Behavioral attraction of Leach's storm-petrels (Oceanodroma leucorhoa) to dimethyl sulfide
1 Section of Neurobiology, Physiology and Behavior, Division of Biological
Sciences, University of California, Davis, CA 95616, USA
2 Division of Natural Sciences and Mathematics, Western Oregon University,
345 Monmouth Ave. N., Monmouth, OR 97361, USA
* Author for correspondence (e-mail: ganevitt{at}ucdavis.edu)
Accepted 10 February 2003
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Summary |
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Key words: dimethyl sulfide, DMS, procellariiform seabird, olfaction, Leach's storm-petrel, Oceanodroma leucorhoa, smell
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Introduction |
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The sensory mechanisms that Leach's storm-petrels use to locate food have
not been well characterized, but several lines of evidence suggest that
olfaction is critical to this behavior. Anatomically, these birds have among
the largest olfactory bulbs of any bird
(Bang, 1966). Behavioral
observations suggest that, while visual cues may be used to locate feeding
aggregations, odor cues aid birds in locating prey
(Grubb, 1972
) or productive
areas where prey aggregate (Nevitt,
2000
). Foraging in low light levels is implied, since many types
of prey catalogued in diet samples migrate vertically to the surface at night
but typically occur at depths beyond the range of petrels foraging during the
day (Vermeer and Devito,
1988
). Behavioral experiments performed at the mouth of the Bay of
Fundy, off New Brunswick, Canada have demonstrated an attraction of Leach's
storm-petrels to cod liver oil (Grubb,
1972
) and krill fractions
(Clark and Shah, 1992
). Results
from preliminary cardiac conditioning experiments also indicate a
physiological sensitivity to component odorants of krill, including carboxylic
acids, amines and phenols (Clark and Shah,
1992
), suggesting a highly sensitive olfactory system in this
species.
Recently, Nevitt (2000)
proposed a new model for olfactory foraging by procellariiform seabirds. This
model suggests that olfactory foraging occurs at both large and small scales
(Nevitt, 1999b
,
2000
,
2001
). Over large scales
(hundreds or thousands of kilometers), procellariiform seabirds use changes in
the odor landscape as signals that they have arrived at a productive area to
forage. Scents associated with primary production that contribute to this odor
landscape include biogenic sulfur compounds such as dimethyl sulfide (DMS;
Nevitt, 1999a
,
2000
;
Nevitt et al., 1995
).
Encountering such odors triggers birds to begin a small-scale, area-restricted
search (tens of kilometers) to locate prey either directly, by olfactory
tracking or glimpsing prey in the water, or indirectly, by locating
aggregations of feeding seabirds (Nevitt
and Veit, 1999
). While the model has implications for
procellariiforms worldwide, the data supporting it are based solely on
detailed studies of Antarctic procellariiform species assemblages (see also
Nevitt, 1999a
,
in press
;
Nevitt et al., 1995
).
The purpose of our current study was to begin to extend this research to an
easily accessible northern species, the Leach's storm-petrel. Leach's
storm-petrels are abundant and could serve as a model species for studying a
variety of problems pertinent to olfactory foraging at sea. In addition, we
wanted to assess the utility of a simple behavioral assay that can be
performed in breeding colonies on land rather than at sea. This assay was
introduced by Clark and Shah
(1992) in a preliminary study.
They showed that Leach's storm-petrels will investigate krill-derived odors
presented on high platforms along flyways in breeding colonies. In our study,
we used similar methods to test two odors DMS and cod liver oil
against unscented controls. We predicted that if Leach's storm-petrels
investigated DMS more frequently than unscented control presentations, this
would indicate an ability to smell DMS and potentially use it as a foraging
cue over the ocean. We chose cod liver oil as a second test odor for this
behavioral assay because it is already known to attract Leach's storm-petrels
and other procellariiforms at sea (e.g.
Grubb, 1972
). As in earlier
studies, cod liver oil might thus serve as a convenient positive control for
the utility of the assay itself (e.g.
Nevitt et al., 1995
).
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Materials and methods |
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Experimental trials
We adapted methods described elsewhere
(Clark and Shah, 1992) to test
Leach's storm-petrels' attraction to odors in the field. This technique is
loosely based on studies designed to assay attractiveness of procellariiforms
to odors at sea (e.g. see Hutchison and
Wenzel, 1980
; Lequette et al.,
1989
; reviewed by Nevitt,
2001
).
Experimental set-up
We mounted a small (10 cmx15 cm) plywood platform on a pole
approximately 1.5 m high over an open field within 10 m of an active breeding
colony (near `petrel path'). A small amount (5 ml) of test odor [DMS (100
µmol l1), undiluted cod liver oil (Bristol-Myers Squibb,
New York, NY, USA) or control solution (plain water)] was placed in a small
(25 mm) Petri dish and positioned on the platform. An observer, positioned 25
m crosswind from the platform, recorded activity of each bird as it approached
the platform. Observations were assisted by a night vision scope (Model MKF28;
Startron Mfg., Freeport, PA, USA) and recorded into a dictaphone.
Experimental protocol
A team of two people carried out experiments. One person was responsible
for setting up the experiment while the second person recorded observations.
The basic protocol was as follows: a test substance (odor or control) was
deployed on the platform. This marked the beginning of an observation period.
Observation periods lasted 5 min. During this period, the observer recorded
the number of approaches to the platform. Birds were counted if they
approached within 1 m of the platform or circled around it; flight
trajectories could generally be seen, so that care could be taken to count
each individual only once. At the end of 5 min, the trial ended. The odor was
removed from the platform and placed in a double Zip-lockTM bag.
Following a rest period of at least 10 min, the procedure was repeated. Each
test odor (DMS or cod liver oil) was paired sequentially with a control, but
the order of stimulus presentation (odor or control) was randomized; thus, all
observations were made blind to the treatment being tested.
Rationale
Response criteria (observation period, intervals between trials and scoring
method to avoid repeated measures) were determined in a series of preliminary
trials. We concluded that recording detailed tracking (turning rate,
instantaneous orientation with respect to wind direction) was not possible
given the speed with which the birds approached the target. We limited
observation periods and separated them by intervals of at least 10 min to
avoid eye fatigue. Since birds tended to travel through the testing area on
the way to the colony, this technique also helped to reduce testing
individuals more than once. Finally, we determined that tests should be made
over several nights to avoid pseudoreplication between trials.
Statistical analysis
We used a Wilcoxon paired-sample test to determine whether odor treatment
(DMS or cod liver oil) attracted Leach's storm-petrels more than the paired
control treatment (Zar, 1996).
The analysis was performed on 12 paired trials (odor-control) for DMS and 11
paired trials for cod liver oil.
We then examined whether birds recruited independently to odor or control
presentations. Here we used a two-tailed G-test to compare the
distribution of the rate of attraction during each of the 12 (or 11) trials
with the distribution predicted by a Poisson process
(Zar, 1996). The distributions
for each treatment (DMS, cod liver oil, DMS-control, cod liver oil-control)
were considered separately.
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Results |
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Quantitative observations
Leach's storm-petrels approached DMS presentations nearly twice as
frequently as they approached controls
(Fig. 1; P<0.05,
N=12; Wilcoxon paired-sample test). By contrast, storm-petrels
approached cod liver oil and controls at the same frequency
(Fig. 2; P>0.1,
N=11; Wilcoxon paired-sample test).
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We next examined the distribution of approach rates of Leach's storm-petrels between experimental trials within each of the four treatments (DMS, DMS-control, cod liver oil, cod liver oil-control). If birds arrived in groups, or if the presence of an initial individual enhanced the probability of more arrivals during a 5-min test period, then we would expect the pattern of arrivals to differ significantly from a chance (Poisson) distribution.
Fig. 3A illustrates that the distributions of approach rates differed significantly from that predicted by a Poisson distribution for DMS presentations (G=17.18, P<0.001, d.f.=6). Thus, the behavior of some individuals may have enhanced the attraction of others. By contrast, Fig. 3B shows that Leach's storm-petrels approached cod liver oil at random (G=2.3, P>0.1, d.f.=3). Similarly, birds approached both control treatments at random (DMS-control, G=3.79, P>0.1, d.f.=3; cod-control, G=7.43, P>0.05, d.f.=3; data not shown but appear similar to Fig. 3B).
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Discussion |
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The interpretation that birds are recruiting to a scent as well as to
social cues provided by conspecifics is consistent with a multimodal foraging
strategy involving both olfactory and visual cues
(Nevitt and Veit, 1999).
Leach's storm-petrels forage opportunistically at upwelling zones and are
often observed congregating in zooplankton-rich areas
(Huntington et al., 1996
).
Prey species include fishes (myctophids), cephalopods, crustaceans
(euphausids, decapods, amphipods, isopods, mysids and copepods) and jellyfish
(Scyphozoa) (Harrison, 1984
;
Montevecchi et al., 1992
;
reviewed by Huntington et al.,
1996
); however, myctophids constitute as much as 70% of prey taken
by volume in Northeast Atlantic populations (Montevechhi et al., 1992). These
and other species migrate to the surface at night to feed
(Watanabe et al., 1999
). It is
commonly assumed that Leach's storm-petrels use visual cues such as streaks of
foam (Brown, 1988
;
Haney, 1987
) or feeding
activity of other birds (Haney et al.,
1992
; Silverman and Nevitt,
1995
) to pinpoint productive areas. However, once a productive
area is localized, it is likely that Leach's storm-petrels and other species
perform an area-restricted search using whatever cues are available.
Because zooplankton feeding is associated with the production of DMS, we
have proposed that DMS signals productive areas of ocean where foraging
success is likely to be high (e.g.
Beresshiem, 1987; for a review,
see Bates et al., 1992
;
Nevitt, 1995
;
Nevitt and Veit, 1999
). DMS is
a by-product of the metabolic decomposition of dimethylsulfoniopropionate
(DMSP) in phytoplankton (Nguyen et al.,
1988
; Turner et al.,
1995
; Yang et al.,
1992
). DMSP is released by phytoplankton as they are broken up
during grazing and is enzymatically cleaved to form DMS (e.g.
Wolfe and Steinke, 1996
). DMS
released into the atmosphere is thus linked to the presence of zooplankton
(Daly and DiTullio, 1996
;
Tokunaga et al., 1997) and may alert birds to areas where prey is likely to be
feeding (reviewed in Nevitt,
2000
; Nevitt and Veit,
1999
).
Multimodal cues may alert birds to subtle differences in foraging
opportunities. Myctophids, for example, are bioluminescent, but this
characteristic is likely to change when animals are stressed or macerated, as
happens during feeding. Distinctive scents may also be released as prey items
are macerated, and these scents may invoke different behaviors. Working in
colonies, Clark and Shah (1992)
have demonstrated that Leach's storm-petrels can detect a variety of scented
compounds from macerated krill, including trymethylamine, pyrazine and
carboxylic acids. However, working in the southern oceans, we have found that
odor cues associated with maceration are not necessarily attractive to smaller
seabirds but might instead serve as a deterrent in highly competitive
situations. For example, although Antarctic krill (Euphausia superba)
comprise as much as 95% of the diet of Wilson's storm-petrels (Oceanites
oceanicus), experimental testing at sea suggests that these birds avoid
scents associated with macerated krill. This result is consistent with the
hypothesis that macerated krill signals an increased risk of predation for
smaller petrels by larger species in mixed-species feeding aggregations
(Nevitt, 1999a
).
Identifying how complex sensory processes drive the foraging ecology of interspecific interactions is a topic of great interest. The technique we adopted for this project is relatively straightforward, but we caution that demonstrating that a bird is attracted to an odor in a breeding colony does not necessarily suggest that the odor operates as a foraging cue on the ocean. Cod liver oil is one of the most potent attractants to Leach's storm-petrels at sea, but birds ignored it here, suggesting that the salience of the stimulus presentation needs to be considered in testing situations. Still, the present study provides a clear demonstration that perhaps the most compelling questions in this field are not simply related to identifying what compounds birds can smell or how these compounds disperse over the ocean but rather in elucidating how procellariiforms make use of a complex variety of foraging cues under circumstances that are ecologically meaningful.
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Acknowledgments |
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