|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online September 19, 2008
Journal of Experimental Biology 211, 3123-3127 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018325
African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour
1 Percy FitzPatrick Institute DST/NRF Centre of Excellence, University of Cape
Town, Rondebosch 7701, South Africa
2 Southern African Foundation for the Conservation of Coastal Birds, PO Box
11116, Bloubergrand 7443, South Africa
* Author for correspondence at present address: Department of Biology, St John Fisher College, 3690 East Avenue, Rochester, New York, NY 14618, USA (e-mail: gcunningham{at}sjfc.edu)
Accepted 15 July 2008
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: olfaction, African penguin, Spheniscus demersus, dimethyl sulphide, foraging behaviour
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
;
Hackett et al., 2008) and
share many common traits with respect to their foraging behaviour. For
example, species within these two broad groups tend to forage on similar types
of prey, such as krill, fish and squid, and exploit similar ocean habitats
(for reviews, see Warham,
1990; Williams,
1995). Furthermore, both penguins and procellariiforms must search
for relatively small and ephemeral productive locations where prey aggregate
(reviewed in Weimerskirch,
2007). Finally, members of both orders tend to nest in large
colonies and are central place foragers during the breeding season
(Stephens and Krebs, 1986;
Williams, 1995). Despite these
many similarities, it is typically assumed that these birds use different
sensory modalities to locate prey. Procellariiforms have large olfactory bulbs
(Bang and Cobb, 1968),
suggesting that they hunt by smell. Numerous studies have confirmed this, as
procellariiforms are attracted to a variety of prey-related odours at sea such
as fishy smelling compounds (Nevitt et
al., 2004) and the scent of krill
(Nevitt, 1999b). By contrast,
it is typically thought that penguins are primarily visual hunters
(Wilson et al., 1993;
Wilson and Wilson, 1995;
Ryan et al., 2007), and the
potential use of olfactory cues by penguins for foraging has largely been
ignored (but see Culik et al.,
2000; Culik,
2001).
A first step in determining whether penguins use odours to hunt is to
demonstrate whether or not penguins have a functioning sense of smell.
Dimethyl sulphide (DMS) is a scented compound produced by phytoplankton that
is elevated when they are grazed upon by zooplankton
(Dacey and Wakeham, 1986;
Wolfe and Steinke, 1996), and
is associated with seamounts and shelf breaks
(Berresheim et al., 1989;
Daly and DiTullio, 1996;
McTaggart and Burton, 1992)
where seabirds tend to forage (reviewed by
Nevitt, 2000). Nevitt et al.
(Nevitt et al., 1995)
demonstrated that DMS serves as a foraging cue (see also
Van Buskirk and Nevitt, 2008).
Since many petrels forage on zooplankton, high levels of DMS may be a reliable
indicator of the birds' prey (reviewed by
Nevitt, 2000). Other studies
on marine animals such as the harbour seal (Phoca vitulina) and the
predatory copepod (Temora longicornis) suggest that this odour is
used by a wide variety of marine predators to locate prey in the ocean (see
Kowalesky et al., 2006; Steinke et al.,
2006). Testing the responses of birds to odours at sea is
difficult (Nevitt, 1999a)
(reviewed by Nevitt, 2008) but
techniques have been developed for testing animals in colonies or experimental
laboratories in field settings.
In the present study, we tested whether African penguins (Spheniscus
demersus L.) responded to artificial sources of DMS. African penguins are
currently listed as a `vulnerable' species
(Birdlife International, 2004),
breeding exclusively on the coast and coastal islands of Namibia and South
Africa (Shannon and Crawford,
1999). They feed primarily on anchovies (Engraulis
capensis) and sardines (Sardinops sagax), and competition for
food with the commercial purse seine fishery is one of the key factors driving
current population decreases (Crawford and
Dyer, 1995; Crawford et al.,
2001; Crawford et al.,
2006). In the present study, we examined whether wild African
penguins could detect DMS by deploying this scent in the penguin colony
(Clark and Shah, 1992;
Nevitt and Haberman, 2003). We
confirmed attraction to DMS using a Y-maze, a technique that has previously
been used in olfactory studies with birds (e.g.
Bonadonna et al., 2003).
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). Most breeding birds at this time of year are rearing chicks
(Cooper, 1980), when adults
head to sea daily to provision their young
(Petersen et al., 2006).
Penguins breed in burrows or under the cover of introduced Acacia
cyclops trees, 10–200 m from the shore, and commute along paths
between their nests and the sea. We took advantage of these well-utilized
routes to investigate whether birds could detect and would respond to DMS
released in the colonies.
We deployed DMS (1 µmolar dissolved in 25 ml distilled water) or a
control (25 ml distilled water) in Petri dishes along three separate penguin
walkways. These sites were separated by approximately 500 m. The concentration
of DMS used in the present study is similar to what has been used in
preliminary tests of procellariiform responses to DMS in the past
(Cunningham et al., 2003).
Flags were placed 1.5 m from the Petri dish in each direction along the
walkway. We recorded the time interval that randomly selected penguins spent
within the 3 m span between the two flags. Observations were conducted from
approximately 30 m from the walkway using 10x50 binoculars in the
morning following sunrise (07.30–09.00 h), when most penguins head to
sea, and in the evening prior to sunset (16.30–18.00 h), when they
return to the island to provision young
(Wilson, 1985a;
Petersen et al., 2006). Wind
direction was offshore on all three days. Thus, as penguins exited the colony,
they walked downwind whereas when they approached the colony from the sea they
walked upwind. Since penguins were either walking from the nest to the beach
or returning from the sea back to their nests, each individual only walked
once through the 3 m span during each observation period. Thus, no penguin was
counted more than once on any given day. Observations were collected in a
blind fashion such that the observer did not know the identity of the solution
that was deployed along the walkway. We used an unpaired t-test
(Zar, 1996) to test whether
birds spent significantly different amounts of time in the presence of DMS
compared with the presence of the control. Using the same test, we also
compared whether there was a significant difference in the time spent between
the flags for birds in the morning compared with the evening.
Testing responses of captive birds to odours in a Y-maze
Thirty-one captive adult African penguins of unknown age and sex were
tested for their attraction to DMS at the Southern African Foundation for the
Conservation of Coastal Birds (SANCCOB) facility at Rietvlei, Cape Town, South
Africa. Each year, this facility receives hundreds to thousands of injured or
oiled birds. Birds are cleaned, treated, fed for a period of four to five
weeks (Parsons and Underhill,
2005) and then released into the wild. Prior to their release, we
tested birds in a Y-maze in an outdoor pen at the facility.
The three arms of the Y-maze, each measuring 90 cm length and 53 cm in diameter, were made of opaque plastic. The Y-junction was made of opaque fibreglass. A CPU fan (model # 8850N; EBMPapst, Cape Town, South Africa) was mounted at the end of each of the odour-choice arms to generate a controlled airflow through the Y-maze (617 l min–1). In each odour-choice arm, a Petri dish was placed directly in front of the fan in a compartment separated from the maze by chicken wire. The Petri dish contained either the odour (1 µmolar DMS in 25 ml of distilled water) or a control (25 ml of distilled water). The location of the experimental and control dishes was varied throughout the trials. The Y-maze was completely cleaned with 75% methanol between trials.
Penguins were randomly chosen from the available birds at SANCCOB. These
birds had been brought to the facility because they had been oiled in the wild
and were housed in an outdoor facility in large groups (>20 birds).
Penguins were individually tested in the Y-maze between 12.00 and 15.00 h
(local time), 1.5 to 4.5 h after being fed at 10.30 h. Birds were placed, one
at a time, inside an acclimating compartment at the base of the maze for five
minutes. The compartment was separated from the rest of the Y-maze by a trap
door. Once the trap door was opened, the bird was able to proceed into the
Y-maze. To assess the choice made by the bird, we listened to the sound and
felt the vibrations of it walking in the Y-maze. A bird was considered to have
made a choice when it travelled halfway up an odour-choice arm and remained
there for at least one minute (from
Bonadonna et al., 2006). The
researcher who decided whether a penguin had made a choice was blind to the
experimental conditions of each trial. A Binomial test was used to test
whether the number of birds choosing the control arm was significantly
different from the number of birds choosing the arm scented with DMS. We also
recorded the time between the trap door opening and when a bird chose an arm;
however, so few penguins chose the control arm (see Results) that we were
unable to conduct statistical analyses on these data.
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
|
|
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
). Although the
concentration of DMS used in our study is higher than seabirds are likely to
encounter at sea (see Nevitt,
2000; Nevitt and Bonadonna,
2005b), our results are, nonetheless, an important first step
demonstrating that penguins can smell and may use olfactory cues while
foraging. We found that wild penguins were able to detect DMS deployments in
their colony. Penguins departing the colony in the morning to forage appeared
to ignore the DMS presentations, while birds returning to their nests at dusk
slowed down in response to the DMS deployments. The direction that penguins
were travelling relative to the wind may explain the differences in behaviour
that we observed between morning and evening. In the morning, penguins would
have been walking with the wind and, hence, would not be likely to detect the
DMS until they were at or past the source of the odour. The beach, however,
was located downwind of the source of our DMS deployments. Therefore, penguins
returning during the evening would be travelling into the wind and could
likely detect the presence of DMS prior to arriving at the 3 m span
surrounding the DMS source, thus modifying their behaviour. Penguins also
appear to be more likely to respond to the odour when in less of a rush, since
the pooled data support the observation that penguins returning from the sea
walked slower overall than penguins departing the colony in the morning. We
also confirmed these results by testing captive birds in a Y-maze; birds
preferred the arm of the maze that was scented with DMS. The high number of
penguins making no choice in the Y-maze that we observed may be due to the
fact that we were working with a stressed captive population that had recently
been oiled, which may have compromised their sense of smell (see
Solangi and Overstreet, 1982)
or their willingness to respond. Both results suggest that African penguins
can detect and orient towards this food-related odour.
Foraging penguins typically commute to predictable regions where
productivity tends to be high but where their prey are patchily distributed
(Williams, 1995), and thus
there is an advantage to having a way to detect prey aggregations from a
distance. While en route to a foraging zone, penguins swim faster and
dive to shallower depths than they do when they are actively foraging (e.g.
Wilson et al., 2005;
Petersen et al., 2006). Once a
productive area is located, a penguin initiates deeper dives to search for
prey. The results of the present study suggest that African penguins can
detect DMS, and this ability may assist them in foraging. Like
procellariiforms (Silverman et al.,
2004), penguins might use a multi-modal search strategy to locate
prey. On a coarse scale, the presence of high levels of DMS at the water
surface may be used to identify foraging areas where fish are located (e.g.
Nevitt, 2000;
Nevitt and Bonadonna, 2005a)
(see also Culik et al., 2000),
since dimethylsulphoniopropionate (DMSP), a precursor to DMS
(Simo, 2004), has also been
shown to serve as a foraging cue to fish across a wide phylogenetic range
(Nakajima et al., 1989;
Nakajima et al., 1990;
DeBose et al., 2008). Even
within historically productive areas, aggregations of foraging prey are likely
to be patchily distributed, and changes in airbourne odours may alert penguins
that foraging in a particular area is more or less likely to be successful.
Anchovies and sardines, the main prey of African penguins, primarily feed on
zooplankton and large phytoplankton
(James, 1987;
van der Lingen, 2002), both of
which have been implicated in the release of DMS
(Dacey and Wakeham, 1986;
Daly and DiTullio, 1996;
Wolfe and Steinke, 1996)
(reviewed by Nevitt, 2000;
Nevitt, 2008). On a finer
scale, visual cues are probably used by penguins to locate their prey. For
example, in African penguins, dive depth is limited by ambient light levels
(Wilson et al., 1993) with
little foraging at night (Wilson and
Wilson, 1995; Ryan et al.,
2007). Whether smell could be used underwater to help find prey,
as is the case in certain mammals (see
Catania, 2006), is an
intriguing question worthy of further investigation.
Studies on how seabirds use DMS to find food have previously focused on
procellariiforms that forage over great distances. For example, the blue
petrel (Halobaena caerulea), which responds to DMS as both a chick
and as an adult (Nevitt et al.,
1995; Nevitt,
2000; Cunningham et al.,
2003; Bonadonna et al.,
2006) forages over pelagic waters at distances of >1000 km from
their nesting island (Cherel et al.,
2002). The ability to smell DMS in these far-flying species is
adaptive as it allows these birds to detect aggregations of zooplankton from
greater distances than would be possible using visual cues alone. Sensitivity
to DMS also allows these birds to exploit a resource prior to the arrival of
more aggressive birds that do not respond to DMS (see
Van Buskirk and Nevitt, 2008).
Although less is known about the sensory ecology of foraging penguins, hunting
by smell is likely in this group for a variety of reasons. Firstly, penguins
are the closest relatives to the procellariiforms [see Ksepka et al.
(Ksepka et al., 2006) and
references therein] and, similar to procellariiform adults, their chicks have
a tube-nose (Kinsky, 1960).
Thus, it seems logical to predict that penguins also have a functioning sense
of smell, particularly in light of recent evidence
(Van Buskirk and Nevitt, 2008)
that suggests that DMS behavioural sensitivity is ancestral in the
procellariiforms. Secondly, although penguins generally forage over shorter
distances compared with procellariiform seabirds [17–62 km for African
penguins rearing chicks (Petersen et al.,
2006)], penguins have a slower commuting speed than flying
seabirds [4.8 km h–1 for the African penguin
(Wilson, 1985b); 23.1 km
h–1 for the white-chinned petrel (Procellaria
aequinoctialis) (Weimerskirch et al.,
1999)], thus making it costly to commute to, and dive in,
unproductive areas. Additionally, because penguins are slower, the amount of
time spent during transit to and from the foraging grounds is comparable
between penguins and procellariiforms, suggesting that these birds may be
similar in their foraging strategies. For example, while provisioning chicks,
African penguins spend 27–36.6 h away from the nest
(Petersen et al., 2006) while
a closely related congener, the Magellanic penguin (Spheniscus
magellanicus), can spend one day to a number of weeks at sea
(Wilson et al., 2005). By
comparison, while provisioning a chick, the blue petrel and thin-billed prion
(Pachyptila belcheri) alternate between short and long trips, with a
mean of 1.8/7.2 (short/long) and 1.4/6.7 days, respectively
(Chaurand and Weimerskirch,
1994; Duriez et al.,
2000).
This is the first study to clearly demonstrate, by way of experimentation,
that a penguin is able to detect an odour (see also
Culik et al., 2000;
Culik, 2001). Although the
present study does not directly test DMS as a foraging cue, it does implicate
the use of odours by penguins while hunting. Future studies at sea in which
DMS, or its precursor DMSP, are deployed into the ocean (e.g.
Nevitt et al., 1995) need to
be conducted to definitively show that penguins, like procellariiforms, are
using odours to forage.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Bang, B. G. and Cobb, S. (1968). The size of the olfactory bulb in 108 species of birds. Auk 85, 55-61.
Berresheim, H., Andreae, M. O., Ayers, G. P. and Gillett, R. W. (1989). Distribution of biogenic sulfur-compounds in the remote southern-hemisphere. In Biogenic Sulfur in the Environment (ed. E. J. Saltzman and W. J. Cooper), pp.352 -356. Washington, DC: American Chemical Society.
BirdLife International (2004). Threatened Birds of the World CD ROM. Cambridge: BirdLife International.
Bonadonna, F., Cunningham, G. B., Jouventin, P., Hesters, F. and
Nevitt, G. A. (2003). Evidence for nest-odour recognition in
two species of diving petrel. J. Exp. Biol.
206,3719
-3722.
Bonadonna, F., Caro, S., Jouventin, P. and Nevitt, G. A.
(2006). Evidence that blue petrel, Halobaena caerulea,
fledglings can detect and orient to dimethyl sulfide. J. Exp.
Biol. 209,2165
-2169.
Catania, K. C. (2006). Underwater `sniffing' by semi-aquatic mammals. Nature 444,1024 -1025.[CrossRef][Medline]
Chaurand, T. and Weimerskirch, H. (1994). The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J. Anim. Ecol. 63,275 -282.[CrossRef]
Cherel, Y., Bocher, P., Trouve, C. and Weimerskirch, H. (2002). Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, Southern Indian Ocean. Mar. Ecol. Prog. Ser. 228,283 -299.[CrossRef]
Clark, L. and Shah, P. S. (1992). Information content of prey odor plumes: what do foraging Leach's storm petrels know? In Chemical Senses in Vertebrates VI (ed. R. L. Doty and D. Muller-Schwarze), pp. 421-427. New York: Plenum Press.
Cooper, J. (1980). Breeding biology of the Jackass Penguin with special reference to its conservation. In Proceedings of the 4th Pan-African Ornithological Congress (ed. D. N. Johnson), pp.227 -231. Johannesburg: South African Ornithological Society.
Crawford, R. J. M. and Dyer, B. M. (1995). Responses by four seabirds to a fluctuating availability of Cape anchovy Engraulis capensis off South Africa. Ibis 137,329 -339.[CrossRef]
Crawford, R. J. M., David, J. H. M., Shannon, L. J., Kemper, J., Klages, N. T. W., Rioux, J.-P., Underhill, L. G., Ward, V. C., Williams, A. J. and Wolfaardt, A. C. (2001). African penguins as predators and prey – coping (or not) with change. Afr. J. Mar. Sci. 23,435 -477.
Crawford, R. J. M., Barham, P. J., Underhill, L. G., Shannon, L. J., Coetzee, J. C., Dyer, B. M., Leshoro, T. M. and Upfold, L. (2006). The influence of food availability on breeding success of African penguins Spheniscus demersus at Robben Island, South Africa. Biol. Conserv. 132,119 -125.[CrossRef]
Culik, B. (2001). Finding food in the open ocean: foraging strategies in Humboldt penguins. Zoology (Jena) 104,327 -338.[Medline]
Culik, B., Hennicke, J. and Martin, T. (2000). Humboldt penguins outmanoeuvring El Nino. J. Exp. Biol. 203,2311 -2322.[Abstract]
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 dimethyl sulfide: production during zooplankton grazing on
phytoplankton. Science
233,1314
-1316.
Daly, K. L. and DiTullio, G. R. (1996). Particulate dimethylsulfoniopropionate removal and dimethyl sulfide 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.
DeBose, J. L., Lema, S. C. and Nevitt, G. A.
(2008). Dimethylsulfoniopropionate as a foraging cue for for reef
fishes. Science 319,1356
.
Duriez, O., Weimerskirch, H. and Fritz, H. (2000). Regulation of chick provisioning in the thin-billed prion: an interannual comparison and manipulation of parents. Can. J. Zool. 78,1275 -1283.[CrossRef]
Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C. K.,
Braun, E. L., Braun, M. J., Chojnowski, J. L., Cox, W. A., Han, K.-L.,
Harshman, J. et al. (2008). A phylogenetic study of birds
reveals their evolutionary history. Science
320,1763
-1768.
James, A. G. (1987). Feeding ecology, diet and field-based studies on feeding selectivity of the Cape anchovy Engraulis capensis Gilchrist. Afr. J. Mar. Sci. 5, 673-692.
Kinsky, F. C. (1960). The yearly cycle of the Northern blue penguin (Eudyptula minor novaehollandiae) in the Wellington Harbour area. Rec. Dominion Mus. NZ 3, 145-218.
Kowalewsky, S., Dambach, M., Mauck, B. and Dehnhardt, G.
(2006). High olfactory sensitivity for dimethyl sulphide in
harbour seals. Biol. Lett.
2, 106-109.
Ksepka, D. T., Bertelli, S. and Giannini, N. P. (2006). The phylogeny of the living and fossil Sphenisciformes (penguins). Cladistics 22,412 -441.[CrossRef]
McTaggart, A. R. and Burton, H. (1992). Dimethyl sulfide concentrations in the surface waters of the Australasian Antarctic and Sub-Antarctic oceans during an austral summer. J. Geophys. Res. Oceans 97,14407 -14412.[CrossRef]
Nakajima, K., Uchida, A. and Ishida, Y. (1989).
A new feeding attractant,
dimethyl-
Nakajima, K., Uchida, A. and Ishida, Y. (1990). Effect of a feeding attractant, dimethyl-β-propiothetin on growth of marine fish. Nippon Suisan Gakkai Shi 56,1151 -1154.
Nevitt, G. A. (1999a). Foraging by seabirds on an olfactory landscape. Am. Sci. 87, 46-53.[CrossRef]
Nevitt, G. A. (1999b). Olfactory foraging in Antarctic seabirds: a species-specific attraction to krill odors. Mar. Ecol. Prog. Ser. 177,235 -241.[CrossRef]
Nevitt, G. A. (2000). Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol. Bull. 196,245 -253.
Nevitt, G. A. (2008). Sensory ecology on the
high seas: the odor world of the procellariiform seabirds. J. Exp.
Biol. 211,1706
-1713.
Nevitt, G. A. and Bonadonna, F. (2005a). Seeing the world through the nose of a bird: new developments in the sensory ecology of procellariiform seabirds. Mar. Ecol. Prog. Ser. 287,292 -295.
Nevitt, G. A. and Bonadonna, F. (2005b).
Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation
by seabirds. Biol. Lett.
1, 303-305.
Nevitt, G. A. and Haberman, K. (2003).
Behavioral attraction of Leach's storm-petrels (Oceanodroma
leucorhoa) to dimethyl sulfide. J. Exp. Biol.
206,1497
-1501.
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]
Nevitt, G. A., Reid, K. and Trathan, P. (2004).
Testing olfactory foraging strategies in an Antarctic seabird assemblage.
J. Exp. Biol. 207,3537
-3544.
Parsons, N. J. and Underhill, L. G. (2005). Oiled and injured African penguins Spheniscus demersus and other seabirds admitted for rehabilitation in the Western Cape, South Africa, 2001 and 2002. Afr. J. Mar. Sci. 27,289 -296.
Petersen, S. L., Ryan, P. G. and Gremillet, D. (2006). Is food availability limiting African penguins Spehniscus demersus at Boulders? A comparison of foraging effort at mainland and island colonies. Ibis 148, 14-26.[CrossRef]
Ryan, P. G., Petersen, S. L., Simeone, A. and Gremillet, D. (2007). Diving behaviour of African penguins: do they differ from other Spheniscus penguins? Afr. J. Mar. Sci. 29,153 -160.[CrossRef]
Shannon, L. J. and Crawford, R. J. M. (1999). Management of the African penguin Spheniscus demersus-insights from modelling. Mar. Ornithol. 27,119 -128.
Silverman, E. D., Veit, R. R. and Nevitt, G. A. (2004). Nearest neighbors as foraging cues: information transfer in a patchy environment. Mar. Ecol. Prog. Ser. 277, 25-35.[CrossRef]
Simo, R. (2004). From cells to globe: approaching the dynamics of DMS(P) in the ocean at multiple scales. Can. J. Fish. Aquat. Sci. 61,673 -684.[CrossRef]
Solangi, M. A. and Overstreet, R. M. (1982). Histopathological changes in two estuarine fishes, Menidia beryllina (Cope) and Trinectes maculatus (Bloch and Schneider) exposed to crude oil and its water-soluble fraction. J. Fish Dis. 5, 13-35.[CrossRef]
Steinke, M., Stefels, J. and Stamhuis, E. (2006). Dimethyl sulfide triggers search behavior in copepods. Limnol. Oceanogr. 51,1925 -1930.
Stephens, D. W. and Krebs, J. R. (1986). Monographs in Behavior and Ecology: Foraging Theory. Princeton, NJ: Princeton University Press.
Van Buskirk, R. W. and Nevitt, G. A. (2008). The influence of developmental environment on the evolution of olfactory foraging behaviour in procellariiform seabirds. J. Evol. Biol. 21,67 -76.[Medline]
Van der Lingen, C. D. (2002). Diet of sardine Sardinops sagax in the southern Benguela upwelling ecosystem. Afr. J. Mar. Sci. 24,301 -316.
Warham, J. (1990). The Petrels: Their Ecology and Breeding Systems. London: Academic Press.
Weimerskirch, H. (2007). Are seabirds foraging for unpredictable resources? Deep-Sea Res. Part II Oceanogr. Res. Pap. 54,211 -223.
Weimerskirch, H., Catard, A., Prince, P. A., Cherel, Y. and Croxall, J. P. (1999). Foraging White-chinned Petrels Procellaria aequinoctialis at risk: from the tropics to Antarctica. Biol. Conserv. 87,273 -275.[CrossRef]
Williams, T. D. (1995). The Penguins Spheniscidae. Oxford: Oxford University Press.
Wilson, R. P. (1985a). Diurnal foraging patterns of the Jackass Penguin. Ostrich 56,212 -214.
Wilson, R. P. (1985b). The Jackass Penguin (Spheniscus demersus) as a pelagic predator. Mar. Ecol. Prog. Ser. 25,219 -227.[CrossRef]
Wilson, R. P. and Wilson, M. P. T. (1995). The foraging behaviour of the African Penguin Spheniscus demersus. In The Penguins (ed. P. Dann, I. Norman and P. Reilly), pp. 244-265. Chipping Norton: Surrey Beatty.
Wilson, R. P., Puetz, K., Bost, C. A., Culik, B. M., Bannasch, R., Reins, T. and Adelung, D. (1993). Diel dive depth in penguins in relation to diel vertical migration of prey: whose dinner by candlelight? Mar. Ecol. Prog. Ser. 94,101 -104.[CrossRef]
Wilson, R. P., Scolaro, J. A., Gremillet, D., Kierspel, M. A. M., Laurenti, S., Upton, J., Gallelli, H., Quintana, F., Freke, E., Muller, G. et al. (2005). How do Magellanic penguins cope with prey variability in their access to prey? Ecol. Monogr. 75,379 -401.[CrossRef]
Wolfaardt, A. C., Underhill, L. G., Crawford, R. J. M. and Klages, N. T. W. (2001). Results of the 2001 census of African penguins Spheniscus demersus in South Africa: first measures of the impact of the Treasure oil spill on the breeding population. Trans. R. Soc. S. Afr. 56, 45-49.
Wolfe, G. V. and Steinke, M. (1996). Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxley. Limnol. Oceanogr. 41,1151 -1160.
Zar, J. H. (1996). Biostatistical Analysis 3rd Edn. Upper Saddle River, NJ: Prentice Hall.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
