Testing olfactory foraging strategies in an Antarctic seabird assemblage
1 Section of Neurobiology, Physiology and Behaviour, University of
California, Davis, California 95616, USA
2 High Cross, British Antarctic Survey, Madingley Road, Cambridge CB3 OET,
UK
* Author for correspondence (e-mail: ganevitt{at}ucdavis.edu)
Accepted 19 July 2004
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Summary |
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Key words: procellariiform seabird, olfaction, smell, odour cue, pyrazine, petrel, albatross, shearwater
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Introduction |
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Current theory suggests that procellariiform seabirds use olfactory cues to
forage at both large and small spatial scales
(Nevitt and Veit, 1999;
Nevitt, 2000
,
2001
). Over large scales
(hundreds or thousands of square kilometres), procellariiform seabirds detect
productive areas for foraging by changes in the odour landscape. Dimethyl
sulphide (DMS) has been implicated as one of the odorants that birds use to
identify areas of high primary productivity
(Nevitt et al., 1995
; Nevitt,
1999
,
2000
; reviewed by
Hay and Kubanek, 2002
). Once a
productive area is found, birds switch to an area-restricted search strategy
to pinpoint ephemeral prey patches (see
Nevitt and Veit, 1999
). During
area-restricted search, hunting strategies vary according to species and
feeding conditions. For example, some species may track prey using their sense
of smell whereas others may be better adapted to use visual cues to locate
prey patches, either by spotting prey directly or by seeing aggregations of
other foraging seabirds alighting on the water
(Silverman et al., in
press
).
We have been investigating foraging strategies used in area-restricted
search in the procellariiform seabird assemblage in the Atlantic sector of the
Antarctic, near South Georgia Island (54°00 ' S, 36°00 '
W). This assemblage is made up of a number of species that feed to a greater
or lesser extent on a patchily distributed prey resource, Antarctic krill
(Euphausia superba; e.g. Prince
and Morgan, 1987). Thus, this species assemblage offers a
relatively simple system for investigating how different species use olfactory
cues associated with krill to exploit prey patches. Given the extensive
information on foraging ecology and diet of seabirds in this area (e.g.
Croxall et al., 1984
,
1997
;
Croxall and Prince, 1987
), we
can also begin to formulate and test hypotheses about the sensory ecology of
how different species forage. For example, it has been suggested that larger,
more aggressive species are likely to be attracted to scents associated with
macerated krill in combination with social cueing by other birds. By contrast,
smaller, less aggressive species may be better adapted to hunting prey
opportunistically, primarily by tracking scents linked to krill or zooplankton
grazing, such as DMS (Nevitt et al.,
1995
; Nevitt,
1999
).
The present study was designed to test this idea by surveying responses of
a much broader range of foraging procellariiforms to 3-methyl pyrazine, a
scented compound found in extracts of macerated Antarctic krill
(Kubota et al., 1989). Unlike
crude extracts, 3-methyl pyrazine is colourless, and its concentration can be
tightly controlled. Thus, in this study, we were able to examine the
behavioural responses to the odour cue independent of any visual cues
associated with prey. Since many species in the area are conditioned to
fishy-smelling compounds (Nevitt et al.,
1995
), we also tested birds' responses to herring oil as a
positive control for the experiment.
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Materials and methods |
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Experimental design
Controlled experiments were designed to identify whether any
procellariiform species might be attracted to 3-methyl pyrazine (`pyrazine'),
a scented component of macerated Antarctic krill (Euphausia superba;
Kubota et al., 1989;
Clark and Shah, 1992
). As in
other studies (Nevitt et al.,
1995
), our aim was to produce a downwind odour concentration in
the nanomolar range. We did this by deploying pyrazine-scented vegetable oil
slicks on the ocean surface at seven different locations along the MEB
transect (Fig. 1B). Because
environmental conditions varied and surface slicks also presented visual cues
to seabirds, pyrazine-scented slicks were always paired with unscented
`control' slicks. We reasoned that if birds used pyrazine as a foraging cue,
then more birds would be attracted to slicks scented with pyrazine than to
control slicks. Since we have previously established that many species in the
area are conditioned to fishy-smelling compounds
(Nevitt et al., 1995
), we
reasoned that if birds were attracted to pyrazine, then their response should
be qualitatively similar to their response to herring oil. Thus, we also
tested birds' responses to herring oil at six locations to provide a positive
control for interpreting our results.
While the ship was positioned into the wind, either a control, pyrazine- or herring-scented oil slick was deployed off the stern. Slicks usually drifted about 100 m from the ship, allowing easy observation of approaching birds. Prior to deployment, a count was made of all birds within a 180° arc with a radius of 300 m from the stern of the ship. Once a slick was deployed, one person using binoculars made observations at 1-min intervals for 12 min; data were recorded by a second person standing close by. Birds were counted if they (1) flew upwind over the slick within approximately 1 m of the surface, (2) landed, (3) milled or (4) pattered on the slick. To avoid bias, the order of slick presentation (control, pyrazine or herring) was randomised at each location, and deployments were separated by at least one hour. We generally tested only two slicks at a location due to time constraints imposed by the ship's schedule. To eliminate inter-observer bias, the same observer recorded data for all trials and was kept blind with respect to the treatments being tested. Slicks were tested one at a time and dissipated within 20 min. Standard meteorological data were recorded during all trials using shipboard instrumentation (Table 1).
Odours
Pyrazine (200 mmol l1 3-methyl pyrazine in 2.5 litres of
vegetable oil; 0.5 moles total; Sigma-Aldrich, St Louis, MO, USA), herring (50
ml commercial herring oil; diluted to 2.5 litres in vegetable oil) and control
(2.5 litres of vegetable oil) slicks were prepared approximately 1 h before
experiments. Because turbulent plume dynamics are not easily predicted under
natural conditions (Dusenbury,
1992), we adapted a simple but well-established sector model
derived from empirically sampling turbulent odour plumes in nature to estimate
average odour profiles downwind of slicks
(Elkinton and Cardé,
1984
). This approach is conservative: it assumes that the odour
disperses as a cone-shaped plume downwind of the slick with edges 20° from
the axis and that dispersal is continuous and rapid (510 m
s1) due to wind. The wind speed recorded during our
experiments ranged from approximately 8 to 20 knots (3.8510.28 m
s1; Table 1).
Thus, even over the short (12 min) time course of the experiment, the odour
gradient established is predicted to extend kilometres downwind of the
slick.
As in other studies (Nevitt et al.,
1995), we used this model to calculate a theoretical maximum for
the average concentration that a bird might encounter traversing a plume
extending 1 km downwind of the slick. To do this, we calculated what would
happen if the entire amount of odour deployed was instantaneously concentrated
in a plume extending 1 km downwind of the slick. While turbulent odour plumes
are not homogeneous, even this exaggerated scenario predicts an average
concentration of <10 nmol m3. Naturally occurring levels
of 3-methyl pyrazine are not known; however, based on studies of other scented
compounds that have been measured over the southern oceans
(Berresheim, 1987
) and recent
studies of sensitivity thresholds (G.N., unpublished data), we considered this
concentration to be within biologically relevant levels.
Underway observations
To determine background species compositions along the MEB
(Fig. 2), we counted all birds
within a 100 m-wide `box' 100 m off the bow of the ship using standard strip
transect methodology while the ship was underway
(Tasker et al., 1984). Using
binoculars, one observer continuously scanned the area while a second person
entered data directly into a portable computer. Birds were counted for 3 km
prior to arriving at stations where slicks were deployed.
Statistical analysis
Our goal was to compare the attractiveness of scented slicks and control
slicks. An inherent difficulty to performing behavioural studies at sea is
that, since individuals cannot be marked, observations of individuals are not
strictly independent. In addition, responses tend to be highly variable
between species over time. Moreover, because experiments are usually performed
in different geographical locations contingent upon ship availability, true
replicates can seldom be performed. While such issues have generally been
ignored in the literature (e.g. Hutchison
and Wenzel, 1980), our analysis was designed to deal with these
concerns more directly. First, we defined the response that each species gave
to a particular slick in terms of `slick attentiveness' over the 12-min
observation period. Attentiveness was determined by summing counts per minute
(or `bird-minutes') over time. We reasoned that if experimental and control
slicks were equally attractive to birds, then the two slicks should also have
equal probabilities of attracting birds for an additional bird-minute
throughout the 12-min observation period. For each species, we then tested
whether the proportion of bird-minutes spent on scented slicks (either
pyrazine or herring) was equal to the proportion of bird-minutes spent on
control slicks (G-test for pooled data;
Zar, 1996
). Analyses were
performed on pooled data to accommodate variability in weather parameters and
bird distributions down the length of the MEB transect.
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Results |
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Preference for scented over control slicks varied with respect to odour (Fig. 3). Of the nine species that were attracted to slicks, four species clearly exhibited a special interest in pyrazine-scented slicks as compared with control slicks (Fig. 3, black bars). Cape petrels, giant petrels and white-chinned petrels, for example, were sighted 1.84 times as often at slicks scented with pyrazine than at control slicks; black-browed albatrosses were sighted only at pyrazine-scented slicks and never at control slicks. The remaining five species were sighted just as frequently at pyrazine-scented as at control slicks. These species included great shearwaters, prions, wandering albatrosses, black-bellied storm-petrels and Wilson's storm-petrels.
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By contrast, eight of the nine species participants recruited to herring-scented slicks in significantly higher numbers than to control slicks (Fig. 3, grey bars). Cape petrels, giant petrels, black-browed albatrosses, white-chinned petrels, prions, wandering albatrosses, black-bellied storm-petrels and Wilson's storm-petrels were sighted 25 times as frequently at herring-scented slicks than at control slicks. Only great shearwaters failed to discriminate between herring-scented and control slicks.
Nine procellariiform species were recorded in transect surveys but were not attracted to slicks. These species were soft-plumaged petrels, blue petrels, sooty shearwaters, Southern royal albatrosses, sooty albatrosses, light-mantled sooty albatrosses, grey-headed albatrosses, white-headed petrels and common diving petrels. Non-procellariiform species noted in the area included king penguins and South polar skuas, neither of which recruited to slicks.
Differences in response profiles
The temporal response profiles over the 12-min observation period were
distinctive for different species and odours. By subtracting controls from
experimental values, we could get a clearer picture of the patterns of
responses over time that could be attributed to the odour cue alone.
Fig. 4 illustrates three
characteristic patterns that we observed using this technique. In the first
pattern, recruitment to an odour cue increased over time and then stabilised.
Fig. 4A illustrates this
pattern for Wilson's storm-petrels in response to herring oil (open circles);
black-bellied storm-petrels showed a similar pattern of recruitment in
response to herring oil slicks. Note that because the response to pyrazine was
indistinguishable from the control response for this species, the plot of the
pyrazine response yields a flat line or `null' response
(Fig. 4A, filled circles).
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In a second pattern, the relative proportion of birds responding to an odour cue peaked rapidly within 34 min and then diminished to near zero levels over the remainder of the 12-min observation period. This pattern most likely reflects conspecific visual cueing initiated by the odour presentation. Fig. 4B illustrates this pattern. Here, giant petrels in the visual area accumulated rapidly at both herring(open circles) and pyrazine-scented slicks (filled circles) and then just as quickly disbanded. We observed similar, though less dramatic, profiles for wandering albatrosses in response to herring oil.
Fig. 4C illustrates the third type of response profile that we observed. Here, the proportion of birds responding to an odour cue peaked rapidly and cyclically throughout the observation period, most likely reflecting birds milling over the slick. This pattern is illustrated for white-chinned petrels in response to both herring oil (Fig. 4C, open circles) and pyrazine (Fig. 4C, filled circles). For this species, response profiles to pyrazine and herring oil showed very similar periodicity. Cape petrels, black-browed albatrosses and prions exhibited similar patterns.
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Discussion |
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Other studies
Although euphausids are common prey to procellariiforms worldwide (reviewed
by Warham, 1996), only a few
other studies have tested responses of seabirds to krill-related odours in the
context of foraging at sea (Hutchison and
Wenzel, 1980
; Hutchison et
al., 1984
; Nevitt,
1994
,
1999
;
Nevitt et al., 1995
). Working
in the coastal waters off southern California, Hutchison et al.
(1984
) compared the
attractiveness of a volatile fraction of cod liver oil to homogenates of squid
(Loligo opalescens) and Antarctic krill. Their results showed that
sooty shearwaters were strongly attracted to floating wicks scented with these
food-related compounds, suggesting that odours from squid and krill
homogenates could serve as foraging cues under more natural situations. In our
study, sooty shearwaters did not recruit to either scented or unscented
slicks. However, these birds were sighted only incidentally during transect
surveys (Fig. 2), suggesting
that there were not many of them around to participate in our experiments.
By contrast, Hutchison et al.
(1984) found that Northern
fulmars (Fulmaris glacialis) were not attracted to food-related cues.
Northern fulmars do not occur in the Southern oceans, and a related species,
the Antarctic fulmar (Fulmaris glacialoides), was absent from the
transect during the present study. They have, however, been found to be
unresponsive to macerated krill in previous work conducted in the Elephant
Island study grid near the Antarctic Peninsula
(Nevitt, 1999
).
With respect to storm-petrels, Hutchison et al.
(1984) provide no data
concerning attraction of this species to macerated krill at sea. However,
whole-krill homogenates and component odours derived from krill (including
pyrazine) have been shown to attract Leach's storm-petrels, Oceanodroma
leucorhoa, in other land-based behavioural experiments
(Clark and Shah, 1992
). These
researchers tested birds' responses to krill odours presented on platforms
positioned within breeding colonies in New Brunswick. Because these
behavioural trials were not performed at sea, their relevance to foraging is
unclear (see discussion in Nevitt and
Haberman, 2003
). Even so, Clark and Shah
(1992
) were the first to use
simulation techniques to predict the dispersion profiles of pyrazine and other
volatiles released by macerating krill. Their model inferred that a patch of
krill 0.5 m in diameter might be detectable to foraging Leach's storm-petrels
from distances in the order of kilometres. Such detection ranges are greater
than the visual range of a petrel foraging within a metre of the surface of
the water in seas that are routinely metres high
(Clark and Shah, 1992
;
Haney et al., 1992
; see also
review by Nevitt and Veit,
1999
).
More precise data on sensory thresholds to specific natural scented
compounds is needed to get a clearer understanding of olfactory detection
ranges. But to start to answer these questions, we need to know what specific
compounds seabirds respond to in real-life foraging situations. The present
study illustrates that responses elicited by pyrazine and krill extracts
(Nevitt, 1999) are similar
across species, even in different regions of the sub-Antarctic. Thus, pyrazine
is a good candidate to examine behavioural response thresholds (e.g.
Cunningham et al., 2003
) and
will undoubtedly serve as a useful probe to facilitate future work modelling
odour dispersal and transport associated with krill swarms.
Inter-specific differences in olfactory foraging
While it is commonly assumed that procellariiform seabirds conduct
olfactory-mediated area-restricted search by tracking odour cues emitted from
prey, understanding the dynamics of olfactory foraging is turning out to be
more complex than simply determining detection thresholds for particular
prey-related odorants. For example, an intriguing feature of the results
presented here and elsewhere (Nevitt,
1999) is that inter-specific differences in the response to
krill-derived odours do not reflect the proportions by mass of krill in these
birds' diets (Table 3). Species
whose diets comprise 3090% Antarctic krill by mass are not
preferentially attracted to krill odours. Thus, an olfactory foraging model
that assumes an increased attraction to krill-derived odours by krill-eating
species is probably a naïve representation of the complex interactions
driving area-restricted search.
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We have proposed an alternative explanation based not on diet but on
foraging behaviour (Nevitt
1999), and the data presented here support this model. Our model
suggests that species that routinely forage in large, mixed-species feeding
aggregations use odours associated with macerated krill to locate these
aggregations from beyond the visual foraging range. These birds tend to rely
heavily on visual cues (such as aggregations of birds foraging) to locate
foraging hotspots. Smaller, less aggressive species use a different strategy:
these birds track prey or productive hotspots by smell, tending to exploit
scented compounds associated with primary productivity (e.g. DMS) to find prey
opportunistically (Nevitt et al.,
1995
).
In support of this idea, the relative proportions of different species
engaged in feeding aggregations near South Georgia reflect the
species-specific responses we observed to both macerated krill and pyrazine
(Harrison et al., 1991).
Black-browed albatrosses, giant petrels and white-chinned petrels dominated
mixed-species feeding aggregations and were also attracted to crude krill
extracts or pyrazine in our studies. Wilson's storm-petrels and prions,
however, were present in much smaller proportions
(Harrison et al., 1991
),
possibly reflecting an increased risk of predation by species such as giant
petrels at such aggregations (Hunter,
1983
; G.N., personal observation). These species were not
attracted to krill scents and, again, this suggests an alternative foraging
strategy for these smaller, more vulnerable species.
The key to this alternative foraging strategy may be found by considering
the responses of these species to DMS. DMS is released by phytoplankton (e.g.
Phaeocystus sp.) during grazing by Antarctic krill and other
zooplankton (Dacey and Wakeham,
1986; Daly and DiTullio,
1996
). Both Wilson's storm-petrels and prions have been shown to
be attracted to DMS in experimental trials, whereas Cape petrels and other
large species present at feeding aggregations are not
(Nevitt et al., 1995
). The
implication is that DMS-responders may rely more on indirect indicators of
krill to opportunistically exploit zooplankton-rich foraging areas
independently of feeding aggregations. A familiarity with DMS as a foraging
cue may also give smaller birds such as storm-petrels a competitive edge to
locate and exploit ephemeral feeding patches independently of other
species.
Little information is available about how large, mixed-species feeding
aggregations develop under natural conditions, particularly in terms of which
species arrive first. Verheyden and Jouventin
(1994) have suggested that
species such as storm-petrels may initiate these aggregations by being the
first birds to locate krill swarms. If this is the case, our data suggest that
stages of recruitment may be dictated by different odour cues and may be
partially dependent on a species-specific response to these different cues.
For example, recruitment of Wilson's storm-petrels may be initiated by
tracking DMS hotspots that presumably develop as krill begin to graze, in
consort with visual cueing by conspecifics (see discussion in
Nevitt and Haberman, 2003
). As
other species join, subsequent recruitment may be facilitated by olfactory
cues released from macerated krill, in addition to obvious visual signals
provided by the aggregation itself.
Alternatively, pyrazine and other scented compounds in krill are presumably
released when krill are macerated or damaged, a situation that is likely to
occur when krill swarms are preyed upon by diving predators such as penguins
and seals as well as other seabirds. Under such circumstances, krill are
thought to be driven to the surface and thus present a profitable feeding
opportunity to procellariiforms (e.g. Hunt
et al., 1992). While visual cueing is certainly critical to this
process (Haney et al., 1992
;
Bretagnolle, 1993
;
Veit, 1995
;
Silverman et al., in press
),
it is also possible that pyrazine and other scented compounds released during
these feeding events direct distant pyrazine-responders to the area.
Storm-petrels detecting pyrazine may simply choose to avoid it until the
aggregation has disbanded whereas giant petrels and some albatross species may
be highly attracted (see Fig.
4B). We suspect that multiple tactics come into play, given the
variety of foraging scenarios that these birds routinely encounter. These
behavioural strategies are likely to be more complex for many species than
simply tracking prey by scent.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bang, B. G. (1965). Anatomical adaptations for olfaction in the snow petrel. Nature 205,513 -515.
Bang, B. G. (1966). The olfactory apparatus of tubenosed birds. Acta. Anat. 65,391 -415.[Medline]
Berresheim, H. (1987). Biogenic sulfur emissions from the SubAntarctic and Antarctic oceans. J. Geophys. Res. 92,13245 -13262.
Bretagnolle, V. (1993). Adaptive significance of seabird coloration: the case of Procellariiforms. Am. Nat. 142,141 -173.[CrossRef]
Clark, L. and Shah, P. S. (1992). Information content of door plumes: what do Leach's storm-petrels know? In Chemical Signals in Vertebrates, vol.VI (ed. R. L. Doty and D. Muller-Schwarze), pp.421 -427. New York: Plenum Press.
Croxall, J. P. and Prince, P. A. (1987). Seabirds as predators on marine resources, especially krill, at South Georgia. In Seabirds: Feeding Ecology and Role in Marine Ecosystems (ed. J. P. Croxall), pp.345 -368. Cambridge: Cambridge University Press.
Croxall, J. P., Rickets, C. and Prince, P. A. (1984). Impact of seabirds on marine sources, especially krill of South Georgia waters. In Seabird Energetics (ed. G. C. Whittow and H. Rahn), pp. 285-317. New York: Plenum Press.
Croxall, J. P., Prince, P. A. and Reid, K. (1997). Dietary segregation of krill-eating South Georgia seabirds. J. Zool. 242,531 -556.
Cunningham, G. B., Van Buskirk, R. W., Bonadonna, F.,
Weimerskirch, H. and Nevitt, G. A. (2003). A comparison of
the olfactory abilities of three species of procellariiform chicks.
J. Exp. Biol. 206,1615
-1620.
Dacey, J. W. H. and Wakeham, S. G. (1986). Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233,1314 -1316.
Daly, K. L. and DiTullio, G. R. (1996). Particulate dimethulsulfoniopropionate removal and dimethyl sulphide production by zooplankton in the Southern Ocean. In Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (ed. R. P. Kiene, P. T. Visscher, M. D. Kellor and G. O. Kirst), pp.223 -238. New York: Plenum Press.
Dusenbury, D. B. (1992). Sensory Ecology: How Organisms Acquire and Respond to Information. New York: Freeman Press.
Elkinton, J. S. and Cardé, R. T. (1984). Chemo-orientation in flying insects. In Chemical Ecology of Insects (ed. W. J. Bell and R. T. Cardé), pp.73 -91. Sunderland: Sinauer.
Haney, J. C., Fristrup, K. M. and Lee, D. S. (1992). Geometry of visual recruitment by seabirds to ephemeral foraging flocks. Ornis Scand. 23, 49-62.
Harrison, N. M., Whitehouse, M. J., Heinemann, D., Prince, P. A., Hunt, G. L., Jr and Veit, R. R. (1991). Observations of multispecies feeding flocks around South Georgia. Auk 108,801 -810.
Hay, M. and Kubanek, J. (2002). Community and ecosystem level consequences of chemical cues in the plankton. J. Chem. Ecol. 28,2001 -2016.[CrossRef][Medline]
Hunt, G. L., Heinemann, D. and Everson, I. (1992). Distributions and predatorprey interactions of macaroni penguins, Antarctic fur seals, and Antarctic krill near Bird Island, South Georgia. Mar. Ecol. Prog. Ser. 86, 15-30.
Hunter, S. (1983). The food and feeding ecology of giant petrels Macronectes halli and M. giganteus at South Georgia. J. Zool. 200,521 -538.
Hutchison, L. and Wenzel, B. M. (1980). Olfactory guidance in foraging by procellariiforms. Condor 82,314 -319.
Hutchison, L., Wenzel, B. M., Stager, K. E. and Tedford, B. L. (1984). In Marine Birds: Their Feeding Ecology and Commercial Fisheries Relationships (ed. D. N. Nettleship, G. A. Sanger and P. F. Springer), pp. 72-77. Ottawa: Canadian Wildlife Service.
Kubota, K., Uchida, C., Kurosawa, K., Komuro, A. and Kobayashi, A. (1989). Identification and formation of characteristic volatile compounds from cooked shrimp. In Thermal Generation of Aromas Parliament. ACS Symposium Series 409 (ed. R. J. McGorrin and C. T. Ho), pp. 376-385. Washington, DC: American Chemcial Society.
Nevitt, G. A. (1994). Evidence that Antarctic procellariiform seabirds can smell krill. Ant. J. US 29,168 -169.
Nevitt, G. A. (1999). Olfactory foraging in Antarctic seabirds: a species-specific attraction to krill odors. Mar. Ecol. Prog. Ser. 177,235 -241.
Nevitt, G. A. (2000). Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol. Bull. 196,245 -253.
Nevitt, G. A. (2001). Mechanisms of olfactory foraging by procellariiform seabirds. In Chemical Signals in Vertebrates, vol. IX (ed. A. Marchlewska-Koj, J. J. Lepri and D. Muller-Schwarze), pp.27 -33. New York: Plenum Press.
Nevitt, G. A. and Haberman, K. L. (2003).
Behavioral attraction of Leach's storm-petrels (Oceanodroma
leucorhoa) to dimethyl sulphide. J. Exp. Biol.
206,1497
-1501.
Nevitt, G. A. and Veit, R. R. (1999). Mechanisms of prey patch detection by foraging seabirds. In Proceedings of the 22nd International Ornithological Congress (ed. N. J. Adams and R. H. Slotow), pp.2072 -2082. Johannesburg: BirdLife.
Nevitt, G. A., Veit, R. R. and Kareiva, P. (1995). Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376,680 -682.[CrossRef]
Prince, P. A. and Morgan, R. A. (1987). Diet and feeding ecology of procellariiformes. In Seabirds: Feeding Ecology and Role in Marine Ecosystems (ed. J. P. Croxall), pp.135 -171. Cambridge: Cambridge University Press.
Silverman, E., Veit, R. R. and Nevitt, G. A. (in press). Nearest neighbors as foraging cues: information transfer in a patchy environment. Mar. Ecol. Prog. Ser.
Tasker, M. L., Jones, P. H., Dixon, T. and Blake, B. F. (1984). Counting seabirds at sea from ships: a review of methods employed and a suggestion for a standardized approach. Auk 10,567 -557.
Veit, R. R. (1995). Pelagic communities of seabirds in the South Atlantic Ocean. Ibis 137, 1-10.
Verheyden, C. and Jouventin, P. (1994). Olfactory behaviour of foraging procellariiforms. Auk 111,285 -291.
Warham, J. (1996). The Behaviour, Population Biology and Physiology of the Petrels. London: Academic Press.
Wenzel, B. M. (1987). The olfactory and related systems in birds. In The Terminal Nerve (Nervus Terminalis): Structure, Function and Evolution, vol.519 (ed. L. S. Demski and M. Schwanzel-Fukuda), pp.137 -149. New York: Annals of the New York Academy of Sciences.
Wenzel, B. M. and Meisami, E. (1990). Quantitative characteristics of the olfactory system of the Northern fulmar (Fulmarus glacialis): a pattern for sensitive door detection? In Proceedings of the 10th International Symposium on Olfaction and Taste (ed. K. B. Doving), pp. 379. Oslo, Norway: GCS A/S.
Zar, J. H. (1996). Biostatistical Analysis. Third edition. Upper Saddle River, NJ: Prentice Hall.
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