High feeding costs limit dive time in the largest whales
Institute of Marine Sciences, Center for Ocean Health, 100 Shaffer
Road, University of California, Santa Cruz, CA 95060, USA
* Present address: Division of Education, California Academy of Sciences, Golden
Gate Park, San Francisco, CA 94118, USA
(e-mail: aacevedo{at}calacademy.org
Accepted 28 March 2002
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: foraging, diving, feeding costs, blue whale, Balaenoptera musculus, fin whale, Balaenoptera physalus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Oxygen is a limiting factor in air-breathing vertebrates, and some marine
mammals, including the blue whale, glide during a dive, a behavior that
appears to reduce oxygen consumption
(Williams et al., 2000;
Davis et al., 2001
;
Nowacek et al., 2001
). The
amount of time that a diver is able to remain under water relying solely on
its oxygen stores is called the theoretical aerobic dive limit (TADL) and is
calculated by estimating the oxygen stores and diving metabolic rate of a
species, usually on the basis of body mass
(Kooyman, 1989
;
Boyd, 1997
). The TADLs of blue
and fin whales are 31.2 and 28.6 min, respectively, yet their foraging dives
average only 7.8 and 6.3 min (Croll et al.,
2001
): the largest predators on earth have the shortest dive
durations relative to their TADL.
Three hypotheses may explain the discrepancy between measured and predicted
dive durations in blue whales and fin whales. (i) Prey are found in shallow
waters and thus dive durations are short. This is because in most
circumstances dive duration is positively correlated with dive depth
(Kramer, 1988;
Houston and Carbone, 1992
).
However, blue whales and fin whales generally forage on prey aggregations at
depths greater than 100 m (Panigada et
al., 1999
; Croll et al.,
2001
). (ii) Prey disperse quickly, forcing whales to feed
elsewhere (Croll et al., 2001
).
However, euphausiids maintain dense aggregations for several days, even when
whales are foraging in the area (Simrad
and Laroie, 1999
). (iii) The rate of energy expenditure is greater
amongst foraging blue whales and fin whales than for other divers. This could
result from lunge-feeding, which may be an energetically expensive behavior
that consumes much oxygen and limits blue whales and fin whales to dives that
are of shorter duration than their TADL
(Croll et al., 2001
).
Blue and fin whales feed by lunging forward to engulf water that contains
prey, such as small (<4 cm) euphausiid crustaceans
(Kawamura, 1980). Prey items
are filtered through keratinized plates called baleen. When lunging, the mouth
and throat engulf a mass of water representing nearly 70 % of the whale's body
mass per lunge (Pivorunas,
1979
) (see Fig. 1).
The fast forward swimming motion of the whale and the displacement of the
tongue, which invaginates to form a hollow structure, force water and prey
into the mouth (Lambertsen,
1983
). When euphausiids have been engulfed, the lower jaw is
closed and water is forced through the baleen
(Pivorunas, 1979
). When
feeding at the surface, whales breathe immediately after each lunge; however,
when feeding at depth, they lunge up to eight times before coming to the
surface to breathe (Tershy et al.,
1993
; Croll et al.,
2001
). Lunging has been termed `the largest biomechanical action
in the animal kingdom' (Brodie,
1983
). However, the cost of lunge-feeding has not been
measured.
|
We estimated the cost of lunge-feeding by attaching time/depth recorders
(TDRs) to seven blue whales and eight fin whales and comparing the observed
dive behavior with predictions made by optimality models of diving
(Houston and Carbone, 1992).
Animals increasingly deplete their oxygen stores as the cost of a dive
increases and therefore need more time to replenish oxygen stores at the
surface after the dive (Kooyman et al.,
1980
). Costs are measured in oxygen utilized; however, we
indirectly estimated the costs of lunge-feeding by measuring the time needed
to recover at the surface after a dive. Specifically, we examined the
prediction that the recovery time of blue whales and fin whales after a dive,
measured to normalize for dive duration as the rate of increase in time spent
at the surface as dive duration increased, would be positively related to the
number of lunges per dive. If this were true, a lunging-costly model should
provide the best fit to the observed dive durations.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Once the tag had been released from the whale, we localized it with the directional VHF system. Dive data were analyzed using software provided by the TDR manufacturer (Dive Analysis, Wildlife Computers). We considered individual whales to be independent observations and calculated the median values of dive parameters for each. We defined a dive as any period under water at depths of 20 m or greater and a surface interval as the post-dive duration at depths of 2 m or less. The software Dive Analysis automatically calculated mean ascent and descent rates of dive.
In a profile of time versus depth, an upward movement of 8 m or
more followed by a downward movement characterized certain dives.
(Fig. 1A). Whales move
significantly faster during the ascent portion than during the descent portion
of such excursions, each of which lasts less than 1 min
(Croll et al., 2001; present
study). In addition, the depth of such vertical excursions corresponds with
regions of densely aggregated euphausiids
(Croll et al., 1998
). Thus,
following Croll et al. (2001
),
each such excursion was counted as a foraging lunge; whales were considered to
be foraging if the profile of time versus depth showed one or more
lunges during the dive (Fig.
1A) and non-foraging if no lunges were recorded. Because
Balaenoptera whales have been observed lunging horizontally at the
surface (Tershy et al., 1993
),
it is possible that such horizontal lunges also occur at depth. However, in a
profile of time versus depth, it would not be possible to discern
whether a whale lunged horizontally. Thus, we only analyzed non-foraging dives
in which the whale dived directly to depth and returned to the surface without
spending time at depth (Croll et al.,
2001
).
Recovery time at the surface
To assess whether whales incurred a cost by lunge-feeding, we employed the
rate of increase of the time spent recovering at the surface as dive duration
increases. This rate was defined as the slope b of the fitted lines
between dive duration and time at the surface after the dive. The higher the
value of the slope, the longer the time that the whale spent recovering at the
surface as dive duration increased. In this manner, we discarded the
confounding effect of dive duration since longer dives require more time at
the surface (Kooyman, 1989).
We divided the slope of foraging dives by the slope of non-foraging dives and
thus defined relative rates of increase of the time spent recovering at the
surface. We tested with an order of heterogeneity test the prediction that as
the number of lunges per dive increased these relative rates would also
increase. An order of heterogeneity test allows comparison of three or more
populations against simply ordered alternative hypotheses
(Rice and Gaines, 1994
). It is
a directional test that allowed us to detect differences in the relative rate
of the time needed to recover among distinct lunge classes from expected
lowest (zero lunges) to expected highest (four lunges).
Optimality models
We compared the observed values of dive duration with the values predicted
by optimality models assuming either a metabolic cost of feeding or no cost of
feeding (Houston and Carbone,
1992), which we termed the lunging-costly and the no-cost models,
respectively. The optimality models employ foraging time at different water
depths as currency. Thus, we added predicted foraging time and observed travel
time to obtain theoretical dive durations, which were compared with the
observed dive durations obtained from TDR data. Travel time was the time that
a whale spent moving to and from the surface and was calculated by subtracting
the foraging time (defined as the time spent at depths greater than 75% of the
maximum depth of dive) from the dive duration. Two equations maximizing
foraging time in divers allowed us to obtain predicted foraging time for both
the no-cost and the lunging-costly models
(Houston and Carbone, 1992
):
![]() | (1) |
![]() | (2) |
Because these are optimality models, the subscript `i' indicates that
different values of time spent recovering at the surface (s)
correspond to different travel times (). To obtain the predicted foraging
time for the no-cost model, we defined m2 as 1, i.e. the
cost of foraging equals the cost of traveling to and from the prey patch
(Houston and Carbone, 1992
).
To obtain the predicted foraging times for the lunging-costly model, we solved
for m2 to obtain the cost of foraging relative to the cost
of traveling to and from the prey patch. We obtained a common cost for
foraging dives by randomly selecting only one foraging dive from each
individual.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
One-lunge dives had a similar relative rate of increase of the time spent recovering at the surface to non-foraging dives (Fig. 3). Thus, they were different from the rest of the foraging dives. We hypothesize that this is because whales exerted the least effort per lunge when lunging once; because of this, we continued the analysis only for dives with two or more lunges per dive. Lunge velocity and distance increased in blue whales from 1.5±0.90 m s-1 and 24.0±11.37 m (N=6), respectively, in dives with one lunge to 2.6±0.95 m s-1 and 34.7±8.07 m (N=6), respectively, in dives with two or more lunges (means ± S.D.; paired t-test; distance, t5=-3.08, P=0.027; velocity, t5=-4.47, P=0.007). Similarly, lunge velocity and distance increased in fin whales from 1.5±0.37 m s-1 and 17.3±6.57 m (N=8) to 1.8±0.31 m s-1 and 23.3±2.83 m (N=8) (means ± S.D.; paired t-test, distance, t7=-2.39, P=0.048; velocity, t7=-2.61, P=0.035).
The optimality models provided a good fit to the observed foraging time for dives with two or more lunges (Fig. 4). The relative cost of foraging was 3.15 for blue whales and 3.60 for fin whales (blue whales, 95% CI 2.58-3.72, r2obs-pred=0.0624; fin whales, 95% CI 2.35-4.85, r2obs-pred=0.615). In all cases, the observed foraging time was far shorter than that predicted by the no-cost model (Fig. 4). Whales foraged at depths greater than 100 m: maximum depth of dive averaged 132.0±48.87 m in blue whales and 102.0±40.77 m in fin whales during two-lunge dives (N=4 blue whales, N=8 fin whales), 157.3±33.27 m in blue whales and 113.3±36.00 m in fin whales during three-lunge dives (N=6 blue whales, N=8 fin whales) and 150.3±52.09 m in blue whales and 109.8±34.62 m in fin whales during four-lunge dives (means ± S.D.) (N=7 blue whales, N=5 fin whales).
|
Absolute differences between predicted and observed dive durations were smaller in the lunging-costly model than in the no-cost model for dives with two or more lunges (paired t-test; blue whales, two lunges, t3=-9.94, P=0.002; three lunges, t5=-15.55, P<0.001; four lunges, t610.91, P<0.001; fin whales, two lunges, t7=-15.03, P<0.001; three lunges, t7=-10.81, P<0.001; four lunges, t4=-3.68, P0.021) (Fig. 5).
|
Whales increased their vertical speed at the beginning of each lunge, suggesting that the costs of lunge-feeding were related to the effort needed to accelerate their large body. The vertical speed of blue whales at the beginning of a lunge averaged 1.3±0.39 m s-1 and at the mid-point of the ascent it had increased to 2.9±0.85 m s-1, up to a maximum of 4.0 m s-1 (means ± S.D., paired t-test, t6=5.51, P=0.002). The vertical speed of fin whales at the beginning of a lunge averaged 2.3±1.66 m s-1 and at the mid-point of the ascent it had increased to 5.0±3.16 m s-1, up to a maximum of 10.7 m s-1 (means ± S.D., paired t-test, t7=-4.078, P=0.005). The ascent phase of lunges averaged 34.2±13.49 s and 32.9±6.74 s in blue whales and fin whales, respectively (means ± S.D., N=7 blue whales, N=8 fin whales for all values in paragraph).
Foraging in both whale species occurred in areas smaller than 1 km2 for extended periods, suggesting that the prey did not disperse. The distance between foraging dives averaged 525.4±144.98 m and 895.7±198.09 m in blue whales and fin whales, respectively (means ± S.D., N=5 blue whales, N=5 fin whales). Foraging bouts consisted of 9.1±8.90 dives and 10.9±10.15 dives in blue whales and fin whales, respectively (means ± S.D., N=7 blue whales, N=8 fin whales).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Non-foraging dives of blue whales and fin whales were shorter than foraging
dives. However, this is an expected result since, when not foraging, whales
are merely traveling from one prey patch to another, presumably not attempting
to maximize the time spent under water, and performing shallow dives between
20 and 30 m in depth (Croll et al.,
2001). Even if a diver is attempting to maximize time spent
foraging, the rate of energetic gain or energetic efficiency optimality models
predict a positive relationship between dive duration and dive depth
(Kramer, 1988
;
Houston and Carbone, 1992
).
This prediction is supported by empirical evidence (for a review, see
Schreer and Kovacs, 1997
). The
only exception to this positive relationship between dive duration and dive
depth occurs when the cost of foraging is smaller than the cost of travel
(Houston and Carbone, 1992
),
which was clearly not the case for blue whales and fin whales.
The horizontal distances that blue whales and fin whales covered while
foraging are well within the size of euphausiid aggregations (approximately
5000-10 000 m in one dimension) upon which the whales typically feed
(Croll et al., 1998;
Simrad and Laroie, 1999
). This
result, and the observation that consecutive foraging bouts consisted of more
than one dive, indicates that prey did not disperse and that whales were
foraging on the same aggregation of euphasiids.
In view of the high cost of lunge-feeding, large whales that do not employ
this mechanism should dive for longer than blue whales or fin whales. This
prediction is supported by data from bowhead whales (Balaena
mysticetus). Adult bowhead whales average 48 250 kg in mass, 48 % less
than blue whales (Croll et al.,
2001), yet they spend more time foraging under water (1.5-2 times)
and less time recovering from a dive (0.5 times) than blue whales diving to
comparable depths (Dorsey et al.,
1989
; Krutzikowsky and Mate,
2000
). Bowhead whales are able to reduce their feeding costs by
maintaining a constant depth and a consistent stroke rate and by
burst-and-glide swimming (Nowacek et al.,
2001
). In addition, bowhead whales are slow swimmers, and a close
relative, the right whale (Balaena glacialis), averages only 0.7 m
s-1 when feeding at depth
(Goodyear, 1995
). In contrast,
during each lunge, blue whales and fin whales accelerate their large bodies to
reach remarkable speeds, frequently changing depths and moving against the
force of gravity. We hypothesize that the feeding costs of bowhead whales are
low because of their energy-saving behaviors and because they move more slowly
than blue whales and fin whales.
High feeding costs have been shown to maintain populations of endangered
species at low levels (Gorman et al.,
1998). Blue whales are a critically endangered species despite a
decade of moratorium on commercial whaling
(Clapham et al., 1999
). Factors
involved in the slow recovery of blue whales may include their small
population size after whaling was banned
(Clapham et al., 1999
), their
dependence on euphausiids as food
(Kawamura, 1980
), the
long-term negative trend in the abundance of euphausiids in relation to
changes in global climate (Loeb et al.,
1997
; Siegel et al.,
1998
) and the high costs of lunge-feeding.
Lunge-feeding is an impressive biomechanical event that comes at a high
energetic cost. At the physiological level, it limits foraging time and dive
duration despite the fact that blue whales, and presumably fin whales, glide
during a dive, thus saving energy
(Williams et al., 2000). At
the ecological level, it confines blue whales and fin whales to areas with
dense prey aggregations and may make them particularly vulnerable to
perturbations in prey abundance. Paradoxically, the behavior that allows these
whales to exploit the patchy and ephemeral resources of the ocean limits them
to short foraging dives in productive regions such as submarine canyons or the
Southern Boundary of the Antarctic Circumpolar Current
(Croll et al., 1998
;
Tynan, 1998
).
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Berta, A. and Sumich, J. L. (1999). Marine Mammals. Evolutionary Biology. San Diego: Academic Press.
Boyd, I. L. (1997). The behavioural and physiological ecology of diving. Trends Ecol. Evol. 12,213 -217.
Brodie, P. (1983). Noise generated by the jaw actions of feeding fin whales. Can. J. Zool. 71,2546 -2550.
Clapham, P. J., Young, S. B. and Brownell, R. L., Jr (1999). Baleen whales: conservation issues and the status of the most endangered populations. Mammal. Rev. 29, 35-60.
Croll, D. A., Acevedo-Gutiérrez, A., Tershy, B. and Urbán-Ramírez, J. (2001). The diving behavior of blue and fin whales: is dive duration shorter than expected based on oxygen stores? Comp. Biochem. Physiol. 129A,797 -809.
Croll, D. A., Tershy, B. R., Hewitt, R. P., Demer, D. A., Fiedler, P. C., Smith, S. E., Armstrong, W., Popp, J. M., Kiekhefer, T., Lopez, V. R., Urbán, J. and Gendron, D. (1998). An integrated approach to the foraging ecology of marine birds and mammals. Deep-Sea Res. II 45,1353 -1371.
Davis, R. W., Fuiman, L. A., Williams, T. M. and Le Boeuf, B. J. (2001). Three-dimensional movements and swimming activity of a northern elephant seal. Comp. Biochem. Physiol. 129A,759 -770.
Dorsey, E. M., Richardson, W. J. and Würsig, B. (1989). Factors affecting surfacing, respiration and dive behaviour of bowhead whales, Balaena mysticetus, summering in the Beaufort Sea. Can. J. Zool. 67,1801 -1815.
Goodyear, J. D. (1995). Dive behavior and the question of food limitation in right whales. In Abstracts of the Eleventh Biennial Conference on the Biology of Marine Mammals, Orlando, FL, 14-18 December 1995 (ed. B. S. Stewart), p.148 . Lawrence: The Society for Marine Mammalogy.
Gorman, M. L., Mills, M. G., Raath, J. P. and Speakman, J. R. (1998). High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391,479 -481.
Hochachka, P. W. and Somero, G. N. (1984). Biochemical Adaptation. Princeton: Princeton University Press.
Houston, A. I. and Carbone, C. (1992). The optimal allocation of time during the diving cycle. Behav. Ecol. 3,255 -265.
Kawamura, A. (1980). A review of food of balaenopterid whales. Sci. Rep. Whales Res. Inst. 32,155 -197.
Kooyman, G. L. (1989). Diverse Divers: Physiology and Behavior. Berlin: Springer-Verlag.
Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. A. and Sinnett, E. E. (1980). Aerobic and anaerobic metabolism during diving in Weddell seals: Evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. 138,335 -346.
Kramer, D. L. (1988). The behavioural ecology of air breathing by aquatic animals. Can. J. Zool. 66, 89-94.
Krutzikowsky, G. K. and Mate, B. R. (2000). Dive and surface characteristics of bowhead whales (Balaena mysticetus) in the Beaufort and Chukchi seas. Can. J. Zool. 78,1182 -1198.
Lambertsen, R. H. (1983). Internal mechanism of rorqual feeding. J. Mammal. 64, 76-88.
Loeb, V., Siegel, V., Holm-Hansen, O., Hewitt, R., Fraser, W., Trivelpiece, W. and Trivelpiece, S. (1997). Effects of sea-ice extent and salp or krill dominance on the Antarctic food web. Nature 387,897 -900.
Nishiwaki, M. (1950). On the body weights of whales. Sci. Rep. Whales Res. Inst. 4, 184-209.
Nowacek, D. P., Johnson, M. P., Tyack, P. L., Shorter, K. A., McLellan, W. A. and Pabst, D. A. (2001). Buoyant balaenids: the ups and downs of buoyancy in right whales. Proc. R. Soc. Lond. B 268,1811 -1816.[Medline]
Panigada, S., Zanardelli, M., Canese, S. and Jahoda, M. (1999). How deep can baleen whales dive? Mar. Ecol. Prog. Ser. 187,309 -311.
Pivorunas, A. (1979). The feeding mechanisms of baleen whales. Am. Sci. 67,432 -440.
Rice, W. R. and Gaines, S. D. (1994). Extending nondirectional heterogeneity tests to evaluate simply ordered alternative hypotheses. Proc. Natl. Acad. Sci. USA 91,225 -226.[Abstract]
Schreer, J. F. and Kovacs, K. M. (1997). Allometry of diving capacity in air-breathing vertebrates. Can. J. Zool. 75,339 -358.
Siegel, V., Loeb, V. and Groger, J. (1998). Krill Euphasia superba density, proportional and absolute recruitment and biomass in the Elephant island region (Antarctica Peninsula) during the period 1977-1997. Polar Biol. 16,393 -398.
Simrad, Y. and Laroie, D. (1999). The rich krill aggregation of the Saguenay St. Lawrence Marine Park: hydroacoustic and geostatistical biomass estimates, structure, variability and significance for whales. Can. J. Fish. Aquat. Sci. 56,1182 -1197.
Tershy, B., Acevedo-Gutiérrez, A., Breese, D. and Strong, C. (1993). Diet and feeding behavior of fin and Bryde's whales in the Central Gulf of California, México. Rev. Invest. Cient. (No. Esp. SOMEMMA) 1, 31-37.
Tynan, C. T. (1998). Ecological importance of the southern boundary of the Antarctic Circumpolar Current. Nature 392,708 -710.
Williams, T. M., Davis, R. W., Fuiman, L. A., Francis, J., Le
Boeuf, B., Horning, M., Calambokidis, J. and Croll, D. A.
(2000). Sink or swim: strategies for cost-efficient diving by
marine mammals. Science
288,133
-136.