Antennae on transmitters on penguins: balancing energy budgets on the high wire
1 Institut für Meereskunde, Düsternbrooker Weg 20, D-24105 Kiel,
Germany
2 Forschungs- und Technologiezentrum Westküste, Hafentörn, D-25761
Büsum, Germany
3 New England Aquarium, Central Wharf, Boston, MA 02110, USA
* Author for correspondence (e-mail: rwilson{at}ifm-geomar.de)
Accepted 30 April 2004
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Summary |
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Key words: penguin, Spheniscus magellanicus, external antennae, drag, energy expenditure, foraging efficiency
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Introduction |
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The effect of inappropriately shaped animal-carried systems is particularly
important in marine animals (e.g. Bannasch
et al., 1994; Culik et al.,
1994a
,b
;
Watson and Granger, 1998
)
because the drag caused by moving non-streamlined units through the dense
medium, i.e. water, leads to substantial increases in energy expenditure.
Following streamlining suggestions by Bannasch et al.
(1994
), many researchers
working with telemetric devices on diving marine endotherms shape their units
accordingly but have, to date, essentially ignored the potentially detrimental
effect that antennae might have.
In this work we assess the drag incurred by marine endotherms carrying telemetric units with antennae as a function of the size and properties of the antennae. The results of this work are then put into context by examining the behaviour of free-living Magellanic penguins and, using a simple energetics model, by considering the extent to which this behaviour might be altered in birds having to carry antennae on telemeters. Finally, we consider how antennae might be constructed so as to minimize their deleterious effects on their carrier animals.
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Materials and methods |
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The penguin model was constructed from fibreglass and derived from a cast
of a dead Spheniscus penguin [original body mass 3.7 kg; mean body
mass of Magellanic penguins = 4.0 kg
(Williams, 1995); body
dimensions without wings and with head retracted in the swimming position 57
cmx14 cmx12 cm]. Such a static, hard-bodied model cannot properly
emulate the water flow characteristics over a real, soft penguin body,
particularly since features such as feather properties may be responsible for
substantial drag reduction (e.g. see
Carpenter et al., 2000
;
Gad-el-Hak, 2002
). We thus
consider that the proportional drag values obtained by this approach will tend
to be more than those actually incurred on a real penguin. However, in order
to maintain water flow over the model as accurately as possible, an original
penguin skull, complete with beak, was incorporated in the head, this being
covered, as appropriate, with fibreglass. The body was supported by a
stainless steel rod contiguous with the ends of the flippers and running away
from the longitudinal axis of the body at 90°. This rod was clamped in
plastic vanes running parallel to the body longitudinal axis so that the
penguin could be held firmly in position underwater within a swim canal. These
vanes were 1.3 cm thick and spaced 90 cm apart so that they minimally
influenced water flow over the model penguin. The canal had dimensions of 20
mx1 mx1 m and was filled with freshwater at ca. 20°C.
The plastic vanes were connected to a vehicle located on top of the canal on
rails running the length of the system so that the penguin model could be
driven through the water from one end to the other at a speed regulated by a
computer. The speed was programmed so that the penguin model experienced a
gentle acceleration phase over the first 3 m before the final speed was
reached, which was maintained over most of the length of the canal until
shortly before the end when the vehicle decelerated to zero over ca. 2 m.
Speed values selected were from 0 to 2 m s1 in 0.25 m
s1 increments and were accurate to within 3%.
The unit constructed to sense the drag experienced by antennae (Fig. 1) consisted of a quarter disc (radius 15 mmx10 mm thick) pivoted about what would be the complete disc's centre. A steel rod with a screw thread was attached to the quarter disc in line with one of the edges of the radii so that it projected directly away from the pivot. A cork bung was screwed onto this rod and could be moved up and down the length of the rod so that the bungpivot distance could be exactly defined. The cork bung rested against the active membrane of a medium-separated pressure transducer (measurement range 06x105 Pa; Sensortechnik, Munich, Germany), located between rails to allow the transducer to be moved to any specified distance from the pivot directly in line with the steel rod, and orientated to face the bung directly. Three screw holes were turned into the quarter disc on the outside edge of what would have been the circumference of the full disc so that they were at angles of 90, 67.5 and 45° to the steel rod. All antennae to be tested conformed in size roughly to antennae used by PTT and VHF transmitters provided by a number of companies. These antennae were attached at their base to a screw, which fitted any one of the screw holes in the quarter disc outside edge so that the angle between antenna and steel rod could be correspondingly defined precisely as either 90, 67.5 or 45°. The unit was placed on the penguin model so that base of the attached antenna was exactly in line with the contours of the penguin's body, the quarter disc, pivot, bung and associated transducer being located within the body and away from the main current flow over the penguin. With an antenna screwed in place, when the penguin model moved forward through the water, drag acting on the antenna from the front exerted a force which acted, via the pivot, on the bung located on the steel rod causing it to exert pressure on the transducer.
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The transducer readings were stored in a two-channel logger (IRDA series, Driesen and Kern GmbH, Bad Bramsted, Germany), which recorded pressure and temperature continuously at 2 s intervals with 16-bit resolution in a 512 kbyte memory. The temperature sensor was used to compensate for temperature-dependent variability in pressure reading over and above that already corrected by the transducer manufacturers. Independent tests on the quality of the pressure transducer readings showed that it was good to better than 100 Pa. The logger was powered by a 3.6 V battery and the unit was started and data were accessed by an infra-red interface via computer.
Tests were conducted with the penguin, complete with pressure-sensitive unit, moving along the canal at defined speeds with no antenna (as the control) and with antennae of diameters of 1, 2, 3 and 4 mm and lengths of 100, 150 and 200 mm. We used two basic types: (i) essentially rigid antennae, although all antennae of this type did bend to some degree, and (ii) highly flexible (wound) antennae. These were considerably more flexible than PTT-type antennae usually used to our knowledge, but were selected to demonstrate the extent to which flexible antennae might be useful in reducing drag.
The pressure measured by the transducer during the various runs was calibrated for the torque incurred due to drag by mounting the unit in air so that the steel screw to which the bung was attached was exactly vertical and an antenna (length 200 mm, diameter 3 mm) fitted so that it was perpendicular to the screw, parallel to the ground and above the steel rod. Weights were hung on the antenna at defined positions and the pressure registered by the transducer, derived from the bung, was recorded by the logger. Calculations enabled us to derive the relationship between recorded pressure and torque.
Field studies
Field work was conducted between September 1996 and December 1997 on
Magellanic penguins Spheniscus magellanicus Forster at Punta Norte
colony (42°05'S, 63°52'W, Peninsula Valdes, Chubut,
Argentina). Breeding birds were equipped with data loggers (DK 600 series,
Driesen and Kern GmbH, Bad Bramstedt, Germany), fitted using tape
(Wilson et al., 1997) to the
lower back, as suggested by Bannasch et al.
(1994
) to minimize drag. 25
devices in total were attached to birds tending the nests and left in place
for 160 days, during which time the birds went to sea to forage. When
they returned, the units were removed and the birds replaced on the nest where
they continued with breeding activities. Data were accessed from the units by
using a computer and a RS 232 interface.
The devices were potted in resin, had maximum dimensions of 140 mmx58
mmx25 mm, weighed 160 g in air and were hydrodynamically shaped.
Previous experiments using Adélie penguins Pygoscelis adeliae
wearing these devices in a swim canal where oxygen consumption was
continuously monitored suggested that energy consumption in birds swimming at
`normal' speeds of 2.1 m s1 was some 6% higher with the
units than without (Culik et al.,
1994b).
The data loggers recorded data up to a maximum of 2 Mb on 6 channels, each
with 16 bit resolution, on swim speed, dive depth, swim direction (2 channels;
see Hochscheid and Wilson,
1999), light intensity and temperature. Only two channels were of
primary importance for this work, these being swim speed and dive depth. Speed
was sensed by a differential pressure sensor linked to a Prandl tube
projecting from the body of the device. These units were calibrated on the
model penguin in the canal for speeds up to 2 m s1 (the
maximum allowed by the system). Speeds could be resolved to better than 0.1 m
s1. Dive depth was sensed by a pressure transducer (range
0106 Pa) reacting to hydrostatic pressure and, after
calibration, was found to be good to better than 0.1 m.
Eight penguins were also given stomach temperature sensors inserted inside
fish, which were then given to the birds to swallow
(Wilson et al., 1995). These
units (Pillbox series; Driesen and Kern GmbH) consisted of a small logger
(maximum dimensions: 18 mm diameter x 85 mm length) enclosed within a
titanium turned housing. Temperature was measured with 8 bit resolution in a
128 kbyte memory. After calibration in a water bath, temperature could be
determined to 0.1°C. Following Wilson et al.
(1998
), the units were
equipped with a spring crown, which reduced the likelihood that they would be
spontaneously regurgitated. In addition, one end of the titanium cylinder was
fitted with a strong rare-earth magnet. After birds containing stomach
temperature sensors had returned from at least one foraging trip, the units
were recovered by inserting a magnetic grab at the end of a silicon tube down
the oesophagus. The grab locked onto the rare-earth magnet on the titanium
housing and the complete system could be withdrawn
(Wilson and Kierspel, 1998
).
Data from the loggers were accessed by a computer linked to a RS232 interface.
Feeding behaviour of the birds was indicated by sudden temperature drops. The
time at which prey were ingested can be determined by assessing the exact time
of the drop and a measure of the mass ingested can be derived by calculating
the area under the asymptote. This is possible after calibrations experiments
where captive birds containing a temperature sensor are given prey fish of
known mass and temperature so that the relationship between the area under the
asymptote and the fish mass can be ascertained (for details, see
Wilson et al., 1995
). This
information was calculated using the programme FEEDINT (Jensen Software
Systems, Laboe, Germany).
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Results |
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![]() | (1) |
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Effect of antenna length
The transducer indicated that for essentially rigid antennae of variable
length, pressure rose gradually for swim speeds up to about 1 m
s1 (Fig. 3A).
After this, pressure rose rapidly with increasing swim speed, the effect being
most apparent with longer antennae. For example, with the 200 mm antenna, the
pressure rose by a factor of about 10.2 at speeds between 1.0 and 2.0 m
s1 whereas with the 100 mm antenna it rose by a factor of
about 7 (Fig. 3A). The point of
inflection appeared to occur at lower speeds with longer antennae
(Fig. 3A).
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Effect of antenna angle
The angles at which essentially rigid antennae of fixed length and diameter
were mounted with respect to water flow affected recorded pressure
substantially. Again, at low speeds, recorded pressure increased only slowly
with increasing speed until ca. 1 m s1
(Fig. 3A), but subsequently
recorded pressure increased much more rapidly, being most apparent at the
least acute angles. For example, the 200 mm long antenna set perpendicular to
water flow increased drag between speeds of 1.0 and 2.0 m s1
by a factor of 10.2 but only increased drag by a factor of 7.7 over the same
speed range when set at an angle of 45° to water flow
(Fig. 3A). The point of
inflection occurred at lower speeds in the least acute angles
(Fig. 3A).
Effect of antenna flexibility
Although the pressure recorded by the transducer increased with increasing
speed for flexible antennae, the form of the increase was sigmoid
(Fig. 3B). This feature was
apparent even for antennae set at acute angles to the direction of water flow.
Unlike the case with primarily rigid antennae, it appeared that increases in
pressure were not systematic with antenna length; the pressure increase
recorded with the 150 mm long antenna was markedly less than that recorded for
both the 200 mm and the 100 mm long antennae. This arose because, although the
material used for the antennae in the tests was the same, there were
substantial differences in the flexibility, presumably due to minute
differences in the way the springs were wound. This affected the recorded
pressure changes and demonstrated the extent to which antenna flexibility may
be important in drag considerations.
Effect of antenna diameter
Recorded pressure for rigid antennae of fixed length increased
substantially with increasing antenna diameter
(Fig. 4). For example, the
pressure recorded for a 200 mm antenna with a diameter of 3 mm at 2 m
s1 was about 230% higher than that for a 2 mm diameter
antenna and about 770% higher than for a 1 mm diameter antenna. It was notable
that, although we attempted to use rigid antennae, the cases with small
diameter were observed to bend somewhat at higher speeds. As in the case of
antenna length, increases in pressure with increasing speed were slight up to
ca. 1 m s1 whereupon, with further increasing speeds, they
increased much more rapidly (Fig.
4). The point of inflection occurred at lower speeds for antennae
of greater diameter.
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Field studies
Swim speeds and time underwater
Birds equipped with external loggers generally swam at speeds calculated to
be between 1.5 and 3 m s1. There was, however, consistent,
marked reduction in swim speeds during the first part of all foraging trips,
which corresponded to periods of travel from the breeding colony to the
foraging site (for a discussion, see e.g.
Wilson and Wilson, 1990). If
these periods are excluded (to facilitate later calculations; see below), the
mean swim speed of Magellanic penguins was 2.3±0.88 m
s1 (mean ± S.D.,
N=8302 from nine birds). Modal swim speed was 2.2 m
s1 (Fig. 5A).
Close examination of individual dives showed that, during foraging, swim speed
generally varied between 1.8 and 2.8 m s1, increasing
markedly during particular dives (Fig.
5B). We interpreted this increase in speed to be due to periods of
prey pursuit, as documented by Wilson et al.
(2002
). Assuming this to be
the case, the mean number of consecutive dives where birds exploited a patch
was 2.74±2.84 (mean ± S.D.,
N=302), although the frequency distribution of this was not normal
(Fig. 6). During periods of
prey exploitation, birds spent a total of 83% of their time underwater, 17%
being spent resting between dives. During periods when prey were apparently
not being exploited birds spent 76% of their time underwater and 24% of their
time resting between dives.
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Feeding behaviour
The stomach temperature loggers showed clearly when birds had ingested food
via sharp drops in measured temperature (cf.
Wilson et al., 1995). However,
this pattern was not apparent over the whole foraging period, the latter half
showing a slow general temperature drop
(Wilson et al., 1995
). This
pattern is due to food ingestion and digestion for the foraging adult during
the initial phase of the foraging trip followed by a period where food is
ingested for the chick, this process necessitating that digestion be stopped
(see Peters, 1998
;
Gauthier-Clerc et al., 2000
).
Calculation of both the timing of food ingestion as well as the mass ingested
is inaccurate for this latter period
(Wilson et al., 1995
;
Peters, 1998
). Thus, our
results regarding feeding frequency and masses are only presented for the
initial period of the foraging trip.
The mean mass of food ingested per ingestion event was 53.3±67.7 g
(mean ± S.D., N=65); however, the
frequency distribution of the masses was not normal, with smaller amounts
being ingested most often (Fig.
6). The mean time between patch encounters was 47.5±74.7
min (mean ± S.D., N=60) although this
was not normally distributed either (Fig.
7). Generally, prey patches were encountered within 10 min of each
other although there were three occasions in excess of 2 h when prey were not
encountered (Fig. 7). Since the
birds carrying stomach temperature loggers were not simultaneously equipped
with external loggers, we could not be sure that, in these cases, the penguins
were actively foraging and we suspect that the birds rested (cf.
Wilson and Peters, 1999). If
these data are excluded, the mean search time between prey patches becomes
36.3±33.3 min (mean ± S.D.,
N=57).
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Discussion |
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Changes under the `psychological' category can only be considered on a
species-by-species basis, so that no general rules can be derived (see e.g.
Calvo and Furness, 1992, and
references therein). Physical disabilities can be determined to some extent by
examination of animals in captivity (e.g.
Heath, 1987
), although their
consequences are often difficult to quantify. Changed energetics can be
accessed by careful gas respirometry studies (e.g.
Culik et al., 1994b
) or by
doubly labelled water studies (e.g. Gales
et al., 1990
) and are also accessible via examination of
heart rate (e.g. Butler, 1993
).
In our treatment of the effects of antennae on the behaviour of marine animals
we have limited ourselves solely to consideration of the energetic
consequences of potentially increased drag. This ignores a number of important
features that we could not quantify, but which should be mentioned. Firstly,
penguins at the surface may be subject to spray drag. Secondly, Magellanic
penguins undergo considerable changes in both angular and absolute
acceleration during foraging (see e.g.
Wilson et al., 2002
;
Simeone and Wilson, 2003
),
whereas we only treat the energetically more mild constant-velocity scenario.
Finally, it is likely that birds equipped with antennae incur extra energy
costs from induced drag associated with trying to maintain trim because the
position of the antenna would produce a torque that would pitch the anterior
part of the penguin upward. All these features will tend to make the case of
penguins swimming with attached antennae more detrimental than we describe
below.
In our treatise of the changing energetics of penguin swimming resulting from increased drag associated with attached antennae, we can allude to potential limitations of maximum swim speed, but we cannot relate this to prey capture success. After making a few assumptions about the way penguins forage we can, however, speculate as to whether birds carrying external antennae can balance energy expenditure with energy gain during normal foraging. This process is based on coupling various necessary elements on penguin energetics and foraging together: derivation of the antenna-dependent drag, as experienced by the bird using the data from the swim canal tests, use of published data on energy expenditure of penguins as a function of speed (and therefore drag), and finally data on foraging parameters (dive durations and swim speeds coupled with prey ingestion rates) of free-living penguins.
Derivation of antenna-dependent drag
A penguin swimming with a rigid antenna on its back perpendicular to water
flow experiences an additional drag (in N) from the antenna. This drag results
in a torque that acts on the antenna at the lever arm r. At the
fulcrum, at the base of the antenna, there is a balance of forces and moments.
The acting force operates against the swim direction, braking the penguin and
necessitating greater energy expenditure to maintain speed. In our tank tests
the resulting torque, M, was translated via the fulcrum to
the second moment arm, leading to the sensor, so that the cork bung exerted a
force on the pressure transducer. During movement, an effective water speed
profile is produced in the boundary layer close to the surface of the device.
According to Bohl (1991), the
layer thickness of the turbulent boundary layer d is greater than the
laminar boundary layer, so that we assume a turbulent boundary layer and use:
![]() | (2) |
If we assume that the drag acts equally over the full length of the
antenna, then M can be deduced from the integral of the force,
Fd, over the length of the antenna, L:
![]() | (3) |
![]() | (4) |
![]() | (5) |
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The power output Po (W) necessary to transport the antenna is:
![]() | (6) |
![]() | (7) |
![]() | (8) |
Costs of swimming for equipped and unequipped penguins
Although there are virtually no data available on the energetics of
Magellanic penguins, there is information on the highly similar (see
Williams, 1995) congeneric
Humboldt Spheniscus humboldti and African penguins Spheniscus
demersus. In fact, it is notable that there are no radical differences in
energy expenditure as a function of activity in any of the medium-sized
penguins (see e.g. Pinshow et al.,
1977
; Culik et al.,
1996
). We therefore assume that we could estimate energy
consumption of Magellanic penguins quite closely.
The mass-specific power requirements for a swimming penguin are reported to
be approximated by a third degree polynomial function
(Culik et al., 1996) according
to:
![]() | (9) |
The equation for calculating the drag on a penguin gliding underwater is:
![]() | (10) |
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Of particular note is that derived values for drag for the antennae differ
from that predicted using Equation 10, where the antenna is treated as an
elongated cylinder (Cd=1,2). This presumably stems from
the complexities of water flow over the penguin's body which, among other
things, cause the water flowing proximate to the body to be moving faster than
that moving an infinite distance away. In addition, as pointed out by Obrecht
et al. (1988), simple addition
of the two different drags, as derived from Equation 10 (of antenna and
penguin), is erroneous since the overall drag is greater than the sum of its
parts.
A key element in determining travelling efficiency is the cost of transport, this being given by the power input divided by the speed. Determination of the cost of transport for penguins with and without external antennae shows that the increase in drag caused by the antenna results in an overall increase in cost of transport, particularly at speeds in excess of 1 m s1, but also that the speed at which the minimum cost of transport occurs is shifted to lower values in birds carrying antennae, with the effect being most pronounced for antennae that produce most drag (Fig. 10B).
Behavioural consequences of transporting an antenna for Magellanic penguins
The most parsimonious reaction to the fact that Magellanic penguins must
ostensibly expend more energy to swim at normal speeds with externally
attached antennae would be to say that the birds must simply work
correspondingly harder to compensate. There are, however, reasons to believe
that a small, inappropriately designed body such as an antenna might result in
an exacerbation of deleterious effects so that ultimately the foraging
efficiency of penguins could be seriously compromised. This can be alluded to
by a simple mathematical model.
We assume that penguin foraging (for a review, see
Wilson, 1995) is typified by
periods during which the bird searches for prey by travelling underwater
during dives interspaced with short rests on the surface. After a prey patch
(normally a shoal of pelagic school fish in Spheniscus penguins;
Wilson and Wilson, 1990
) is
encountered, the penguin remains underwater, ingesting more or less
continuously until oxygen reserves are depleted, whereupon the bird must
return to the surface. After recovery at the surface, the penguin dives again
and attempts to relocate the prey patch
(Wilson and Wilson, 1995
). If
successful, the process of ingestion is repeated. If not, the bird must begin
the search for a new prey patch. The success of this strategy critically
depends on prey density but can be modelled out using energy expenditure and
gain over time.
The energy expended during the search phase is:
![]() | (11) |
The energy expended during the patch exploitation phase is:
![]() | (12) |
![]() | (13) |
![]() | (14) |
![]() | (15) |
Note that the power requirements for swimming at different speeds are
contained within the 1 term (see Equations 9, 14). The energy gain
during patch exploitation is:
![]() | (16) |
![]() | (17) |
![]() | (18) |
If we assume that Magellanic penguins conform to the equation for energy
expenditure over time with respect to speed described earlier (Equation 9),
then birds swimming at cruising speeds of 1.77 m s1 and
engaging in prey capture speeds of 2.25 m s1 (for Magellanic
penguins feeding on small sardines; see
Wilson et al., 2002)
theoretically expend 12.7 and 20.5 W kg1, respectively. This
is 50.7 and 81.9 W,respectively, for a standard Magellanic penguin weighing 4
kg (see Williams, 1995
). If we
use literature values for total body oxygen stores from Pygoscelis
penguins as applicable for Magellanic penguins (data summarized in
Culik et al., 1994a
), then
birds have 59.5 ml O2 kg1 or 238 ml O2
bird1. Since the consumption of 1 ml oxygen corresponds to
approximately 20 J (Schmidt-Nielsen,
1990
), Magellanic penguins swimming at 1.77 and 2.25 m
s1 would be able to dive aerobically for only 93.9 and 58.1
s, respectively. We note that the formulation that we use is most appropriate
for swim speeds up to ca. 2.5 m s1 but may become
increasingly problematic at higher speeds. This is because Luna-Jorquera and
Culik (2000
) only worked with
Humboldt penguins that swam at maximum speeds of 2.2 m s1 in
their experimental setup, resulting in increasing uncertainties at higher
speeds.
We were unable to measure prey ingestion in relation to diving behaviour
directly in our field work, since birds were either equipped with external
loggers or stomach temperature loggers. Ideally, both units should be deployed
together so that the mass ingested per patch exploited can be directly equated
with the time spent underwater in the pursuit of prey, as measured by the
depth gauges in the loggers. Generally, however, it is to be expected that the
longer a bird spends in a patch feeding, the more it will ingest. In this
regard, comparison of the frequency distribution of the mass of food ingested
by Magellanic penguins foraging from Punta Norte, Argentina is remarkably
similar to the frequency distribution of the number of dives in a feeding bout
from birds from this region (cf. Fig.
5, where the number of classes has been, in each case, limited to
ten to allow comparison). The implication from this is, therefore, assuming
that the stomach temperature of logger-equipped birds and TDR-equipped birds
were subject to the same conditions, that Magellanic penguins from the region
ingest about 20 g of anchovy per successful dive. This translates to a mean of
54 g ingested per patch (assuming the average patch to be exploited over 2.7
dives see Table 1) or
ca. 82 g h1 spent foraging (assuming that birds search for
36.4 min between patches and that patch exploitation takes ca. 3 min, composed
of 2.7 dives of 58 s plus pauses amounting to 17% of these; see
Table 1). This compares well
with the value of 0.025 g of prey ingested per second at sea (or 90 g
h1) noted by Wilson and Grémillet
(1996) for African penguins,
although it should be noted that recently acquired data suggest that in some
areas Magellanic penguins may ingest much higher quantities of prey per unit
time (Wilson, 2004
).
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For the purposes of our calculations, we assume the above conditions to be
representative of those experienced by free-living Magellanic penguins and,
for our presented model on the efficiency of foraging Magellanic penguins with
and without antennae, we make the assumptions listed in
Table 1, most of which are
derived from our fieldwork or from the literature. Much fieldwork data is
derived from device-equipped birds, albeit individuals without antennae. We
assume that these birds behaved in the same way as non-equipped conspecifics,
although it is likely that their foraging capacities were also somewhat
compromised. In addition, we assume that Magellanic penguins only exploit a
patch underwater aerobically (cf. Butler
and Woakes, 1984), after which time they return to the surface to
breathe, and that birds feed exclusively on anchovy Engraulis
anchoita (Frere et al.,
1996
; Scolaro et al.,
1999
).
Our model indicates that if free-swimming Magellanic penguins foraging from
Punta Norte, Argentina ingest 20 g of anchovy per dive when exploiting a
patch, they have a foraging efficiency of 2.5. By so doing, the penguins more
than compensate for the energy expended for foraging, a condition that must be
fulfilled if birds are to survive in the long term. There is remarkably little
information on the foraging efficiency of animals, but Nagy and Shoemaker
(1984) summarize data from
three major groups with values of 1.01.6 for sit-and-wait insectivores,
1.42.5 in widely foraging insectivores and 917 in herbivores. In
seabirds a value of 1.3 has been quoted for northern gannets Sula
bassana (Garthe et al.,
1999
, Garthe et al.,
1999
) and ca. 3.5 for great cormorants Phalacrocorax
carbo (Grémillet,
1997
).
Our model predicts that the foraging efficiency of Magellanic penguins
drops dramatically if birds are equipped with antennae with, for example,
penguins carrying antennae measuring 150 mmx3 mm incurring a more than
twofold reduction in foraging efficiency and birds carrying antennae measuring
200 mmx3 mm incurring an almost fivefold reduction in foraging
efficiency (Table 2). This
apparent increasing deleterious effect of what appears a relatively trivial
body attached to the penguin reflects two primary processes: (i) that the
power output necessary to achieve particular swim speeds with the antennae
increases dramatically with speed, and (ii) that the power input from the
penguin also increases as an approximately cubed function of the drag. An
obvious consequence of this is that the conditions under which the penguin
must operate are particularly sensitive to speed
(Fig. 11). We note that
Adélie Penguins, which capture prey at speeds lower than their
travelling speeds (1.7 m s1 and 2.0, respectively;
Wilson et al., 2002) and, in
any event, have prey capture speeds markedly lower than those of Magellanic
penguin, have a foraging efficiency just above one, even if equipped with an
external antenna (200 mmx3 mm). Thus, even in the case of the
Adélie penguin, although foraging efficiency with such an antenna is
reduced compared to non-equipped birds by a factor of just over three, the
chances of the birds surviving would be increased considerably (apart from
prey capture speed, all other parameters taken are those from the Magellanic
penguin). Since there is a general relationship between prey swim speed and
prey size (Wardle, 1975
;
Peters, 1983
) and the general
division of penguin feeding habits is divided into those species that feed on
fish and squid and those that feed on considerably smaller crustacea
(Williams, 1995
), we would
predict that fish-feeding penguins equipped with external antennae will be
more compromised than crustacean-feeders.
|
|
In fact, penguins may be able to compensate for the effects of externally
attached devices by altering swim speed in a general sense
(Wilson et al., 1986) so as to
reduce metabolic rates. This can occur if species concentrate on smaller,
slower-moving prey species than they might otherwise take or if travelling
speeds are decreased. The consequences for the latter for foraging efficiency
can be readily assessed using our model. If, for example, a penguin reduced
travelling speed to 1 m s1, although the time spent
travelling between patches would increase proportionately, overall foraging
efficiency would rise to almost two even if prey capture speed were 1.7 m
s1 (Fig.
11). Thus, appropriate changes in foraging parameters might allow
penguins equipped with antennae to forage more efficiently than they would
otherwise if they adopted their standard pattern and this may, in part,
explain why penguins equipped with larger devices tend to travel more slowly
(Wilson et al., 1986
).
The process of determining the survival likelihood of Magellanic penguins can be examined conversely by setting a minimum foraging efficiency of 1.0 and determining the rate at which birds must encounter prey in order for them to be able to compensate for the increased drag imposed by external antennae. This might help us identify whether penguins could potentially be fitted with devices including antennae if they occurred at localities where prey are particularly abundant (although this premise assumes that the birds never stop foraging). Our model predicts that unequipped Magellanic penguins need to encounter a prey patch at least once every 85 min to have a foraging efficiency of exactly 1, whereas birds equipped with antennae 200 mm long and with a diameter of 3 mm would have to encounter a prey patch once every ca. 17 min. For prey densities in excess of this, penguins would be able to gain mass.
Our model is necessarily simplistic. For example, we only consider the
effect of the antenna rather than the antenna plus attached device (cf.
Culik et al., 1994b). In
addition, we consider, for example, that the prey capture speed is that used
for the whole of the dive during which prey are exploited, something that
ignores the time (and energy) that birds need to descend from the water
surface to the foraging depth. However, the energy for transit will also use
body oxygen reserves, further limiting the time available for prey capture.
Normal swim speeds of 1.77 m s1 for Magellanic penguins
swimming with an external antenna (200 mmx3 mm) will give an aerobic
dive limit of ca. 40 s, which will allow a bird diving vertically to sample
only the top 20 m of the water column. An unequipped bird swimming at this
speed may dive for 94 s, reaching 80 m. Note that this treatise ignores recent
buoyancy findings by Sato et al.
(2002
) and Wilson and Liebsch
(2003
), and the fact that
Magellanic penguins do not descend vertically anyway (cf.
Wilson and Wilson, 1995
).
This work indicates that apparently relatively trivial bodies attached to swimming and diving animals may do more than simply substantially affect their energetics, although this in itself may affect standard dive parameters such as swim speeds, dive depths and rates of change of depth. Animals may also switch foraging strategies. The implications of this are profound and in light of this we would suggest that more careful assessment of the effects of externally attached devices is needed. This could be facilitated by current advances in logging technology, which are so substantial that is it now possible to equip free-living animals with minimal recording systems so that device-dependent changes in their behaviour can be documented as the attached units are carefully expanded in size. Such an approach would allow researchers to work with free-living animals, benefiting from all the advantages that this brings with it, while at the same time gaining quantitative data on the more intractable effects of devices.
Recommendations for antennae design
Although our treatise involves a number of assumptions, it is clear that
externally attached antennae can be potentially extremely detrimental to the
well-being of equipped marine animals. In order that effects be minimized we
suggest the following avenues be explored:
In any event, in view of the worrying consequences on penguin well-being implied by this study, we suggest that any workers using devices with external antennae on penguins set up rigorous controls to examine differences in foraging behaviour between equipped and unequipped birds. The aim should be to demonstrate, via appropriate device modification etc., that equipped animals are able to perform in manner that is a broadly similar to unequipped conspecifics.
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