, dolphins, manatees, turtles, rays, and sharks are among the organisms where a female in heat can attract a “rowdy group” of males, which may seriously injure each other while competing for access to the female.
Reef squid compete for mates more safely using colour displays. A male will often display one pattern on the side of his body facing the female he is courting, and another pattern on the opposite side, directed toward a competing male. Male Right whales do not fight for mates like sperm whales and humpbacks, but rather compete to produce the most semen - the more the better to wash out the seed of the female’s last mate and replace it with their own. This “arms race” has produced the largest gonads in the animal kingdom. The two testes can weigh over a ton. The penis is also a natural wonder, perhaps the longest on earth, but relatively narrow and flexible. It looks like an aircraft refuelling hose with an internal guidance system, able to locate and connect with a moving, and often resistant, target that is out of sight and 10 metres or so away from the whale’s head is quite remarkable. Successful copulation may depend on the presence of other suitors who restrain the female, then may take a turn afterwards.
Sharks may injure their mates as well as their competitors. Sharks utilize the more advanced reproductive strategy of internal fertilization and live birth. They do not merely spawn, or release gametes in the vicinity of their partner like most bony fish, but actually mate. The male shark has two penis-like organs, called claspers. However, he has no appendages equivalent to hands with which to grasp his mate. He uses his teeth for this purpose, often inflicting deep wounds on the female. Internal fertilization is also practiced by rays, chimaeras, marine reptiles, mammals and a few types of bony fish.
Most invertebrates are spawners, but some practice crude forms of internal fertilization. Cephalopods use an elongated arm or tentacle to slip a sperm packet inside the female’s mantle, which is probably a wise strategy, given the female’s predilection for cannibalism in some species. Some barnacles use a penis (the longest in the animal kingdom in proportion to body size), to squirt sperm into their neighbour’s shell.
In some corals, all polyps in a colony are of the same sex. Male colonies release sperm at the same time the female colonies spawn eggs. Other corals are hermaphroditic. During spawning, each polyp spits out a bundle that looks like a big egg, but is actually a bunch of small eggs and sperm all packaged together. The package opens at the surface, and the gametes go looking for “partners", but miraculously avoid fertilizing each other. Releasing eggs to the currents is called “broadcast spawning”. Some types of corals and sponges are broadcast spawners, but others are brooders, with the males releasing sperm into the water, and the females drawing it into their body cavities to fertilize their eggs. Broadcast-spawning corals and sponges need to coordinate their releases. It is believed that the actual release is a chain reaction, triggered by chemical signals from the first individuals to go off, but that the preparation is prompted by a variety of cues, including lunar phase, water temperature, tide level, day length, etc. A mass spawning can look like an underwater blizzard. In some areas multiple species coordinate their spawning on the same night, overwhelming the ability of egg predators to consume the vast amounts of material released.
While sexual reproduction is dominant among most creatures large enough to be visible to the naked eye, asexual reproduction is also important. Fragmentation - reproducing from 
broken bits - is an important method by which corals, sponges and other creatures can recover from a disaster and repopulate an area after a storm. Some corals and anemones can clone themselves by budding and/or fission. Some sea stars can reproduce either sexually (by spawning), by fission (splitting down the middle), or by autotomy (casting off a part which then regenerates the rest of the animal). Some can grow an entire body from a single cast-off arm. Sponges are the regeneration champions. In laboratory experiments, sponges have been ground up in a blender, then strained to separate the cells, and the cells were able to reform themselves into a new sponge!
In the sea, sex is all around you all the time. Dawn and dusk dives are generally preferred by subsea voyeurs as many reef fish spawn at these times. However, it is a rare dive where some type of reproductive activity is not occurring. Even clear seawater contains substantial portions of gametes and larvae, sometimes to the dismay of those who have personally discovered the connection between the spawning of the sea thimble jelly and the malady known as “sea bather’s eruption”. It is no wonder many divers describe their underwater experiences as highly sensual - they are actually swimming in a sexual soup!
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