Shark Science Blog

Future Predators Avoid Becoming Prey

Electroreception is the ability of certain marine vertebrates to detect minute electrical charges transmitted through the water.  The shark electroreceptor system is composed of sensory organs called ampullae of Lorenzini, that lie within small pores across the head of the shark.  All animals emit low level electrical fields generated by the activity of their cells, and this highly sophisticated system allows sharks to detect minute changes in the surrounding electrical field.  These electrical signals help them localize and identify nearby prey, enhancing their visual hunting abilities. 

A prey species finding itself in the vicinity of a hungry shark therefore seems doomed to become a meal.  After all, he can’t alter his electrical field.  Or can he?  If that prey is a developing shark, with its own sensory system beginning to come online, it seems he can use these early electroreception abilities to avoid becoming a meal himself, at the teeth of another shark or other predator.

In work recently published, Kempster et al examined the electroreception abilities of embryos of the Brownbanded bamboo shark (Chiloscyllium punctatum).  These small sharks are oviparous, completing their development within egg cases, the leathery structures that female sharks attach to sea grasses and other substrates.  The egg-encased, tethered embryos have no ability to flee from approaching predators.  As they near the end of their development, the shark egg cases open to the water, and both transmit and receive electrical signals.

When Kempster et al exposed embryonic bamboo sharks to small electrical fields that resembled those of other sharks or large fish, the embryos immediately became very still and stopped all gill movements – in effect they “held their breath”.  These actions are likely to diminish both the electrical changes caused by the respiration of the embryos, as well as any physical movement of the water that might give away their presence.  The response was strongest in the older embryos with more fully developed electroreception systems.  The young sharks couldn’t be fooled again, however, when the same artificial stimulus was given half an hour later – perhaps realizing that no actual predator appeared the first time – they no longer responded.

Kempster et al suggest that a better understanding of electroreception might inform the development of more efficient shark repellant devices, but even on its own this is an key insight into the survival mechanisms of developing embryos.

The article is: Kempster RM, Hart NS, Collin SP (2013) Survival of the Stillest: Predator avoidance in shark embryos. PLoS One 8(1): e52551.

And can be found open access at: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0052551

Photo credit: www.abc.au

Report from Oslob

It’s been a while since I wrote on this blog, mostly because I’ve spent the last year on sabbatical visiting whale shark aggregations around the world – Djibouti, Philippines, Mexico....  It’s a rough job but someone has to do it!  Seeing so many whale shark aggregations in a short time really lets you compare the animals, habitats and tourist operations.  The report below concerns a new whale shark tourism operation in Cebu, Philippines that I visited in April.  It was a disturbing situation, and as you will see had an even more disturbing follow-up.

Whale shark ecotourism operations exist in many countries that host seasonal aggregations of these animals. The docile nature and surface feeding behavior of whale sharks at coastal aggregations provides an ideal opportunity for tourists to observe and snorkel alongside these huge sharks. In many cases, ecotourism has replaced fishing of whale sharks, with former shark fishermen converting their boats and crews to staff the ecotourism operation. This can be a win-win situation for both the sharks and the local community - fishermen earn an equivalent or often greater income, while whale sharks receive protection as a renewable resource. Unregulated, however, ecotourism has the potential to endanger the very animals it should protect.

As a set of guidelines to protect whale sharks, nearly all ecotourism operations have adopted a code of conduct first established by the Australian government for ecotourism at Ningaloo Reef. This code stipulates that 1) only one tourist boat should interact with a shark at one time, 2) no more than six snorkelers should be in the water with a shark at any time, 3) snorkelers must maintain a distance of three meters from the shark, and 4) snorkelers may not touch the shark or block its movement. When followed, as they are to varying degrees in different countries, these regulations ensure a safe and enjoyable whale shark experience for tourists with minimal impact on the sharks.

Recently, the town of Oslob, Cebu, Philippines, has started a different sort of whale shark ecotourism. For a number of years, fisherman in Oslob have been hand feeding a group of whale sharks, dropping small amounts of shrimp (locally called uyap) into the water as the sharks follow behind the boats. They began this practice to lead the sharks, which they considered a nuisance, away from their fishing areas. Last year tourists began coming to see the “friendly” whale sharks up close, and the fishermen realized they could also use uyap to lead sharks towards the shore, and charge tourists to see the animals. When this story hit the international news in November of 2011, the tourism industry in Oslob exploded. Large numbers of tourists began arriving in Oslob, and more fishermen began offering whale shark interactions.  Within weeks the crowds arriving in Oslob grew from the dozens into the hundreds, and the situation quickly became chaotic with no infrastructure yet in place. There were reports of sharks being injured by boats, and being touched and ridden by tourists.

The conservation group Physalus, run by Italian researcher Ale slot machines online Ponzo, has been studying whale sharks in the Philippines for the past two years, and they were early observers of the Oslob situation. Seeing the need for regulation of Oslob whale shark tourism, Physalus took on the role of advisor and monitor for this evolving operation. Since December of 2011, they have been monitoring the interactions between tourists and sharks, and working with the local government to provide structure and oversight to ensure tourist and shark safety.  Working in the Philippines with Physalus this past April, I had a chance to visit Oslob and survey the situation there.

Arriving in Oslob late in the evening after a 3-hour bus ride from Cebu City, we found many small resorts in various stages of construction, evidence of the rapidly growing tourism.  The following morning was Good Friday, the beginning of the Easter holiday weekend. Tourists began arriving at the interaction site by 8am, and the numbers grew quickly; we would later learn that crowds that day reached 1500 people. Even before reaching the water, the impact of this tourist influx is clear. The small road along the shore is crowded with tourist transport ranging from the sidecar-equipped motorcycles called tricycles, to huge commercial tour buses. Along the beach, the large number of tourists has spawned a host of cottage industries, with impromptu restaurants and souvenir stands, operators hawking other local tours, and always the hammering of new construction.

At the time I visited Oslob, the first set of tourism regulations had just been put into place. There are roughly 100 boats participating in the whale shark interactions, small outrigger boats called bancas that each carry two crew and 4-6 tourists.   It had been decided that only 25 boats would be on the water at any time, and they were to form two lines 5 meters apart. A “feeder” boat would then lead the whale shark between the boat lines so the tourists could observe the animals. While many people were happy to see the sharks from the boat, others got into the water, often hanging onto the outriggers of the boat. There are also several dive operations that work the aggregation site, and while the dive boats must stay outside the interaction area, as many as 20 divers may enter and move under the sharks. Physalus observers who had been in Oslob for several months said these new regulations created a more organized operation, as previously the tourist boats simply massed around the feeder boat and shark.

Watching both from the shore and the water, however, it was difficult to imagine how the scene could have been any more chaotic. The boats frequently moved off the lines, giving the sharks far less than 5m of space.  When the water is rough, as it was that weekend, the massed boats begin heaving in the swell, with their outriggers hitting each other as well as swimmers and sharks. We saw sharks run over by boat outriggers, and swimmers in the water nearly hit by adjacent boats. One small boat capsized when too many snorkelers climbed onto one outrigger, and all passengers were dumped into the water. Beneath the surface, divers must try to avoid the boats, the snorkelers and the whale sharks. As the water is only 25-30 feet deep, there is little room for the divers to move an adequate distance away. Inevitably there is much touching, accidently and intentionally, and it is quite difficult to police actions beneath the surface.

There are concerns for the whale sharks that come to this area. Many sharks show injuries to their mouths and heads, consistent with damage from the boats. These sharks have also come to associate humans and boats with food; this familiarity could have a devastating effect if these animals move into waters where hunting of whale sharks persists. There is also the concern that while the Oslob sharks are getting an easy meal, it is a very limited diet in both quantity and variety. Studies of whale sharks in other aggregations have shown that a small 4 meter whale shark typically eats 11 kilograms of food per day. The sharks in Oslob, usually several animals per day, share uyap totaling only a few kilograms.  The animals may spend as long as 8 hours per day at the site, leaving them little opportunity to feed elsewhere.

As I was returning to Manila, Dr. Ponzo was meeting with the Oslob mayor and city council to offer the results of Physalus’ observation of these interactions, and to recommend guidelines for ongoing whale shark tourism.  The primary changes suggested include limiting the number of boats that can be in the water at one time, and the length of time they can spend there, and enforcing the existing regulations on boat and swimmer distance from the shark. Though the situation in Oslob appears to be stabilizing and hopefully maturing, neighboring towns have recently announced that they would also be feeding whale sharks for tourists. While whale sharks may be largely safe from hunting in Philippine waters, Filipinos may end up loving their whale sharks to death.

Do Sharks See Color?

Elasmobranchs have highly developed sensory systems that help them find food - a sense of smell that can detect prey at long distances, and the ability to read the minute electrical fields emitted by fish.  But what about their vision?  Do sharks see in color? Two recent studies use biological and behavioral tests to try to understand how sharks and rays perceive their world.

The retina of the eye of most vertebrates contains specialized cells, called photoreceptors, that detect light.  The pattern of light falling on the retina is converted into a neuronal signal that is sent to the brain, and the brain then interprets the signal, changing it back into the “picture” seen by the eye.  Light exists along a spectrum of wavelengths, and in the visible range these are perceived by the brain as different colors.  The blue end of the color spectrum is made up of light of shorter wavelengths, while the red end of the spectrum is composed of light of longer wavelengths.

Most vertebrates have two main types of photoreceptors, rods and cones.  Rods are highly sensitive cells that can detect very small amounts of light, but they do not discriminate color.  Cones are activated by larger amounts of light, but they allow discrimination of different wavelengths of light, i.e. colors.  True trichromatic color vision comes from having three different cone photoreceptors detecting wavelengths in the red, green and blue ranges.  Specific colors are interpreted by the varying degrees of activation of these three photoreceptors.

Experiments by Hart et al tested the isolated photoreceptors taken from 17 different species of shark, measuring the wavelength of light each is able to detect.  They used microspectrophotometry, which passes a range of wavelengths of light across a section of retinal tissue, and measures the wavelength(s) absorbed by the photoreceptors in that tissue.  Each shark species was found to have only a single rod photoreceptor that captured a single wavelength of light, and no shark had more than a single cone photoreceptor.  In fact, in 10 of the 17 shark species they were unable to find any cones at all!  This means that that these shark species have little or no ability to discriminate colors.  A complete lack of color vision is rare in terrestrial animals, which typically have two or three different cones and at least some degree of color vision.  It may be common in the marine environment, however, as whales and dolphins are also thought to be color blind.  It has been proposed that in some marine mammals a rudimentary sort of color vision may be achieved by comparing the wavelengths of one rod and one cone photoreceptor, but more data is needed to confirm this hypothesis.

Among the different species of shark, the wavelengths of light detected by their single cone photoreceptors varied across a wide range.  The ideal wavelength for a given species is determined to a large degree by the depth at which they live.  Longer (redder) wavelengths of light are quickly lost with increasing ocean depth, while shorter blue wavelengths penetrate more deeply.  Shallow water species therefore often have photoreceptors detecting redder light, while deeper species have photoreceptors detecting predominantly blue wavelengths.  The authors also note that deeper species might benefit from a blue range photoreceptor to help them see bioluminescent deep water animals, who usually emit a light in the blue range.

Additional work addressing this question comes from Van-Eyk et al, who realized that while laboratory techniques can determine a species’ ability for color vision, whether or not sharks are able to see and respond to colors requires behavioral assays.  They tested the color vision capabilities of the shovelnose ray (Glaucostegus typus).  In contrast to sharks, most ray species are known to have three different types of cones detecting different wavelengths of light.  This is not the first time behavioral tests have been used to analyze elasmobranch color vision, but a confounding factor of previous studies was that they did not control for the differences in brightness among the colors tested.  A bright yellow versus a dark blue, for example, could cause animals to react to the brighter target without discriminating its color.

To circumvent this problem, Van-Eyk designed a color discrimination test that also controlled for brightness.  The rays were kept in a large training tank, and trained to touch a blue colored panel with their nose to obtain a food reward (Mmm, shrimp paste).  Once trained, they were tested for their ability to identify that same blue panel against a background of gray panels of varying brightness.  They were then presented with multiple targets, all blue but with a range of lighter and darker blue tones.  The sharks therefore had to discriminate blue from grey, as well as different shades of blue from the original training blue.  In both assays the rays performed significantly better than would be predicted by chance; they selected the correct target between 62% and 100% of the time.

These data provide strong evidence for color vision in the greater shovelnose ray, and likely in the many other ray species that have multiple photoreceptors.  So why are most rays able to see color while most sharks likely cannot?  Rays typically live a different lifestyle than sharks, inhabiting shallower water illuminated by light of multiple wavelengths.  It may be that rays are better able to make use of color vision than sharks that spend much of their time at depth.  It’s unlikely rays use their vision in feeding, they are largely substrate feeders who don’t find their prey by sight.  The upper levels of the water column suffer from a significant degree of “flicker”, the ripple effect of light near the surface as waves move the water.  So one advantage may come from the ability to more easily spot predators, who may use flicker as a sort of camouflage against species without color vision.

The papers are:
Microspectrophotometric evidence for cone monochromancy in sharks. Hart, NS, Theiss, SM, Harahush, BK and Collin, SP (2011) Naturwissenschaften 98:193-201

Behavioural evidence for colour vision in an elasmobranch. Van-Eyk, SM, Siebeck, UE, Champ CM, Marshall J and Hart NS. (2011) Journal of Experimental Biology 214:4186-92.

Shark Strandings Investigated

Sharks strand, or beach themselves, with some frequency in certain coastal areas.  This phenomenon is seen in other marine creatures as well, and is particularly common in dolphins and small whales.  It’s a frustrating occurrence, as the cause for strandings is rarely known, and most stranded animals eventually die.  Even in cases where the animal is helped back into the water, it will often strand again.  It is usually assumed that stranded animals are sick, or compromised in some way, and have lost their ability to navigate and/or survive at sea, but rarely is the specific cause found.

In one of the most interesting investigations of recent strandings, it was found that mass strandings of whales were likely a result of the use of navy sonar devices in the area.  Necropsies of the animals found gas bubbles in their tissues.  This is indicative of decompression sickness, what divers call the bends, and typically results from surfacing too rapidly from depth.  It is believed that the whales may have dived and surfaced rapidly to escape the discomfort of the sonar on their sensitive hearing.  These data led to regulations on sonar use when conducted in areas that whales frequent.  In other cases, mass strandings are thought to be a result of poisoning by the toxic algal blooms known as red tides.

In a recent paper by Schaffer et al, another potential cause of stranding is identified.  The authors observed that significant numbers of juvenile salmon sharks (Lamna ditropis) strand along the northern California and Oregon coasts each year.  They collected and necropsied 18 salmon sharks, both fresh and preserved carcasses, that stranded and died between 2002 and 2007.  Upon initial observation they observed that the meninges, the membranous coverings of the brain, showed signs of inflammation.  Various regions of the brain itself also had many inflammatory immune cells, typically a response to some sort of infectious agent, and in some cases abscesses filled with bacteria were seen.  When the shark’s livers were available for analysis these also showed signs of severe infection.

In many of these sharks the bacteria could be cultured, and were then subjected to DNA analysis to identify the species.  The authors sequenced the 16S ribosomal RNA gene of the isolated bacteria, a region of the genome commonly used to identify bacterial species.  This analysis showed the bacteria to be a Carnobacterium, likely the species Carnobacterium maltaromaticum.  This is a common bacteria in various marine creatures, though it had not previously been found in sharks.  In fish, it typically causes no pathology to its host, but in some cases may result in sickness and death.  The bacterium was not seen in any of the control sharks analyzed in this study.  Interestingly, all the bacteria isolated from the different sharks (which stranded in different coastal areas) were genetically identical, without even the small genetic differences expected of separate bacterial isolates.  This suggests there may be a single source from which all sharks acquire the bacteria.

Meningitis has occasionally been found in stranded sharks before, but its role in the strandings was unclear.  The nearly 100% incidence of this disease in the stranded juvenile salmon sharks provides compelling evidence that this is likely to be the cause of the stranding.  Meningitis can cause disorientation and confusion, which might lead the sharks to strand inadvertently.  Identifying the source of this bacteria, and understanding why it appears specific to juvenile salmon sharks, may help to prevent loss of these animals in the future.

The article is: Schaffer, PA, Lifland, B, Van Sommeran, S, Casper, DR, and CR Davis. (2012) Meningoencephalitis associated with Carnobacterium maltaromaticum–like bacteria in stranded juvenile salmon sharks (Lamna ditropis), Veterinary Pathology (online before print).

It can be found at: DOI: 10.1177/0300985812441033