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First published online May 19, 2008
Journal of Experimental Biology 211, 1706-1713 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015412
Sensory realms in the oceanic environment |
Sensory ecology on the high seas: the odor world of the procellariiform seabirds
Section of Neurobiology, Physiology and Behavior, College of Biological Sciences, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA and Bodega Marine Laboratory, University of California, 2099 Westside Road, Bodega Bay, CA 94923, USA
e-mail: ganevitt{at}ucdavis.edu
Accepted 12 March 2008
Summary
Procellariiform seabirds wander the world's oceans aided by olfactory abilities rivaling those of any animal on earth. Over the past 15 years, I have been privileged to study the sensory ecology of procellariiforms, focusing on how olfaction contributes to behaviors, ranging from foraging and navigation to individual odor recognition, in a broader sensory context. We have developed a number of field techniques for measuring both olfactory- and visually based behaviors in chicks and adults of various species. Our choice of test odors has been informed by long-term dietary studies and geochemical data on the production and distribution of identifiable, scented compounds found in productive waters. This multidisciplinary approach has shown us that odors provide different information over the ocean depending on the spatial scale. At large spatial scales (thousands of square kilometers), an olfactory landscape superimposed upon the ocean surface reflects oceanographic or bathymetric features where phytoplankton accumulate and an area-restricted search for prey is likely to be successful. At small spatial scales (tens to hundreds of square kilometers), birds use odors and visual cues to pinpoint and capture prey directly. We have further identified species-specific, sensory-based foraging strategies, which we have begun to explore in evolutionary and developmental contexts. With respect to chemical communication among individuals, we have shown that some species can distinguish familiar individuals by scent cues alone. We are now set to explore the mechanistic basis for these discriminatory abilities in the context of kin recognition, and whether or not the major histocompatibility complex is involved.
Key words: olfaction, Procellariiformes, seabirds, sub-Antarctic
Introduction
The tube-nosed seabirds (order: Procellariiformes) are noted for their
wide-ranging, pelagic lifestyle. This order covers a diverse range of species
groups including the storm-petrels, albatrosses, gadfly petrels, diving
petrels, fulmars, prions and shearwaters
(Warham, 1990
;
Warham, 1996). These birds
spend most of their lives in flight over the ocean, and are tied to land for
only a few months each year or every other year to breed and rear a single
offspring. Most species have lifespans ranging from four to six decades, and
tend to remain faithful to both their mate and nest site throughout their
adult life. Like mustelids (the family that includes the weasels, badgers and
ferrets), procellariiforms are renowned for their strong, musky personal scent
(Bonadonna et al., 2007),
which perfumes their oily plumage, their nest material and even their eggs.
Not surprisingly, procellariiforms have among the largest olfactory bulbs of
birds (Bang, 1966) and their
neuroanatomy suggests a highly developed sense of smell in the few species
that have been examined at the cellular level. For example, the olfactory
bulbs of Northern fulmars (Fulmarus glacialis) have twice as many
mitral cells as rats (120000 vs 60 000) and six times as many as mice
(120 000 vs 20 000) (Wenzel and
Meisami, 1987). These cells are fundamental to olfactory
processing and play a key role in odor contrast enhancement (reviewed by
Shepherd et al., 2007). While
such comparisons suggest a multitude of questions to explore with respect to
anatomy and function, my current research program has been directed towards
investigating the sensory ecology of these birds, focusing on how olfaction,
combined with other sensory modalities, contributes to behaviors ranging from
foraging and navigation to individual odor recognition. This mini-review
highlights some of our major findings and future directions.
An overview of foraging
Most procellariiforms forage over immense areas of the ocean for patchily
distributed prey, including various species of fish, squid and krill. Their
survival depends on finding the proverbial needle in a haystack on a daily
basis. Depending on the species, procellariiform diets can be highly variable,
and can vary with respect to prey availability
(Reid et al., 1997;
Reid et al., 1996) or time of
year (Ainley et al., 1984).
During the breeding season, procellariiforms are central place foragers
(Stephens and Krebs, 1986),
meaning that they are temporally constrained to return to their nest either to
relieve a mate or to provision a hungry chick. Results from satellite tracking
studies of larger species have revealed that species use different strategies
to efficiently accomplish this task, including opportunistic and commuter
foraging strategies (Weimerskirch,
1998). Opportunistic foragers such as wandering albatross
(Diomedea exulans) tend to hunt for prey along continuous, looped
paths covering many thousands of kilometers of pelagic and neritic water even
on a single foraging trip (Fig.
1A). These birds forage mainly on fish (myctophids) and various
squid species. A large fraction of their diet tends to be squid in the form of
carrion (Croxall and Prince,
1994), which they track using a combination of visual and
olfactory cues (Nevitt et al.,
2008). On the other hand, commuters such as black-browed albatross
(Thalassarche melanophrys) may travel thousands of kilometers to a
shelf break or seamount where prey are likely to be more concentrated
(Fig. 1B). Upon arrival, these
birds engage in area-restricted search (ARS) to locate prey
(Fig. 2A,B) (reviewed by
Nevitt, 2000). This particular
species tends to forage on a combination of squid, krill and fish in roughly
equal proportions during the breeding season
(Rodhouse and Prince, 1993).
Thus, foraging strategies tend to operate over different spatial scales. At
larger scales, the task is to localize productive areas within the vast,
seemingly featureless oceanic environment where prey are likely to be
encountered, whereas at small scales, birds must pinpoint and capture prey
using whatever proximate cues are available to them
(Fig. 2).
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I have proposed that natural scent cues in the marine environment present
guideposts to aid seabirds in foraging and navigation
(Nevitt, 2000). At large
spatial scales, I have suggested that seabirds use changes in the olfactory
landscape to recognize potentially productive foraging opportunities as they
fly over them (Fig. 3)
(Nevitt et al., 1995). These
changes in the olfactory landscape reflect bathymetric features, which tend to
accumulate phytoplankton and therefore prey, and we speculate that birds build
up a map of these features over time
(Nevitt, 2000). Thus, in the
context of foraging, a bird might navigate to a historically rich productive
area (a shelf break, a seamount or an upwelling zone) using mechanisms that we
have yet to work out. The bird knows that it has arrived, however, by a
predictable variation in the way the ocean smells
(Fig. 2A). This change in the
background scent triggers the bird to begin ARS at a much smaller sale (tens
to hundreds of square kilometers). For ARS, birds might use olfactory, visual
or a combination of signals, including the foraging activity of other birds,
to locate and capture prey (Fig.
2B) (Nevitt,
1999a; Nevitt et al.,
2008).
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This conceptual model stems from the discovery that seabirds and other
marine predators can smell trace concentrations of sulfur compounds, which are
naturally associated with oceanic features where prey tend to aggregate. Most
critically, we have established that dimethyl sulfide (DMS), and its precursor
dimethylsulfoniopropionate (DMSP), can be detected by a variety of marine
organisms including procellariiforms
(Nevitt and Haberman, 2003;
Nevitt et al., 1995) and some
species of fish (DeBose et al.,
2008). This work has been extended by others to include harbor
seals (Kowalewsky et al.,
2006) and whale sharks (reviewed by
Martin, 2007). DMS is a
scented compound that is involved in climate regulation through the production
of cloud condensation nuclei (reviewed by
Simó, 2001). Biogenic
marine DMS is a major contributor to geochemical sulfur cycling. Thus,
considerable effort has been directed towards understanding and monitoring its
production and distribution in the marine environment, extending from local
(prey patch size) to global spatial scales (reviewed by
Simó, 2001). It is
arguably unprecedented to have such detailed information on the production and
distribution of a biogenic signal molecule, and these data have provided
important insights into how seabirds and other marine organisms might use
scented compounds in foraging and navigation at both local and global spatial
scales.
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). In the
Southern ocean, DMS is frequently associated with oceanic features where
phytoplankton are plentiful (including upwelling zones, seamounts and shelf
breaks) (Berresheim et al.,
1989; Daly and DiTullio,
1996; McTaggart and Burton,
1992). These are areas where seabirds and other marine predators
tend to aggregate and forage (Nevitt and
Bonadonna, 2005b; Nevitt et
al., 1995). DMSP tends to be released when phytoplankton cells are
crushed and it is then rapidly converted to DMS via processes within
the marine microbial food web (reviewed by
Pohnert et al., 2007). As
Fig. 4 illustrates, it is now
well established that DMS emissions increase when phytoplankton are grazed by
protozoans (Wolfe and Steinke,
1996), metazoans (Dacey and
Wakeham, 1986) and krill (Daly
and DiTullio, 1996), suggesting that, during ARS at small spatial
scales, local elevations in DMS may opportunistically alert higher order
predators (including birds) to rapidly accumulating aggregations of
zooplankton (e.g. krill) and zooplankton predators (fish and squid). Different sensory-based foraging strategies
To test these ideas experimentally, we conducted a multi-year study of
small-scale foraging in the Atlantic sector of the Southern ocean, which
confirmed that birds tend to be attracted not to prey scents per se
but rather to odors such as DMS that are released during feeding interactions
(Nevitt, 1999a;
Nevitt, 1999b;
Nevitt et al., 2004;
Nevitt et al., 1995). To put
it more colloquially, predators tend to be messy eaters, and procellariiform
species are adapted to pay attention to who is eating whom
(Hay and Kubanek, 2002;
Nevitt, 1999b;
Nevitt et al., 2004). For
example, when DMS was presented to seabirds in controlled experimental trials
performed at sea, several species of storm-petrels (Oceanodroma sp.),
prions (Pachyptila sp.) and gadfly petrels (Procellaria sp.)
responded by tracking this odor to its source, using a zigzag, upwind search
behavior characteristic of olfactory tracking in organisms as diverse as fish,
moths and crustaceans (DeBose and Nevitt,
2008; Montgomery et al.,
1999; Moore and Crimaldi,
2004; Nevitt et al.,
1995; Willis,
2005; Zimmer-Faust et al.,
1995). Surprisingly, these species tended to ignore krill odors,
even though krill contributes significantly to their diets. By contrast, other
typically larger and more conspicuous species recruited to visual cues and to
odors associated with crushed krill (pyrazines). Nearly every species
recruited to fishy scents, presumably through conditioning to fishing boats
(Nevitt, 1999b;
Nevitt et al., 2004;
Nevitt et al., 1995).
These and other results suggested that procellariiforms within this
sub-Antarctic assemblage exploit at least two fundamentally different sensory
strategies for ARS. DMS responders are adapted to forage opportunistically on
small or less concentrated prey patches, whereas more aggressive species (e.g.
albatross, Diomedeidae, and giant petrels, Macronectes) are better adapted to
exploit multi-modal cues, which include scents from crushed prey and visual
cues associated with the activity of other birds and marine predators
(Nevitt, 1999b;
Nevitt and Bonadonna, 2005b;
Nevitt et al., 2004).
Evolutionary questions
We have now categorized search strategies for a number of species and
species groups, and have begun to explore these behaviors using phylogenetic
techniques (Van Buskirk and Nevitt,
2008). These analyses show that odor responsiveness is linked to
life history strategy (Fig. 5).
This surprising result has suggested to us that the early environment that
chicks experience may be linked to the evolution of different sensory-based
foraging strategies among the procellariiforms. Compared with other birds,
procellariiforms have a lengthy chick-rearing period that can last from 6
weeks in some species to nearly a year in some of the larger albatrosses
(Warham, 1990). Thus, chicks
reared in burrows spend their early life in a dark, underground nest, where
odors are likely to dominate their early sensory experience. Moreover, because
predation on chicks tends to be extreme in breeding colonies, burrow-nesting
chicks usually remain deep underground in the dark until just before fledging.
By contrast, chicks reared above ground or in surface crevices grow up with
early access to light, and are exposed to a wide range of stimuli, including
visual, auditory and olfactory inputs. In an evolutionary framework, these
differences in rearing environment could lead to differences in sensory
function.
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; Imber,
1985; Kennedy and Page,
2002; Nunn and Stanley,
1998), and the underlying phylogenetic relationships between the
subgroups are well researched. Using comparative methods, we found that burrow
nesting was significantly correlated to DMS tracking behavior, but not to a
behavioral attraction to odors more directly associated with macerated krill
or fish (including pyrazines or trimethylamine)
(Van Buskirk and Nevitt, 2008)
(Fig. 5C). Ancestral trait
reconstruction further indicated that the procellariiforms arose from a
burrow-nesting lineage, with the albatrosses and the fulmarine petrels
independently adopting a surface-nesting strategy
(Fig. 6). The implication is
that the move to the surface may have constituted a life history innovation
that presented new opportunities for selection to act on the development of
other sensory modalities (most likely vision), while relaxing the need to
track prey by scent, and offers new questions to explore. For example,
surprisingly few studies have investigated anatomical or functional
differences in eye structure among the procellariiforms, and our results
suggest that a more complete characterization of these structures is warranted
(see discussion in Nevitt et al.,
2008). Equally interesting is that burrow nesting appears to be an
ancestral trait, suggesting that some degree of DMS sensitivity may also have
been an ancestral condition for the Procellariiformes and their sister order,
the Sphenisciformes (penguins). Penguins are generally not thought to be
particularly olfactory birds, but since they also forage in productive areas
that are characterized by high levels of DMS
(Culik, 2001), their olfactory
abilities should be further investigated. Interestingly, little penguins
(Eudyptula minor) not only nest underground but also show tube-like
structures on their nares during development
(Kinsky, 1960).
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Developmental mechanisms
In parallel with our phylogenetic work, we have been investigating how
olfactory behaviors develop in burrow-nesting chicks. Blue petrels
(Halobaena caerulea) are a common burrow-nesting species in the
sub-Antarctic and they have served as an important model for these
investigations. Adults forage opportunistically on a variety of crustaceans
(including euphausids, gammarid and hyperiid amphipods, mysids, decapods and
copepods), squid and fish (Ridoux,
1994). We have shown that they respond to experimental deployments
of DMS and fishy-smelling odors at sea
(Nevitt et al., 1995), and
that foraging activity is associated with areas of naturally elevated DMS
concentrations (Nevitt,
2000).
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;
Nevitt et al., 2006)
(Fig. 7A,B). However, they can
also detect scents like rosy-smelling phenyl ethyl alcohol (PEA), which they
would likely never encounter in nature
(Cunningham et al., 2003;
Nevitt et al., 2006). To test
whether and which of these odors also elicit olfactory search, we studied
chicks' responses to odors using a simple wind tunnel developed for field use.
While we did not test DMS in this context, we found that blue petrel chicks
responded to fishy-smelling odors but not to PEA by increasing their turning
behavior (Cunningham et al.,
2006). This search behavior was monitored in chicks 3–4
weeks before fledging, when their parents were still provisioning them, and is
typical of olfactory search in other animals
(DeBose and Nevitt, 2008;
Moore and Crimaldi, 2004).
One of the questions we are currently exploring is whether odor preference
is innate or, rather, learned through interactions with parents in the nest to
prepare the chick to forage on its own after fledging. Like other
procellariiforms, blue petrels provision chicks until a few weeks prior to
fledging, at which time they are abandoned. Although other types of seabird
provision and likely tutor their offspring at sea after fledging
(Davoren and Montevecchi,
2003), procellariiform fledglings are adapted to forage on their
own after leaving the nest. How they are able to accomplish this task is
widely debated, and it is generally assumed that fledglings rely on the
activity of other seabirds to find food
(Ward and Zahavi, 1973).
However, in a variety of other organisms, juveniles learn foraging odors
through interactions with their parents
(Hudson et al., 1999;
Schaal et al., 2000;
Vargas and Anderson, 1996).
Although blue petrel chicks should be naive to DMS as they are growing up in
the burrow, we have observed that adult birds often smell like DMS or
phytoplankton when they return to the colony to provision chicks. This
observation inspired us to test the response of more ambulatory blue petrel
fledglings to DMS at very low concentrations (10–12 mol
l–1) just days before they were to leave the nest to forage.
Using a simple Y-maze design, we found that blue petrel fledglings were
attracted to DMS over a control odor, suggesting that a preference for DMS is
already established before chicks leave the nest
(Fig. 7C,D)
(Bonadonna et al., 2006).
These results provide a framework for understanding how foraging behavior
develops in blue petrels, and perhaps in other burrow-nesting species as well.
Our current hypothesis is that, prior to fledging, chicks acquire information
about prey-related odors through feeding interactions with their parents.
Scents that the fledgling has previously associated with feeding may then
serve to alert the bird to potential foraging opportunities as they are
encountered at sea. These foraging opportunities will likely also involve
interactions with hetero- or conspecifics
(Silverman et al., 2004;
Ward and Zahavi, 1973). As the
fledgling gains foraging experience, it acquires a working knowledge of
potential foraging locations by associating foraging success with other cues
(e.g. scent cues associated with prey or productivity, visual cues provided by
other seabirds, geomagnetic references associated with foraging location). It
follows that a bird might thus develop a map of foraging locations, which are
tied to spatially explicit features (such as a shelf break or seamount, for
example). However, in the marine environment, productive foraging areas are
dynamic. Foraging opportunities typically vary both temporally and spatially
over large areas (for example, over upwelling and convergence zones),
suggesting that any map cannot be strictly or entirely spatially explicit, but
must be used together with proximate cues that allow the bird to recognize
when it has arrived in a profitable zone to forage
(Nevitt, 2000). Whether the
foraging location is spatially fixed (such as a seamount) or dynamic (such as
an upwelling or convergence zone), scent cues associated with trophic
interactions would provide a foraging petrel with immediate feedback as to
whether foraging is likely to be successful at that particular time or
place.
Olfactory navigation
Because DMS is produced by phytoplankton, which often occurs in spatially
predictable locations, a logical extension of this model is that an ability to
recognize predictable features such as shelf breaks or seamounts by scent may
also be adaptive for navigation as the bird matures. Although olfactory
navigation has been controversial in other avian systems, most notably in the
context of pigeon homing (Able,
1995; Alerstam,
2006), much of the debate has centered on the inherent problems of
identifying a biogenic scented compound or suite of compounds that pigeons can
detect at appropriate concentrations and therefore utilize as a substrate for
an olfactory map (reviewed by DeBose and
Nevitt, 2008; Wallraff and
Andreae, 2000). By contrast, in the marine environment, DMS is
clearly linked to a physical source (phytoplankton) and association with
predictable oceanic features is established (reviewed by
Nevitt, 2000). Until recently,
what was lacking was a clear demonstration that a procellariiform was
sensitive enough to detect DMS at concentrations that would typically be
encountered at sea (10–12 to 10–9 mol
l–1) since these concentrations are as much as a million
times lower than previously reported odor sensitivities for birds (reviewed by
Roper, 1999). We have since
used heart rate monitoring techniques to demonstrate that Antarctic prions
(Pachyptila desolata) can physiologically detect DMS at
5x10–9 mol l–1, which was, for
technical reasons, the lowest concentration we tested. We have also shown that
these birds (as well as blue petrel fledglings, discussed earlier) will orient
to DMS in non-foraging contexts in simple Y-maze experiments at concentrations
as low as 10–12 mol l–1
(Nevitt and Bonadonna, 2005b).
Considering that many species routinely travel in the dark or under conditions
where visibility is limited by fog or extreme cloud cover, these results
provide some of the most compelling evidence to date that an olfactory
landscape superimposed upon the ocean is detectable to seabirds, and may
present navigational guideposts in non-foraging contexts.
Navigation systems tend to involve multimodal cues, however, and the
spatial scales over which birds operate suggest that geomagnetic cues might be
useful for cross-referencing positional information of olfactory features that
are spatially predictable. Several albatross and petrel species [including
black-browed albatross (Diomedea melanophris), waved albatross
(Diomedea irrorata), wandering albatross (Diomedea exulans)
and white-chinned petrels (Procellaria aequinoctialis)] have been
investigated with this in mind, but do not apparently rely on earth-strength
magnetic cues to navigate back to a nesting colony
(Benhamou et al., 2003;
Bonadonna et al., 2005;
Mouritsen et al., 2003).
Because navigation systems tend to be redundant
(Able, 1995;
Papi, 2006), these studies do
not rule out the possibility that procellariiforms are sensitive to
earth-strength magnetic fields. Many of the breakthroughs made in
investigating geomagnetic orientation in marine organisms have been
accomplished by manipulating test subjects (for example, sea turtles and spiny
lobsters) in experimental coil systems (see
Lohmann et al., 2008), and
these methods have not yet been used to test procellariiforms even though they
may be tractable for this type of investigation. While our research has
focused on olfaction, how sensory information is integrated across different
modalities is not known for this group of seabirds or, perhaps, for any marine
organism (see discussion in DeBose and
Nevitt, 2008; Nevitt et al.,
2008). Gaining a more thorough understanding of the sensory worlds
these birds inhabit will be an exciting area for future work.
Individual recognition
During the breeding season, procellariiforms must be able to relocate their
nest or burrow, often in dense colonies among hundreds of other birds. This
topic has been studied extensively in a variety of petrels, and the best
evidence to date suggests that odor cues are required for nest-site relocation
in burrow-nesting species (for a review, see
Nevitt and Bonadonna, 2005a).
How this behavior develops has received much less attention, but may be a key
to understanding how procellariiforms learn individual-specific odor cues for
use in other social contexts. One of the few published studies addressing this
topic found that European storm-petrel (Hydrobates pelagicus) chicks
required an intact sense of smell to relocate their burrows after they had
been displaced short distances (1 m) from them
(Minguez, 1997). Subsequent
experiments revealed that these chicks could distinguish their own body odor
from a control scent, or even when tested against the scent of a conspecific
(De Leon et al., 2003). The
European storm-petrel population where these researchers worked was somewhat
unusual for the species in that adults tended to nest in caves where chicks
were observed wandering out of their burrows into enclosed, protected
crevices. The researchers logically concluded that individual odor recognition
was thus adaptive for homing behavior, because parents were only observed
feeding chicks within the nest cavity, and chicks needed to return to the
proper cavity to be fed (Minguez,
1997). As it turns out, however, this situation is not typical for
European storm-petrels (e.g. Cramp et al.,
1976). Due to heavy predation in colonies, storm-petrel chicks are
much more likely to be confined to their burrow until they are ready to
fledge. This more typical situation suggested to us that learning to recognize
personal scents may be adaptive to the development of kin recognition in the
context of both dispersal and mate choice
(O'Dwyer et al., 2008).
We have since re-examined individual odor recognition using Leach's
storm-petrels (Oceanodroma leucorhoa) as a model system. Leach's
storm-petrels dig burrows up to 1 m deep where they lay a single egg, and
chicks do not typically survive if they leave the burrow prior to fledging. In
addition, our previous work indicates that Leach's storm-petrels are not
natally philopatric to the nesting colony (E. Milot, L. Bernatchez and G.A.N.,
unpublished observations), suggesting that learning the scent of their own
nest is not necessary for relocating the home colony once an individual
reaches breeding age. Using simple choice tests, our results showed that
Leach's storm-petrel chicks could recognize petrel-scented nest material, and
could easily distinguish scents associated with their own nest material from
scents associated with a conspecific's nest material. Given that an ability to
recognize individual odor is not adaptive for homing at this life stage, these
data suggest that the development of individual-specific odor recognition may
serve other functions (O'Dwyer et al.,
2008).
In line with this idea, we have also demonstrated that adult Antarctic
prions (Pachyptila desolata) can perform individual choice tests
based on scent alone (Fig. 8)
(Bonadonna and Nevitt, 2004).
Like other burrow-nesting procellariiforms, Antarctic prions return to
colonies at night, and most interaction on land occurs underground, in dark
burrows, suggesting that a chemically mediated identification system would be
adaptive. The behavioral tests again employed a simple Y-maze design that
allowed us to test responses to individual odors, collected from birds by
first placing them in clean cotton bird bags and then passing air over the
scented bags in the maze. We found that the majority of test birds preferred
conspecific odor to their own odor, suggesting that birds were attracted to
less familiar scents (Fig. 8A).
This result was surprising because, like other procellariiforms, pairs are
socially and biologically monogamous and philopatric to a single burrow. What
is more, incubating birds do not typically explore other burrows because
predation pressure can be severe in colonies even for adult birds that wander
outside their burrows (e.g. Warham,
1996). In combination with these experiments, we also tested
whether birds could recognize the scent of their mate. Here we found that
birds tended to prefer the scent of their partner to the odor of a random
conspecific (Fig. 8B).
Additional tests showed that prions preferred their own personal odor, but
only when tested against a blank odor (Fig.
8C).
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Future directions
Together, these results have led us to wonder whether odors may also play a
role in mate choice (Zelano and Edwards,
2002). The potential that scent-based cues contribute to mate
choice decisions has been typically overlooked in birds [for exceptions, see
Douglas (Douglas, 2008);
Hagelin (Hagelin, 2004) and
Hagelin and Jones (Hagelin and Jones,
2007)] but kin recognition is mediated by scent in a wide range of
vertebrates, including humans (Wedekind et
al., 1995), mice (Yamazaki et
al., 1976; Yamazaki et al.,
1979), fish (Reusch et al.,
2001) and lizards (Olsson et
al., 2003). Given that breeding birds form long-term pair bonds,
producing just one egg per season with, presumably, little or no extra-pair
paternity (Austin and Parkin,
1996; Quillfeldt et al.,
2001; Swatscheck et al.,
1994), selecting an appropriate mate is critical to lifetime
reproductive success. Although we know little about how procellariiforms
choose mates and establish long-term pair bonds
(Jouventin et al., 1999), the
fact that many procellariiform species are natally philopatric to remote
islands (Warham, 1990)
suggests that mechanisms may have evolved to avoid breeding with close kin and
to enhance genetic diversity.
Although work in this context is still in its infancy, this new avenue of
research suggests that the odor world of the procellariiforms may be much
richer than we originally suspected. Scents are used not only in foraging,
homing and, potentially, navigation, but also within social and familial
interactions. The data that we have collected so far suggest that petrels can
learn familial odors as chicks in the nest, and that adults learn to recognize
odors associated with their partner. While the underlying mechanisms are
unclear, it is well established that genes of the major histocompatibility
complex influence individual odors in other systems
(Penn and Potts, 1998). This
highly polymorphic set of genes encodes a range of molecules involved in
immune responses and self–non-self recognition. Characteristics of the
major histocompatibility complex, in turn, influence mating preferences in a
diverse range of vertebrate groups
(Carroll et al., 2002;
Milinski et al., 2005;
Penn and Potts, 1999). Thus,
an intriguing future area of research will be to explore the mechanistic basis
of individual recognition in the context of mate choice, and whether or not
the major histocompatibility complex is involved.
Acknowledgments
I thank Ken Lukowiak and Janis Weeks for organizing this most inspiring symposium on neurosensory ecology. I am also grateful to M. Losekoot, T. O'Dwyer and R. Van Buskirk for thoughtful discussion and editorial assistance, F. Bonadonna, D. Shutler, P. Trathan and H. Weimerskirch for logistical support at Kerguelen, Bon Portage, South Georgia and Crozet, and to R. R. Veit and P. Kareiva for introducing me to seabirds. This work was largely made possible through collaboration with the French polar institute (IPEV program no. 109 and no. 354) and the British Antarctic Survey with additional support from NSF and NGS. Contribution number 2412, Bodega Marine Laboratory, University of California, Davis.
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