Surface pauses in relation to dive duration in imperial cormorants; how much time for a breather?
1 Institut für Meereskunde, Düsternbrooker Weg 20, D-24105 Kiel,
Germany
2 Centro Nacional Patagonico (Conicet) (9120) Puerto Madryn, Chubut,
Argentina
* Author for correspondence (e-mail: rwilson{at}ifm.uni-kiel.de)
Accepted 8 March 2004
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Summary |
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Key words: diving, imperial cormorant, Phalacrocorax atriceps, oxygen saturation curve, time optimization, surface interval between dives
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Introduction |
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In an interesting consideration of the law of diminishing returns, Kramer
(1988) pointed out that, since
oxygen uptake rate at the surface was dependent on tissue deficit, maximum
uptake rates should be achieved in animals that surface with oxygen reserves
virtually exhausted. A consequence of this is that animals attempting to
minimize time at the surface should not dive with body tissues saturated with
oxygen, but rather only with that needed for the dive. This incorporates point
(2) above and leads to the prediction of point (3), ultimately leading to the
conclusion that diving animals need not have a systematic ideal single level
of oxygen concentration in the body, but rather that the ideal pre-dive level
must be highly variable if time is to be optimised
(Wilson et al., 2003
).
In view of the complexities discussed above, any attempt to understand the relationship between dive and surface duration should consider data where the diving animal is in steady state. That is to say that dive duration should be constant over a series of dives so that surface pauses may also stabilize, incorporating both the recovery and preparation components. The dive/pause relationship should also be determined for different batches of dives to different depths so that a general strategy, resulting from different amounts of oxygen being used, can be alluded to. Finally, since even within a constant dive duration regime, diving animals might show some variability in pre-dive levels of oxygen (this being mediated by more or less extended surface pauses), it would be helpful if dives were not considered singly but in a series as a cumulative surface duration plotted against a cumulative dive duration, the slope of this regression identifying the dive/pause relationship and automatically ironing out inconsistencies that might occur in particular surface pauses.
To this end, we used imperial cormorants Phalacrocorax atriceps,
which are known to forage primarily benthically at a particular locality in
Argentina (Sapoznikow and Quintana,
2003; Punta et al.,
1993
) where bottom topography changes only very slowly (F.
Quintana, unpublished data). Since, in cormorants, the time for transit from
the water surface to the seabed and back accounts for a substantial part of
the time underwater (Wilson and Wilson,
1988
; Croxall et al.,
1991
; see later), swim speed is constant
(Wilson and Wilson, 1988
) and
bottom duration tends to increase in a predictable manner with increasing dive
depth (Wilson and Wilson,
1988
; Croxall et al.,
1991
; Grémillet et al.,
1999
; see later), we reasoned that use of these birds in this
locality would give us the best chance of attaining the steady state
conditions referred to above. This paper describes how imperial cormorants
partition their time into dive and pause durations as a function of water
depth and how the various strategies that they adopt might be used to optimize
for time. Although this work considers imperial cormorants in detail, it
potentially applies to all air-breathing diving animals and thus has broad
implications for aquatic birds, mammals and reptiles.
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Materials and methods |
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Timedepth recorders (TDR Mk7, Wildlife Computers, Woodinville, WA, USA) were deployed on 15 adult male imperial cormorants during the first 10 days of the chick-rearing period. The TDRs measured 10 cmx2 cmx1 cm and weighed 30 g, less than 1.5% of adult body mass. Devices were attached to the feathers in the centre of the back, using waterproof tape and two cable ties. The procedure was completed in less than 5 min and birds quickly returned to their nest. All birds carrying devices continued breeding normally during the study period. Depth data were recorded with a resolution of 0.5 m andrecorded at 1 Hz. Birds were recaptured after several foraging trips (110, undertaken during periods of 15 days), the TDRs removed and the data downloaded.
Data obtained from the TDRs were analysed using the programme MTDIVE (Jensen Software Systems, Laboe, Germany). This programme displays the depth data against time graphically and then places cursors at the start and end of dives as well as at points of inflection in the dive profile, to indicate the initiation of the bottom phase where birds forage along the seabed. The appropriateness of the cursor positions was checked visually by the user before the data were written to an ASCII spreadsheet with the following parameters for each dive being determined: the time of initiation of each dive, the durations and rates of the descent, bottom and ascent phases as well as the maximum depth reached during the dive. Data were then processed using EXCEL, TABLECURVE and STATEASY software packages. Although all dives were analysed for determination of the rates of descent and ascent as well as the time spent in the bottom phase of the dive, dives were specifically selected for consideration of the ratio of the pause duration:dive duration versus dive duration (see earlier). Here, only those data were considered where birds had dived consistently to a specific depth, not varying by more than 10% for the duration of the bout considered, and where at least 20 dives had been conducted in succession (see rationale in the Introduction).
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Results |
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3149 dives in total were analysed for standard dive parameters, and 47 bouts from 14 birds (no more than 5 per individual) for determination of the relationship between the ratio pause duration:dive duration and dive duration.
Consideration of the cumulative pause duration versus the dive duration in a dive sequence showed a steady increase in both parameters, provided that water depth during that sequence remained constant (Fig. 1). Where water depths were shallow the gradient flattened off, steepening again when dive depth increased (Fig. 1).
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The time spent descending and ascending the water column during dives was strongly linearly correlated with depth (Fig. 2) with birds taking about 0.67 s to descend and ascend every 1 m of water depth, resulting in vertical travelling speeds of the order of about 1.5 m s-1, irrespective of the maximum depth to which they dived. A similar, though less strong, correlation was apparent between the time spent on the bottom and maximum depth achieved during the dive, where birds spent an average of 25 s plus approx. 1.2 s for every 1 m depth dived (Fig. 2B). Thus, taking all parameters together, birds diving deeper dived for longer periods (Fig. 2D). Longer periods underwater, however, resulted in longer periods spent at the surface; graphical examination of the regression of the slope of the cumulative pause duration divided by the cumulative dive duration (y-axis) as a function of dive duration (x-axis) showed that during deeper, longer dives, the pauses became proportionally longer with the best fit curve having the form Ts=0.374+0.00558Tu+ 2.744x10-7Tu3 (r2=0.65, F=81.0, P<0.001; residuals normally distributed (ShapiroWilk test), W=0.98), where Ts is the time at the surface (s) and Tu is the time spent underwater (s) (Fig. 3).
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Discussion |
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Overall, the results obtained by us for the imperial cormorant accord with
those presented for other species of cormorant: dive duration appears linearly
related to maximum dive depth, rates of descent and ascent are roughly
constant and the time spent on the bottom increases with increasing dive depth
(e.g. Croxall et al., 1991;
Wanless and Harris, 1991
;
Wanless et al., 1993
;
Grémillet et al.,
1999
).
For our cormorants, the relationships between the time taken for the
descent, bottom phase, ascent and maximum depth reached during the dive means
that the total time spent by birds underwater can be readily calculated as:
![]() | (1) |
![]() | (2) |
The energy used during the time underwater can be approximated by data
derived from great cormorants Phalacrocorax carbo by Schmidt et al.
(1995) where, at speeds of
ca. 1.5 m s-1, birds had a power consumption of 35 W
kg-1. We assume, for simplicity, that these power requirements are
independent of depth or dive angle, although it is known that air in the
plumage and respiratory spaces affects the work done by diving birds as a
function of depth (Lovvorn et al.,
1999
; Sato et al.,
2002
). We note, however, that this effect is likely to be
minimized in cormorants, which have less plumage air than any other bird
(Wilson et al., 1992
). Using
the conversion factor of 1 litre of oxygen being needed for every 20.1 kJ
(Schmidt-Nielsen, 1993
) and
assuming that birds weigh on average 2.5 kg (our unpublished data), we can
calculate oxygen use (VO2) (in l) as a function
of dive duration to be:
![]() | (3) |
During steady state diving such as that studied by us, this amount of
oxygen is repaid at the surface during a pause duration
(Ts) that is related to time underwater by:
![]() | (4) |
![]() | (5) |
The expression in Equation 5
above gives the mean rate of oxygen uptake over the whole of the surface
pause, incorporating both the dive and the observed pause durations. Although
derivation of a mean value implies that the rate of gas exchange does not
change over the considered pause duration this is not the case. At any one
time within the pause period, irrespective of bird body oxygen concentration
at the beginning or end of the pause, the rate of uptake of oxygen into the
body is likely to be a direct function of the difference in partial pressure
between the air (PairO2) and the bird body
tissues (PbirdO2). Note that this assumes that
blood flow to the lungs is constant, mediated by constant tachycardia and
appropriate blood shunting (Butler and
Jones, 1997; Butler,
1998
), so that at any one time:
![]() | (6) |
Since, during steady state diving, the total oxygen uptake during the surface pause is equal to that expended during the period underwater, this is given by the integral of the rate of uptake of oxygen over the surface pause. Assuming that the rate of uptake is directly proportional to the deficit (Equation 6), the rate of oxygen uptake at any one time during the surface pause can be calculated together with the body oxygen concentrations at the start and end of the pause by adhering to the precise conditions of surface to dive ratios defined by our results (Equation 4) and by assuming that we can reasonably allude to energy expenditure during the dive (Equation 3). In order to do this, an appropriate constant, k (see Equation 6), or appropriate range of constants that conform to the figures used for oxygen levels, has to be determined. Then, a particular known dive duration resulting in a defined oxygen use can be equated to the surface pause of defined length (via Equation 4), during which the oxygen must be taken up by the body according to Equation 6. Since the oxygen used during the dive must equal that repaid during the surface period, there is only one solution to this, which can be solved by iteration by setting pre-dive oxygen levels to a particular value and then seeing the extent to which this differs from that observed after mathematical treatment so that the initial value can be corrected accordingly. This process can be conducted over the range of dive durations.
For this we assume that the maximum amount of oxygen that can be contained
within a cormorant body can be calculated via the metabolic rate of
cormorants underwater (Schmidt et al.,
1995) multiplied by the maximum dive duration. In fact, we assume
that the maximum value observed by us (280 s)represents the 95% confidence
limit, so that the full oxygen capacity of the body is given by
0.00435x295
1.28 l. We note that this far exceeds that predicted
using standard values for body oxygen concentrations derived from
consideration of factors such as the amount of respiratory pigment (e.g.
Mill and Baldwin, 1983
;
Chappell et al., 1993
), the
oxygen binding capacity (e.g. Lenfant et
al., 1969
; Kooyman,
1989
), the saturation prior to dives
(Stephenson et al., 1989a
;
Croll et al., 1992
) and the
volume of air in the respiratory tract
(Lasiewski and Calder, 1971
;
Stephenson et al., 1989b
;
Wilson et al., 2003
), but
actually, for the model, precise figures are unimportant since we are only
interested in relative, rather than absolute, changes in pre- and post-dive
body oxygen levels. In order to access the rate of oxygen uptake at the
surface we assume that this is proportional to the difference between maximum
body oxygen levels (corresponding to saturation) and that observed at any one
time. Note that our treatise does not specifically attempt to define the upper
limit to oxygen reserves because the inconsistencies noted above from the
literature, perhaps due to marked inter-specific differences, make such a
procedure questionable. Rather, we stress that our presented derivations from
the model are useful in indicating trends rather than absolute values, and
that the robustness of our methodology can only be extended that far.
Use of our values necessitates that we use k = 0.0050.015, depending on the initial pre-dive oxygen body levels chosen, with the lower rate constants precluding the occurrence of long dives since oxygen levels in the body cannot be replaced in the time at the surface defined by Equation 4. For any particular value of k, the points on the oxygen saturation curve that correspond to the pre- and post-dive levels can be defined (Fig. 4A). Consideration of these values with respect to dive duration shows that increasing dive durations result in increasing pre-dive body oxygen levels and decreasing post-dive body oxygen levels (Fig. 4B) (note that differing values of k do not affect the overall form of the pre- and post-dive oxygen levels in the body, merely shift the curves up or down). This does not substantiate Kramer's hypothesis that diving animals should only take down enough oxygen to complete their dive because, by so doing, the minimal body oxygen levels on return to the surface lead to maximized uptake rates and reduced (non-foraging) time. Rather, it would appear that oxygen reserves are important even if the extent of these reserves held by the birds decreases with increasing dive duration (Fig. 4B). Why should this be?
|
Obviously, in an absolute sense, oxygen reserves over and above those
projected to be needed for the dive are beneficial since they could be used
for predator avoidance (Heithaus and Frid,
2003) or extensive prey handling where a particularly large prey
item was discovered. However, these reserves come at a price in terms of time
invested at the surface, since they must be paid for during every recovery
interval. Of particular importance is that, due to the logarithmic-type form
of the oxygen saturation curve over time, the reserves are not linearly
detrimental (in terms of time) but tend to be more onerous with increasing
pre-dive oxygen levels (as is necessary for long dives). This might explain
why the effective extra time invested in the reserves decreases with
increasing dive duration (Fig.
5 line labelled `reserves first'). In other words, birds
might benefit from having extra oxygen reserves during any particular dive,
but the time that has to be invested in maintaining these reserves is a
critical factor in determining their extent. In the dynamic state of the
cormorants diving, if the reserves themselves are ignored (assuming that they
are effectively never used), the real cost in terms of time for the birds
diving with and without reserves is given by the ratio of the recovery time
for a bird with, compared to without, reserves
(Fig. 5). Here it can be seen
that birds diving for short periods without reserves would be three times more
efficient in terms of time at the surface as birds diving with reserves
although, due to decreasing reserves with increasing depth
(Fig. 4B), they are only about
twice as efficient for extended dive durations
(Fig. 5). Ultimately, however,
the extent of the reserves and the decrease in efficiency that they imply will
be expected to be balanced out by the advantages accrued when they are used,
and in this respect the extent of the reserves might vary according to local
conditions, even on a day to day basis.
|
The model used here is simplistic in assuming, for instance, that energy
expenditure is constant during the dive and independent of depth (cf.
Wilson et al., 1992;
Lovvorn et al., 1999
;
Sato et al., 2002
) and,
although cormorants have little plumage air
(Wilson et al., 1992
), this is
unlikely to be completely true. Costa and Gales
(2000
) note, for example, that
New Zealand sea lions Phocarctos hookeri expend less energy during
deeper dives, presumably because they are able to spend more time gliding due
to reduced upthrust following decreases in body air volume due to hydrostatic
pressure. We also assume that the rate of oxygen uptake at the surface is
directly proportional to the oxygen deficit, when actually this will depend on
the extent of tachycardia and blood shunting at the surface (e.g. Butler,
1998
,
2000
). However, the trends are
well defined so that a substantial deviation from our assumptions will be
needed to invalidate them. The major element in our model that affects the
outcome is the form of the recovery duration/dive duration regression (cf.
Fig. 2). There is considerable
literature on dive recovery durations in a general sense (e.g.
Harcourt et al., 1994
;
Campagna et al., 1995
;
Boyd and Croxall, 1996
) but
relatively little in relation to dive performance. Nonetheless, in a paper
summarizing data from 19 cormorant species, Cooper
(1986
) considered the
relationship between inter-dive duration and dive duration to be linear
although depths were generally shallow and dive durations short. Both Croxall
et al. (1991
) and Wanless et
al. (1993
) note that long dive
durations result in overly long subsequent surface pauses. Kramer
(1988
) postulated that
recovery duration should increase as a power function of dive duration and
this is ultimately close to that observed by us (cf.
Fig. 2), although Wanless et
al. (1993
) found a better fit
using an exponential function. In fact, the difference is really only one of
degree and, given the scatter in data, it is hard to be equivocal about which
is really the best fit. Although accelerating surface pause durations with
respect to dive durations are often used to invoke anaerobic metabolism (e.g.
Ydenberg, 1988
;
Wanless et al., 1993
) this is
not necessarily the case since the oxygen saturation curve over time is not
linear (Butler and Jones,
1997
), so that as diving animals use an increasing proportion of
their overall oxygen stores, recovery durations are expected to accelerate
with respect to dive duration (Kramer,
1988
). Resolution of the extent of anaerobic metabolism (cf.
Carbone and Houston, 1996
;
Carbone et al., 1996
) will be
critical in any consideration of this type and, ultimately, the question can
only be definitively resolved by direct measurement of oxygen and/or lactate
levels in foraging birds. Perhaps recent advances in this field (e.g.
Parkes et al., 2002
;
Halsey et al., 2003
) indicate
that it may not be long before this happens.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bevan, R. M., Butler, P. J., Woakes, A. J. and Boyd, I. L. (2002). The energetics of gentoo penguins, Pygoscelis papua, during the breeding season. Funct. Ecol. 16,175 -190.[CrossRef]
Boyd, I. L. and Croxall, J. P. (1996). Dive durations in pinnipeds and seabirds. Can. J. Zool. 74,1696 -1705.
Butler, P. J. (1998). The exercise response and the `classical' diving response during natural submersion in birds and mammals. Can. J. Zool. 66, 29-39.
Butler, P. J. (2000). Energy cost of surface swimming and diving of birds. Physiol. Biochem. Zool. 73,699 -705.[CrossRef][Medline]
Butler, P. J. (in press). Metabolic regulation in diving birds and mammals. Resp. Physiol.
Butler, P. J. and Jones, D. R. (1997). The
physiology of diving of birds and mammals. Physiol.
Rev. 77,837
-899.
Butler, P. J. and Woakes, A. J. (1984). Heart rate and aerobic metabolism in Humboldt penguins Spheniscus humboldti during voluntary dives. J. Exp. Biol. 108,419 -428.[Abstract]
Campagna, C., Le Boeuf, B. J., Blackwell, S. B., Crocker, D. E. and Quintana, F. (1995). Diving behaviour and foraging location of female southern elephant seals from Patagonia. J. Zool. Lond. 236,55 -71.
Carbone, C. and Houston, A. I. (1996). The optimum allocation of time over the dive cycle: an approach based on aerobic and anaerobic respiration. Anim. Behav. 51,1247 -1255.[CrossRef]
Carbone, C., De Leeuw, J. and Houston, I. (1996). Adjustments in the diving time budgets of tufted duck and pochard: is there evidence for a mix of metabolic pathways. Anim. Behav. 51,1257 -1268.[CrossRef]
Chappell, M. A., Shoemaker, V. H., Janes, D. N., Bucher, T. L. and Maloney, S. K. (1993). Diving behavior during foraging in breeding Adélie penguins. Ecology 74,1204 -1215.
Cooper, J. (1986). Diving patterns of cormorants (Phalacrocoracidae). Ibis 128,562 -569.
Costa, D. P. and Gales, N. J. (2000). Foraging
energetics and diving behaviour of lactating New Zealand sea lions
Phoarctos hookeri. J. Exp. Biol.
203,3655
-3665.
Costa, D. P. and Gales, N. J. (2003). Energetics of a benthic diver: Seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecol. Monogr. 73, 27-43.
Costa, D, P., Gales, N. P. and Goebel, M. E. (2001). Aerobic dive limit: How often does it occur in nature? Comp. Biochem. Physiol. 129A,771 -783.
Croll, D. A., Gaston, A. J., Burger, A. E. and Konnoff, D. (1992). Foraging behavior and physiological adaptations for diving in thick-billed murres. Ecology 73,344 -356.
Croxall, J. P., Naito, Y., Kato, A., Rothery, P. and Briggs, D. R. (1991). Diving patterns and performance in the Antarctic blue-eyed shag Phalacrocorax atriceps. J. Zool. Lond. 225,177 -199.
Culik, B. M., Pütz, K., Wilson, R. P., Allers, D., Lage,
J., Bost, C.-A. and Le Maho, Y. (1996). Diving energetics in
king penguins (Aptenodytes patagonicus). J. Exp.
Biol. 199,973
-983.
Dewar, J. M. (1924). The Bird as a Diver. Witherby, London.
Grémillet, D., Wilson, R. P., Storch, S. and Gary, Y. (1999). Three-dimensional space utilization by a marine predator. Mar. Ecol. Progr. Ser. 183,263 -273.
Halsey, L., Butler, P. J. and Woakes, A. J. (2003). Testing optimal foraging model for air-breathing divers. Anim. Behav. 65,641 -653.[CrossRef]
Handrich, Y., Bevan, R. M., Charrassin, J. B., Butler, P. J., Pütz, K., Woakes, A. J., Lage, J. and LeMaho, Y. (1997). Hypothermia in foraging king penguins. Nature 388, 64-67.[CrossRef]
Harcourt, R. G., Schulman, A. M., Davis, L. S. and Trillmich, F. (1994). Summer foraging by lactating female New Zealand fur seals (Arctocephalus forstei) off Otago Peninsula, New Zealand. Can. J. Zool. 73,678 -690.
Heithaus, M. R. and Frid, A. (2003). Optimal diving under the risk of predation. J. Theoret. Biol. 223, 79-92.[CrossRef][Medline]
Herrera, G. O. (1997). Dieta reproductiva de la gaviota de Olrog Larus atlanticus en la provincia del Chubut. Undergraduate thesis, Universidad Nacional de la Patagonia San Juan Bosco. Puerto Madryn, Argentina.
Horning, M. (1992). Die Ontogenese des Tauchverhaltens beim Galapagos-Seebären Arctocephalus galapagonensis (Heller 1904). PhD thesis, University of Bielefeld, Germany.
Kato, A., Croxall, J. P., Watanuki, Y. and Naito, Y. (1992). Diving patterns and performance in male and female blue-eyed cormorants Phalacrocorax atriceps at South Georgia. Mar. Orn. 19,117 -129.
Kooyman, G. L. (1989). Diverse Divers. Berlin, Springer-Verlag.
Kramer, D. L. (1988). The behavioral ecology of air breathing by aquatic animals. Can. J. Zool. 66, 89-94.
Lasiewski, R. C. and Calder, W. A. (1971). A preliminary allometric analysis of repiratory variables in resting birds. Resp. Physiol. 11,152 -166.[CrossRef][Medline]
Lenfant, C., Kooyman, G. L., Elsner, R. and Drabek, C. M.
(1969). Respiratory function of the blood of the Adélie
penguin (Pygoscelis adeliae). Am. J. Physiol.
216,1598
-1600.
Lovvorn, J. R., Croll, D. A. and Liggins, G. A.
(1999). Mechanical versus physiological determinants of
swimming speeds in diving Brünnich's guillemots. J. Exp.
Biol. 202,1741
-1752.
Mill, G. K. and Baldwin, J. (1983). Biochemical correlates of swimming and diving behavior in the Little penguin, Eudptula minor. Physiol. Zool. 56,242 -254.
Parkes, R., Halsey, L. G., Woakes, A. J., Holder, R. L. and Butler, P. J. (2002). Oxygen uptake during post dive recovery in a diving bird, Aythya fuligula: implications for optimal foraging models. J. Exp. Biol. 205,3945 -3954.[Medline]
Ponganis, P. J., Van Dam, R. P., Levensen, D. H., Knower, T., Ponganis, K. V. and Marshall, G. (2003). Regional heterothermy and conservation of core temperature in emperor penguins diving under the ice. Comp. Biochem. Physiol. 135A,477 -487.
Punta, G., Saravia, J. and Yorio, P. (1993). The diet and foraging behavior of two Patagonian cormorants. Mar. Ornithol. 21,27 -36.
Sapoznikow, A. and Quintana, F. (2003). Foraging behavior and feeding locations of imperial cormorants and rock shags breeding in sympatry in Patagonia, Argentina. Waterbirds 26,184 -191.
Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y.,
Charrassin, J.-B., Bost, C.-A., Handrich, Y. and Le Maho, Y.
(2002). Buoyancy and maximal diving depth in penguins: do they
control inhaling air volume. J. Exp. Biol.
205,1189
-1197.
Sato, K., Mitani, Y., Cameron, M. F., Siniff, D. B. and Naito,
Y. (2003). Factors affecting stroking patterns and body angle
in diving Weddell seals under natural conditions. J. Exp.
Biol. 206,1461
-1470.
Schmidt-Nielsen, K. (1993). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.
Schmidt, D., Grémillet, D. and Culik, B. (1995). Energetics of underwater swimming in the Great Cormorant (Phalacrocorax carbo sinensis). Mar. Biol. 123,875 -881.
Stephenson, R., Turner, D. L. and Butler, P. J. (1989a). The relationship between diving activity and oxygen storage capacity in the tufted duck (Aythia fuligula). J. Exp. Biol. 141,265 -275.
Stephenson, R., Lovvorn, J. R., Heieis, M. R. A., Jones, D. R. and Blake, R. W. (1989b). A hydromechanical estimate of the power requirements of diving and surface swimming in the lesser scaup (Aythya affinis). J. Exp. Biol. 147,507 -519.
Taylor, S. S., Boness, D. J. and Majluf, P. (2001). Foraging trip duration increases for Humboldt penguins tagged with recording devices. J. Avian Biol. 32,369 -372.[CrossRef]
Wanless, S., Harris, M. P. and Morris, J. A. (1988). The effect of radio transmitters on the behavior of common murres and razorbills during chick rearing. Condor 90,816 -823.
Wanless, S. and Harris, M. (1991). Diving patterns of full-grown and juvenile rock shags. Condor 93, 44-48.
Wanless, S., Corfield, T., Harris, M. P., Buckland, S. T. and Morris, J. A. (1993). Diving behaviour of the shag Phalacrocorax aristotelis (Aves: Pelecaniformes) in relation to water depth and prey size. J. Zool. Lond. 123, 11-25.
Williams, T. D., Davis, R. W., Fuiman, L. A. M., Francis, J., Le
Boeuf, B. J., Horning, M., Calabokidis, J. and Croll, D. A.
(2000). Sink or swim: strategies for cost-efficient diving by
marine mammals. Science
288,133
-136.
Wilson, R. P., Hustler, K., Ryan, P. G., Noeldeke, C. and Burger, A. E. (1992). Diving birds in cold water: do Archemedes and Boyle determine energy costs. Am. Nat. 140,179 -200.[CrossRef]
Wilson, R. P. and Wilson, M.-P. (1988). Foraging behaviour in four sympatric cormorants. J. Anim. Ecol. 57,943 -955.
Wilson, R. P. (2003). Penguins predict performance. Mar. Ecol. Progr. Ser. 249,305 -310.
Wilson, R. P., Simeone, A., Luna-Jorquera, G., Steinfurth, A.,
Jackson, S. and Fahlman, A. (2003). Patterns of respiration
in diving penguins: Is the last gasp based on an inspired tactic?
J. Exp. Biol. 206,1751
-1763.
Woakes, A. J. and Butler, P. J. (1983). Swimming and diving in tufted ducks, Aythya fuligula, with particular reference to heart rate and gas exchange. J. Exp. Biol. 107,311 -329.
Ydenberg, R. C. (1988). Foraging by diving birds. Proc. Int. Orn. Congr. 19,1831 -1842.
Yorio, P., Frere, E., Gandini, P. and Harris, G. (1998). Atlas de la distribución reproductiva y abundancia de aves marinas del litoral patagónico Argentino. Plan de Manejo Integrado de la Zona Costera Patagónica. Patagonia, Argentina: Fundación Patagonia Natural and Wildlife Conservation Society.