Foraging by Seabirds on an Olfactory Landscape

Erica G Klarreich. American Scientist. Volume 88, Issue 2. Mar/Apr 2000.

In February 1990, Pierre Jouventin and Henri Weimerskirch of the Centre National de la Recherche Scientifique in Beauvois, France, reported the first successful tracking of a seabird with satellite telemetry. The seabirds they chose to follow were six male albatrosses-of the species Diomedea exulans, the wandering albatross-breeding on a small chunk of land called Possession Island, part of the Crozet Archipelago in the middle of the Southwest Indian Ocean. Until this time, scientists and seafarers alike had assumed the wandering albatross to range widely in its foraging habits. These birds have historically been company to sailors miles from shore, resulting in considerable sea lore about their mysterious habits. But not even folk tales matched Jouventin and Weimerskirch’s data: Satellite tracks of their six wanderers showed them traveling distances of 3,600 to 15,000 kilometers during an incubation shift. By now it is clear that albatrosses and other petrels routinely travel vast distances to forage at frontal zones-productive areas where cold water is driven to the surface, providing rich nutrients and zooplankton for foraging.

As an investigator interested in sensory navigation, I have been fortunate enough to have contributed an interesting twist to this developing story. My work suggests that procellariiform seabirds (which include the albatrosses, petrels and shearwaters) use an olfactory landscape superimposed on the ocean’s surface to locate these productive patches where prey is likely to be found. These findings supply only one possible piece in an intricate behavioral and ecological puzzle. But in the process of seeking answers to a subset of questions, my colleagues and I have learned a surprising amount about the challenges of conducting careful behavioral research under hostile and complex environmental conditions, and have even developed some ideas about practices that might help reduce the tremendous number of fatal encounters between seabirds and long-line fishing equipment.

Procellariiform seabirds (the “tubenose” seabirds) come in a variety of shapes and sizes, from tiny Wilson’s storm-petrels weighing less than 50 grams to giant wandering albatrosses with wingspans of over 3 meters. Nearly all make their living flying over seemingly featureless ocean in search of patchily distributed food resources such as squid, fish and krill. With few exceptions, members of this diverse order share an unusual feature among birds: Nearly all possess a well-developed sense of smell, at least by anatomical measures. Procellariiform noses are made up of an elaborate olfactory neuroepithelium designed for capturing and detecting odors in the environment, and their brains are equipped with large olfactory bulbs that process and relay information to higher centers. Many species are also readily attracted to fishy-smelling odors.

As a graduate student at the University of Washington, I had studied the cellular basis of olfactory homing in salmon. I was particularly interested in how salmon learn the scent of the home stream and use this odor memory to guide them back to their natal spawning grounds. Like any graduate student motivated to obsession by a doctoral dissertation, I had spent hours in the library scouring the literature on all manner of olfactory-mediated homing behaviors. I was familiar with reports about the proficiency of certain species of procellariiform seabirds at finding their way back to remote breeding colonies by using olfactory cues. Nevertheless, I considered such reports with a kind of naive skepticism. After all, the textbooks said that birds had a poor sense of smell, and petrels were not anything like salmon. Or were they?

Just as salmon home to specific streams to spawn, petrels were reported to home accurately to remote island breeding colonies using olfactory guidance. One of the species that had been studied most intensely at that time was the Leach’s storm-petrels nesting on Kent Island in the foggy Bay of Fundy off New Brunswick. Early studies performed by Tom Grubb and Betsy Bang at Bowdoin College’s Kent Island Biological Research Station showed that Leach’s storm-petrels lost their ability to relocate breeding colonies if their olfactory nerves had been transected, rendering them anosmic, or smell-blind. Birds with intact olfactory nerves could relocate their half-mile-long island home from as far away as Europe. More recent studies by Eduardo Minguez suggest that British storm-petrels may be able to recognize their burrows by nest-specific smells, perhaps emitted from the birds themselves.

For nearly seven years, I have been exploring the olfactory abilities of an assemblage of procellariiform seabirds in the sub-Antarctic waters near South Georgia Island in the South Atlantic. In particular, my colleagues and I have investigated birds’ responses to dimethyl sulfide (DMS), an odorous gas that is associated with areas of high primary productivity and also plays a role in global cooling. DMS is produced by phytoplankton, and emission rates are known to go up during grazing by zooplankton-which seabirds, in turn, eat. My work suggests that DMS and other aromatic compounds could provide a bird foraging over thousands of miles of open ocean with immediate information about whether it is in an area where food is likely to be found.

Sniffing Out Seafood

In the sub-Antarctic, nearly all animals rely to some extent on a small, shrimplike animal called the Antarctic krill (Euphausia superba). Krill is a primary component of the Antarctic food web, so all animals in this region-from small seabirds to gigantic whales-are in some way dependent on it. Some species feed directly on krill; others are secondary predators that consume fish and other primary predators of krill. Even for secondary predators the presence of krill can be a predictor of a food supply, since their desired prey is likely to be attracted to areas of high primary productivity or a concentration of krill.

Krill live in patchily distributed swarms. These swarms might cover just a few cubic meters or stretch across the area of several football fields. A krill swarm offers a food bonanza for a seabird lucky enough to encounter it. Finding one of these swarms, however, presents seabirds and fishermen alike with a complex and age-old problem: Where a krill swarm accessible to the surface is likely to form is not always easy to predict, and the search area usually includes thousands of square miles of open ocean. Even if an animal follows the proper cues, searching out a krill swarm in the vast open ocean resembles hunting for a needle in an enormous and constantly changing haystack.

No one knows how procellariiform seabirds pinpoint the likely position of a prey patch over vast expanses of open ocean. Black-browed albatrosses nesting on Bird Island near South Georgia in the South Atlantic have been satellite-tracked traveling as far as the coast of South America-a round-trip distance of over 3,000 kilometers-to retrieve a meal for a chick on the nest. Smaller white-chinned petrels have been tracked traveling similar distances to foraging grounds. How these birds know where to go to find food remains a mystery, but the olfactory landscape may tell them that they have arrived in the right general area, alerting them to locations where foraging hotspots are likely to be found. Once at a hotspotthe vicinity of a krill swarm or feeding aggregation-seabirds may follow local odor trails or visual cues, including searching for other birds foraging on prey patches. An albatross plunging into the water is a good indicator that food is at hand.

Smell is an attractive sensory modality for the task of locating a prey patch. A prey patch has a certain physical size, but the odor emanating from the prey occupies additional space, increasing the effective size of the patch and thereby the likelihood that a foraging petrel will encounter it. Although many animals can hunt by smell, any hypothesis based on olfactory cues presents special problems with respect to procellariiforms because the routinely traveled distances appear to be so great for many species. What role could olfactory cues play in the foraging strategy of such animals? As with most science, finding the right questions presents the most crucial problem.

One hypothesis is that birds smell krill directly. But little empirical information is available about the odors likely to be associated with a krill swarm. Unfortunately, I soon learned that getting this type of information is enormously expensive and not favored by funding agencies. I was inspired, however, to find that other investigators had grappled with the same problems using simple behavioral techniques. Bernice Wenzel of the University of California, Los Angeles, and her graduate student, Larry Hutchison, had found that presenting homogenates of krill off the coast of California attracted sooty shearwaters. Larry Clark, then at the Monell Chemical Senses Institute, and his colleagues demonstrated that component odors of krill-specifically pyrazene, trimethylamines and carboxylic acidsattracted Leach’s storm-petrels when presented to birds at nesting sites on Kent Island. Using quantitative simulations, they also proposed that a small patch, about 0.5 square meter in diameter, of krill might be detectable to foraging petrels from distances on the order of kilometers.

In the ocean waters in the South Atlantic, a variety of species-from fur seals to seabirds-gather in large, mixed-species feeding aggregations at krill swarms. Presumably, krill are driven to the surface by diving predators such as penguins and fur seals, and the crunching that results might release volatile compounds from krill, which seabirds might smell. I wondered if Antarctic procellariiforms would be attracted to odors from macerated krill.

Crashing Kites and Scented Slicks

Studying these birds presented a significant challenge. How would I provide them with odor cues in an area of the world where 12-meter seas are more the rule than the exception? J. R. Forster described a trip to South Georgia in 1775 by writing: The Storm increases, the Sea runs high … If a Capt, some Officers & a Crew were convicted of some heinous crimes, they ought to be sent by way of punishment to these inhospitable and cursed Regions … The very thought to live here a year fills the whole Soul with horror & despair. God! what miserable wretches must they be, that live here in these terrible Climates. Charity lets me hope, that human nature was never thought so low by his Maker, as to be doomed to lead or rather languish out so miserable a life.

If my research voyage promised such a “miserable life,” I needed a handful of contingency plans for testing how birds responded to odor cues. The winter seas proved too unpredictable to deploy buoys with pricey radio-controlled aerosols or even simple wicks emitting odor plumes that birds might follow. My colleagues and I tried a variety of creative odor-deployment techniques, including flying kites over the oceans dangling thousands of odor-soaked tampons. Unfortunately, the kites kept crashing into the ocean, and we quickly abandoned this approach.

Eventually, we settled on a variation of a common practice used by fisherman and birders alike: We tested the attractiveness of odors to seabirds by chumming for them with small vegetable-oil slicks perfumed with a crude krill extract. We also presented birds with plain vegetable-oil slicks to control for any visual or olfactory effect that the vegetable oil might have in attracting birds to the area. If birds are attracted to krill scent, we reasoned, then more birds should come to the krill-scented slicks as compared with the plain vegetable-oil ones. A team of observers, all unaware of the identities of the slicks, counted birds showing interest. A bird was counted as showing interest if it flew upwind into the slick, milled around or alighted on the slick.

We obtained our first results from such experiments near South Georgia and then Elephant Island off the Antarctic Peninsula. The krill-scented slicks attracted procellariiform seabirds five times more frequently than did plain vegetable-oil slicks. Moreover, these experiments revealed an unexpected species-specific attraction. Cape petrels flocked to krill-scented slicks. Giant petrels and black-browed albatrosses also were sighted only at krill-scented slicks, although in smaller numbers. Wilson’s and black-bellied storm-petrels, on the other hand, were sighted just as frequently at plain vegetable-oil slicks as they were at krill-scented slicks. This response pattern showed no clear-cut relation with diet because all of these species rely on Antarctic krill as an important primary food source.

Although these results were encouraging, questions loomed in the back of my mind once we had time to analyze our data. For one thing, I was going along with a long-held assumption that birds are likely to use these food-related odors as foraging cues because the human nose associates them with fish and krill, which are among the type of foods that these birds eat. But I didn’t even know whether aromatics from these prey items were associated with krill swarms or with feeding aggregations in nature. These are long-lived birds that might simply be conditioned to come to these odors from human fishing practices, which are much reduced today but present historically in the area. As it turned out, the answer to some of these questions were, to use a cliche, right under our proverbial noses.

Species Split on Smells

Once while our ship was being reoutfitted in port, I met Tim Bates, an atmospheric scientist at the National Oceanographic and Atmospheric Administration and chief scientist for the next cruise of NOAA’s RV Surveyor. Bates studies a naturally occurring scented compound, dimethyl sulfide (DMS), not for its potential role as a foraging cue but because it is involved in global cooling. From the unforgettable aroma emitted by DMS during the calibration of his measuring equipment, a new idea began to germinate in my mind-one that changed my entire thinking about olfactory foraging.

DMS is a biogenic aromatic released as a metabolic byproduct when phytoplankton is eaten by zooplankton, including Antarctic krill. DMS dissolved in seawater is in turn emitted into the atmosphere. Work by Bates and others has shown convincingly that these emissions can persist for hours or even days. In addition, DMS levels tend to be highest over areas of high primary productivity, including shelf breaks, seamounts and areas of upwelling. I was overwhelmed by the idea that a DMS front on a vast ocean journey could easily alert birds to the presence of krill or other potential prey items that eat krill. I needed to get back to South Georgia to test this hypothesis in the field.

In 1994 Dick Veit and I conducted a series of controlled experiments near South Georgia Island in collaboration with the British Antarctic Survey aboard the RRS James Clark Ross. I wanted to determine whether procellariiform seabirds could smell DMS, and, if they could, whether they responded to it as they might to an olfactory foraging cue. To test the birds’ responses to DMS in the field, I presented birds with DMS-perfumed vegetable-oil slicks paired with plain vegetable-oil slicks as controls. At some locations, my collaborators and I also tested birds’ reactions to slicks scented with cod liver oil. This fishy-smelling oil has long been used by scientists and pelagic birders alike to attract procellariiform seabirds. If DMS serves as a feeding cue, I thought, then the birds should respond to it as they do to cod liver oil.

In our experiments, the DMS-scented slicks attracted some species of procellarform seabirds-including prions, white-chinned petrels and two species of storm-petrels-as much as twice as frequently as plain vegetableoil slicks did. By contrast, three species of albatrosses-wandering, grey-headed and black-browed-and Cape petrels were attracted in nearly equally numbers to DMS-scented and plain vegetable-oil slicks.

The response profiles of these species to slicks scented with DMS or cod liver oil offered some insight. Wilson’s stormpetrels, for example, came to slicks of DMS or cod liver oil nearly twice as frequently as they came to control slicks. The patterns of recruitment were remarkably similar, however, which suggests that DMS is just as potent as cod liver oil in attracting this species. Blackbrowed albatrosses showed a dramatically different response. They flew in within 2 minutes to DMS-scented slicks and control slicks, but left just as rapidly. It seems that this species flies in to check out a slick, but the similarity in their responses to DMS and plain vegetable oil indicates that odor was probably not mediating this behavior. Moreover, these birds were not recruited from beyond the immediate vicinity of where the experiments were carried out. White-chinned petrels presented an intermediate scenario. They flew in rapidly to DMS-scented slicks and then milled about-zigzagging upwind into the slick, circling around and repeating this behavior. They approached the slick scented with cod liver oil, but then left rather than circling back, and showed little interest in the control slicks.

During these experiments, we noticed-as others had reported-that many procellariiform seabirds zigzag upwind into odor cues. Presumably this behavior concentrates a bird’s activity so that it travels to the source of the odor plume. I reasoned that a bird that was interested in the scent of DMS might zigzag up the odor plume, and that this could be reflected as an increased turning rate in a bird’s flight path. To test this idea, my colleagues and I dispersed an aerosol of either DMS or plain water off the stern of the RRS James Clark Ross while observers blind to the treatments being tested monitored turning behavior of birds in the area. The observers tracked single birds for up to one minute, while an assistant recorded the time at which a bird turned.

The results of this experiment supported our earlier findings. Whitechinned petrels, for example, zigzagged about 25 percent more when they encountered DMS-scented plumes as compared with plain water. As predicted, black-browed albatrosses, which in the earlier experiment had simply flown to both DMS and control slicks and back out again, did not change their turning rates in the presence of DMS. If these birds track DMS, they must do so in a way not measured by either experiment.

A Scented Scape

I believe that procellariiform seabirds use olfactory cues in at least two distinct types of foraging activity. First, as we and others have observed, some of these birds undoubtedly track ephemeral odor cues upwind to focus activity toward the source of an odor plume. But of course such plumes alone could not lead birds on some of the feeding journeys that have been documented. Instead, we hypothesize that some of these birds use “odor landscapes” to identify general regions where prey is likely to be found. These birds probably locate these feeding areas by using a variety of navigational mechanisms: celestial navigation, magnetic-field strengths, odor landscapes and more. Potentially rich feeding grounds probably share an olfactory signature, possibly including an elevated DMS level, that a long-distance forager recognizes on arrival.

Although our experiments have focused on DMS, a constellation of aromatics might provide a wealth of information about a foraging area’s quality. Based on satellite telemetry, we know that these localities represent areas of high primary productivity where many species of procellariiform seabirds forage. Odor cues associated with these regions would logically provide birds with a direct and instantaneous means of assessing an area’s potential productivity. Such location-specific cues might also trigger a long-distance forager’s visual search strategies aimed at pinpointing feeding activity by other seabirds and marine mammals. Thus in analogy to the visual landscape, a region rich in DMS and some other aromatics would be a sort of “peak” on the olfactory landscape that overlays the ocean.

As fascinating as these birds are, many species might go extinct before we have the opportunity to understand their secrets for foraging over vast areas of open ocean. Every year, longline-fishing vessels destroy many seabirds around the world. These vessels, fishing mainly for bluefin tuna, trail 50 miles of lines that dangle as thousands of hooks baited with squid or fish. Albatrosses and petrels follow these boats and try to snatch the bait from the hooks, but a bird can be snagged, pulled underwater by the weighted line and drowned. Tens of thousands of albatrosses and petrels get killed this way each year. Such losses are severely depleting world populations, since these birds take nearly a decade to mature and can spend up to four years in courtship before they choose a mate for life. The loss of a mated bird to a long line therefore has a double impact on breeding.

One of the challenges longliners and biologists face is finding ways of keeping these magnificent birds off the hook, but these efforts are also pointing to a need for understanding proximate foraging behavior in greater detail. Since fisherman lose valuable catches by hooking birds, a common practice is to try to lure birds away from lines by dumping offal in the water around the ship. The idea is that birds will go after the discards instead of nabbing the baited hooks and tangling the lines. However, based on our present understanding of how these birds forage, it is likely that odors emitted from fish discards do more to attract procellariiforms to the ship, and this effect is likely to extend miles downwind along the length of line being fished. Birds whose behavior is switched to a proximate-search mode in response to such olfactory cues may follow visual cues to what turns out to be a field of baited hooks rather than a profitable prey patch.

Nevertheless, the longlining bycatch problem might be solvable. Efforts are being made to develop mechanisms of sinking lines beneath the surface of the ocean, rendering them less visible to foraging seabirds. In addition, practices are being developed to reduce odor cues by using frozen bait and eliminating offal discharge. In any case, the more explicitly we understand their foraging behavior, the better equipped we will be to save these birds from the fate of so many other speaes-remembered only in old sea tales as marvelous creatures that used to be.