Have Ecosystem, Will Travel

A posting came across SHARK-L : "A friend of mine was telling me that there are things that eat at sharks eyes and eyelids, like parasitic/symbiotic organisms. I haven't heard of any such things, . . ." I responded:

A shark is never "just" a shark, it is a mobile community of organisms living in intimate association with its fearsome host. In addition to a whole mob of parasites feeding upon the shark's various tissues or directly on food in its gut, there are also several fishes that are known to feed on shark exoparasites (external parasites) and others that feed on its nitrogen-rich feces (It's a living!). But your question is about critters that nosh on shark eyes and eyelids.

The great 19th Century Irish satirist Jonathan Swift (of Gulliver's Travels and The Drapier's Letters fame) was among the earliest literary types to notice how wide-spread are such 'nested' communities when he wrote in his Poetry, A Rhapsody (1733): "Great fleas have little fleas upon their backs to bite 'em,/And little fleas have lesser fleas, and so ad infinitum.". Sharks' too, have countless lesser creatures which feed upon their various body parts, from mucus between the lips and gums to undigested foodstuffs in the gut. The sheer variety of these lesser dinner guests is nothing less than astonishing: crustaceans (copepods, isopods, and barnacles), nematodes (roundworms), platyhelminths (cestode tapeworms, monogenean and digenean flukes), hirudinoideans (leeches), molluscs (bivalves), protozoans, and uncountable legions of bacteria. A shark is thus a swimming bestiary of strange and underappreciated critters that, in their wondrous diversity, rival anything to spring from the imaginations of Disney or Tolkein.

Perhaps the best known creature that dines on sharks' eyes is a strange, 3-centimetre-long, pinkish-white copepod known as Ommatokoita elongata, which permanently attaches itself to the corneas and associated tissues of the Greenland Shark (Somniosus microcephalus). You can find gorgeous photographs of this creature attached to the eyes of free-swimming Greenland Sharks in the September 1998 issue of National Geographic magazine (pages 60-71).

Greenland Shark (Somniosus microcephalus)

The 6- to 7-metre-long Greenland Shark is basically an overgrown dogfish (order Squaliformes, family Somniosidae) and widely regarded as preternaturally sluggish. There are numerous stories of Innu baiting these sharks to the surface with seal entrails, whereupon they are hauled out of the water bare-handed like so much wet laundry. So, despite its size and sharky appearance, Somniosus microcephalus is a sort of 'couch potato shark'. Thus, it has long been something of a mystery how this supposedly sluggish and slow-moving creature could manage to catch such speedy fish prey as herring, salmon, char, smelt, cod, ling, haddock, and rockfishes. (This shark is also known to consume slow, bottom-dwelling fishes such as flatfishes, sculpins, lumpfish, skates and their eggcases, as well as jellyfishes, squids, crabs, amphipods, marine snails, brittle stars, sea urchins, sea birds, and marine mammals, such as narwhals and Arctic seals [possibly taken as carrion] and terrestrial mammals such as horses and reindeer.)

In a 'classic' 1961 paper (Nature, vol. 191, no. 4790, pages 829-830), Norwegian fisheries biologist Bjorn Berland found that 1,270 (84.4%) Greenland sharks taken in east Greenland waters were afflicted with O. elongta, usually one on each cornea. Based on its conspicuous paleness, Berland suggested that the copepod may be bioluminescent and thus serve to lure potential prey to the shark. If true, this would make the relationship between the copepod and the shark mutualistic rather than parasitic in nature*. Unfortunately for this nifty theory, recent (as-yet unpublished) work by American shark parasitologist George Benz has revealed that O. elongta is not bioluminescent. The fact that O. elongata is not bioluminescent does not  of itself  preclude the idea that the conspicuous copepod may lure potential prey within striking range of the host shark, but it does weaken the case somewhat. Further weakening the case is recent observational and circumstantial evidence that the Greenland shark is not nearly as sluggish as it was long supposed to be: there are several reports by credible Canadian wildlife biologists of Greenland Sharks in Arctic Canada actively grabbing caribou (= reindeer) that ventured too close to the waters edge (in a manner reminiscent of Nile Crocodiles ambushing Wildebeast and zebras at African waterholes) as well as a curious phenomenon of numerous Grey Seals off Sable Island with their blubber-rich skins ripped off in a bizarre spiral pattern, for which the investigating biologist feels the Greenland Shark is responsible.

O. elongta does significant damage the cornea of its host. Although the Greenland shark usually has only one copepod per eye, Berland (1961) deduced that the round scars over the cornea of these sharks are probably former attachment sites of the parasite. At the most recent meetings of the American Elasmobranch Society (1998, Gulph, Canada), histologist J.D. Borucinska presented a paper of research carried out with George Benz on corneal pathology associated with attachment of O. elongta to the eyes of the Greenland Shark. Borucinska and Benz examined the eyes of six Greenland Sharks infected with O. elongta. They found that the scraping/grazing mouthparts of O. elongta (which can be seen in a startling electron microscope image on page 69 of the aforementioned National Geographic article) create significant damage to the corneal tissue of the host shark, including a 50% thickening of the limbus epithelium, inflammation and massive edema (fluid accumulation) of corneal cells. Borucinska and Benz concluded that the activities of O. elongta severely compromise vision in host sharks and thus the relationship between them is clearly parasitic rather than mutualistic. (I rather like E.O. Wilson's definition of a parasite as, "a predator which eats its prey in units of less than one.")

While copepod parasites are occasionally noted from the eyes of other species of sharks (while diving off San Diego, I have personally seen a pandarid copepod attached to the left eye of a free-swimming subadult Shortfin Mako, Isurus oxyrinchus), in no other species is their occurrence as regular or as well documented as O. elongta noshing on on the corneas of the Greenland Shark, so this is very probably the symbiotic relationship to which your friend was referring. In any case, I hope you found this posting of interest.

Cheers,

 R. Aidan Martin

*NOTE: although many people use the term 'symbiosis' as a synonym of mutualism, in the broadest sense of the term, a symbiont is simply an organism of one species that lives in association with another. Thus, parasitism (one partner benefits at the expense of the other, termed the 'host'), commensalism (one partner benefits while the other is not directly harmed or benefited), and mutualism (both partners benefit) are all symbiotic relationships. [Return to Text]