Developmental changes in cardiorespiratory patterns associated with terrestrial apnoeas in harbour seal pups
1 Department of Biology, University of Waterloo, Waterloo, ON, Canada N2L
3K8
2 Department of Biology, SUNY Potsdam, Potsdam, NY 13676, USA
3 Department of Biological Sciences, University of Alaska Anchorage,
Anchorage, AK 99508, USA
4 Maurice Lamontagne Institute, Department of Fisheries and Oceans,
Mont-Joli, QC, Canada G5H 3Z4
Author for correspondence (e-mail:
schreejf{at}potsdam.edu)
Accepted 29 July 2004
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Summary |
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Key words: apnoea, eupnoea, respiration, heart rate, bradycardia, sleep, ontogeny, cardiorespiratory control, harbour seal, Phoca vitulina
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Introduction |
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The physiological factors that limit both diving and sleep apnoea duration
are correlated with animal size and age. In adults, total body oxygen stores
are proportional to body mass (Mb;
Kooyman, 1989), whereas
metabolic rate scales to Mb0.75
(Kleiber, 1961
). Thus, apnoea
durations are shorter for smaller species. In addition, pups and juveniles
have reduced breath-holding capacities because young, growing animals have
higher mass-specific metabolic rates and lower mass-specific total body oxygen
stores, compared to adults of similar size
(Brody, 1945
;
Kleiber, 1961
;
Poczopko, 1979
;
Lavigne et al., 1986
).
Furthermore, the ability to regulate physiological processes such as heart
rate, respiration, body temperature and vasoconstriction is not fully
developed at birth (Cherepanova et al.,
1993
; Castellini et al.,
1994b
; Thorson and Le Boeuf,
1994
; Burns et al.,
1996
; Hansen and Lavigne,
1997
; Falabella et al.,
1999
).
The rate of physiological development appears to be closely linked to the
onset of independent foraging (Castellini
et al., 1994b; Burns et al.,
1996
; Castellini,
1996
; Burns, 1997
;
Falabella et al., 1999
;
Noren et al., 2001
). To
survive this transition, seal pups must develop adequate swimming and diving
skills before their energy reserves are depleted. A key component of neonatal
development is increased cardiorespiratory control
(Castellini, 1996
). Prior to
their first foraging trip, weaned elephant seals (Mirounga
angustirostris and M. leonina) spend several months on land,
which represents a critical period for the maturation of cardiorespiratory
control mechanisms (Castellini et al.,
1994b
; Castellini,
1996
; Falabella et al.,
1999
). Older seals not only exhibit a stable breathing pattern,
consisting of extended apnoeas followed by short periods of eupnoea, they also
display a lower and less variable heart rate during apnoea, and a
well-developed sinus arrhythmia during eupnoea
(Castellini et al., 1994b
;
Castellini, 1996
;
Falabella et al., 1999
).
Harbour seals Phoca vitulina, unlike most other phocid neonates,
enter the water within hours of birth
(Newby, 1973) and are
increasingly aquatically active throughout the nursing period
(Bekkby and Bjørge,
2000
; Jørgensen et al.,
2001
). Therefore, the acquisition of swimming and diving skills is
temporally separated from the onset of independent foraging. As such, the
degree of cardiorespiratory control may be greater at birth, and/or the rate
of maturation more rapid in this precocial species, compared to phocid species
that delay aquatic activity until after weaning (Castellini,
1995
,
1996
;
Burns, 1997
). Thus, the aim of
this study was to describe the ontogenetic changes in cardiorespiratory
patterns associated with terrestrial apnoeas in harbour seal pups from birth
to weaning.
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Materials and methods |
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Data collection
Due to the precocial nature of this species, and the logistic constraints
imposed by working on small boats, measurements could not be obtained from
unrestrained animals. As a result, during the 2001 field season, pups were
manually restrained during measurements: with a pup positioned in ventral
recumbency, a single handler, facing in the opposite direction, knelt and
straddled the pup at midbody, pinioned the foreflippers to the side of the
animal, and then leaned forward and applied pressure to the hindflippers. In
2002, pups were physically restrained using a custom built adjustable wooden
V-board and canvas harness. Adult females were covered with a net and manually
restrained by a single handler. Electrocardiogram (ECG), heart rate and
respiration data were collected using a portable multi-channel physiological
recorder (BioTach with Serial Linked Interface Component Software, Model
2121/3R-SP, UFI, Morro Bay, CA, USA) connected to custom designed electrodes
(25 G x 1.5 inch hypodermic needles soldered to 8 m lengths of
4-conductor 20 G microphone cable; PrecisionGlide® #305127,
Becton-Dickinson, Franklin Lakes, NJ, USA; #8424, Belden Inc., Richmond, IN,
USA) and a portable computer. Electrodes were inserted subdermally in the
mid-dorsal region of the animal and then anchored to the fur using
cyanoacrylate adhesive and accelerator (Superbonder® 422 Instant Adhesive
and Tak Pak® 7452 Accelerator, Loctite Canada Inc., Mississauga, ON,
Canada). The negative electrode was placed over the left scapula, the positive
electrode at a diagonal equidistant from the heart on the opposite side, and
the ground to the left of the positive electrode. The BioTach monitor
converted changes in thoracic impedance into a respiratory signal; therefore
any movement in addition to that of the ribcage (e.g. the seal, handler, boat,
etc.) was also detected, resulting in erroneous values. As a result, a
camcorder (Sony Handycam®, CCD-TRV57, and Rain Jacket, LCR-TRX3, Sony
Ltd., Toronto, ON, Canada) was also used to record respiration visually and to
obtain additional behavioural data.
Analysis and statistics
Rest was defined as a period of time during which an animal was lying
quietly with its eyes closed (Blackwell and
Le Boeuf, 1993; Castellini et
al., 1994b
). However, it should be noted that even though an
animal is lying motionless with its eyes closed, it may not be sleeping; such
a state has also been exhibited during periods of quiet wakefulness
(Mukhametov et al., 1982
).
Eupnoea was categorized by regular opening and closing of a pup's nostrils,
while apnoea was observed as a breath-hold, during which nostrils remained
closed for >10 s following an exhalation
(Bacon et al., 1985
;
Blackwell and Le Boeuf, 1993
;
Falabella et al., 1999
). Since
electroencephalographic activity was not recorded during this study,
respiratory pauses are referred to as terrestrial apnoeas rather than sleep
apnoeas (Castellini et al.,
1994b
).
Video recordings were viewed and the percentage of time spent resting was calculated using the camcorder on-screen clock display. The occurrence of each respiration was determined from the video recordings using an elapsed timing program designed in MatLab 6.1® (The Mathworks Inc., Natick, MA, USA). Subsequently, the time interval between consecutive breaths was converted to an instantaneous breathing rate (breaths min1). The precise onset and cessation of each apnoea was verified by the respiration trace obtained by the physiological monitor. For instances where no corresponding video recording was obtained, apnoeas were selected using a combination of information from field notes, event markers, and the respiration trace. The time interval between successive heartbeats was measured using an R-wave peak detection program designed in Mathcad 2001 Professional® (MathSoft Engineering & Education Inc. Cambridge, MA, USA). Subsequently, each RR interval was converted to an instantaneous heart rate (beats min1).
Pups weighing 11.1 kg at first capture were considered newborn (pup age
= 1 day; Dubé et al.,
2003
). For pups not captured on the day of birth, age (days) was
calculated by subtracting the published mass at birth (11.1±0.22 kg)
from the mass at first capture (in kg) and dividing by the observed growth
rate (kg day1)
(Dubé et al., 2003
).
The lactation period for this population of harbour seal pups has been
estimated to last 34±1.8 days
(Dubé et al., 2003
).
Pups approaching this age were considered weaned if they were observed to be
alone and their blood plasma was clear (i.e. non-lipaemic;
Clark, 2004
;
Bowen et al., 1985
).
To achieve statistical independence, and to optimize age distribution, only one data file was selected from individuals monitored multiple times throughout the nursing period. Effects of year and sex were assessed using a two-way analysis of variance (ANOVA); age relationships were examined using least-squares linear regression; and paired t-tests were used to compare heart rate during apnoea and eupnoea (Systat 9 for Windows®, SPSS Inc., Chicago, IL, USA; SAS System for Windows 8.02®, SAS Institute Inc., Cary, NC, USA). Significance level was set at 0.05. Data are presented as means ± S.E.M.
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Results |
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Pre-weaned pups spent 57.0±3.0% of the observation time resting; during this time, breathing became episodic, consisting of eupnoea interspersed with periods of apnoea. Breathing frequency did not change significantly over the course of the nursing period; on average, pups breathed at a rate of 35.0±0.9 breaths min1 (Fig. 2). Eupnoea episodes lasted 2.5±0.2 min. Pups spent 12.5±1.7% of the time resting in apnoea. Pups exhibited significantly fewer apnoeas during the 2001 field season compared to 2002 (F27,18=7.704, P=0.008); the mean number of apnoeas was 2.7±0.5 (range 09) and 5.2±0.8 (range 012), respectively. Mean apnoea duration increased significantly during the nursing period (Fig. 3). However, maximum apnoea duration (43.4±2.8 s,range 1178 s) did not increase with age. The longest breath-hold observed occurred in a 19 day-old pup and lasted for 78 s.
|
|
Heart rate was significantly lower during apnoea than during eupnoea (t31=16.05, P<0.0001). Mean eupnoeic heart rate was 159.6±1.9 beats min1 and did not change significantly during the nursing period (Fig. 4). Mean apnoeic heart rate decreased significantly with age (Fig. 5A). The distribution of apnoeic heart rate was bimodal, with a minimum number of observations around 100 beats min1. Heart rates were categorized as `low' (<100 beats min1) or `high' (>100 beats min1; Fig. 6). High apnoeic heart rate decreased significantly with age, while the low apnoeic heart rate remained stable at 75.7±1.0 beats min1 (Fig. 5B). The proportion of time spent in each mode changed throughout the nursing period. The low mode dominated as age increased (Figs 5C, 6, 7). The lowest instantaneous heart rate recorded, 9 beats min1, occurred in a 19 day-old pup during a 78 sapnoea. The highest instantaneous heart rate recorded was 213 beats min1 and occurred during eupnoea in three pre-weaned pups ranging in age from 428 days. No sex differences were observed for any of the parameters reported above.
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Discussion |
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The terrestrial breathing pattern of resting, pre-weaned harbour seal pups
was irregular, consisting of apnoeas and eupnoeas of varying durations.
Breathing frequency did not change throughout the nursing period and fell
within the range observed previously for juvenile harbour seals (1853
breaths min1; Harrison
and Tomlinson, 1960;
Påsche and Krog, 1980
;
Skinner and Milsom, 2001
).
Terrestrial apnoea duration increased during the lactation period, paralleling
an increase in dive duration (Greaves et
al., in press a
), and values were similar to those obtained for
resting, captive harbour seal pups less than 2 weeks of age (31 s;
Bacon et al., 1985
).
Upon weaning, however, several changes occurred. Respiration rate decreased
(Fig. 2), approaching adult
levels (822 breaths min1;
Harrison and Tomlinson, 1960;
Bacon et al., 1985
). Consistent
with dive duration (Greaves et al., in
press a
), the length of terrestrial apnoeas continued to increase
post-weaning (Fig. 3).
Terrestrial apnoea durations were similar to those obtained previously for
juvenile harbour seals (19104 s;
Irving et al., 1935
;
Dykes, 1974
;
Påsche and Krog, 1980
;
Jobsis et al., 2001
), but less
than those displayed by adults (225 s;
Williams and Bryden, 1993
).
Additionally, upon weaning, the alternating apnoeiceupnoeic breathing
pattern began to stabilize. For example, a 41 day-old weanling that appeared
to be sleeping displayed a regular apnoeaeupnoea cycle until it awoke.
Irving et al. (1935
) observed
a similar breathing pattern in quietly resting 4 month-old harbour seals,
describing it as a regularly maintained sequence of 612 respirations
followed by an apnoea of 3060 s. The observed changes, from birth to
adulthood, can be attributed in part to an increase in total body oxygen
stores (Kodama et al., 1977
;
Ponganis et al., 1993
;
Thorson and Le Boeuf, 1994
;
Burns et al., 1999
;
Clark, 2004
) and a decrease in
metabolic rate (Miller and Irving,
1975
; Ashwell-Erickson and
Elsner, 1981
; Rea and Costa,
1992
; Hansen,
1995
) that occurs with increasing size and age. Additionally,
improved cardiovascular control also contributes to the increased
breath-holding capacity observed
(Castellini et al., 1994b
;
Castellini, 1996
).
In phocids, while diving or sleeping, heart rate follows the pattern of
bradycardia during apnoea and tachycardia during eupnoea
(Kooyman and Campbell, 1972;
Andrews et al., 1997
). This
bimodal or two-speed heart rate pattern begins to develop in utero
(Liggins et al., 1980
;
Bacon et al., 1985
). During the
last third of gestation, foetal harbour seals exhibited a `slower' heart rate
(79 beats min1) that was distinct from the `faster'
embryonic rate (125 beats min1) first observed early in
gestation (Bacon et al., 1985
).
The amount of bradycardia steadily increased as parturition approached
(Bacon et al., 1985
). This
bimodal heart rate pattern continues to develop postpartum
(Table 1).
|
Eupnoeic heart rate remained stable during the lactation period and was
similar to the surface heart rate of free-ranging, diving harbour seal pups
(155 beats min1;
Greaves et al., in press a
),
but greater than the mean rate obtained for resting, captive harbour seal pups
(138 beats min1; Bacon et
al., 1985
). Eupnoeic heart rate presumably begins to decrease
post-weaning once animals start to accumulate body mass (
46 weeks
post-weaning; Muelbert et al.,
2003
), and then gradually declines
(Fig. 4) as animals grow into
adulthood (Fig. 4;
Stahl, 1967
;
Castellini and Zenteno-Savin,
1997
). Terrestrial apnoeic heart rate decreased throughout the
nursing period, paralleling a similar decrease in mean diving heart rate (from
140 to 70 beats min1;
Greaves et al., in press a
).
However, Bacon et al. (1985
)
observed a lower mean terrestrial apnoeic heart rate for harbour seal pups
less than 2 weeks of age (84 beats min1). Similar to
eupnoeic heart rate, further decreases in mean apnoeic heart rate
(Fig. 5) would be expected as
animals grow into adulthood (Stahl,
1967
; Castellini and
Zenteno-Savin, 1997
).
Similar to Greaves et al. (in press
a), our findings suggest that refinement of the regulatory
mechanisms, which brought about the foetal bradycardia observed by Bacon et
al. (1985
), continues after
birth. Terrestrial apnoeic heart rate, like diving heart rate
(Greaves et al., in press a
),
was bimodal with a trough around 100 beats min1. The high
terrestrial apnoeic heart observed in this study was comparable to the `diving
tachycardia' (
150 beats min1), and the low terrestrial
apnoeic heart rate equivalent to the `diving bradycardia' (
70 beats
min1), described by Greaves et al.
(in press a
) for pre-weaned
harbour seal pups. In both studies, the decline in mean apnoeic heart rate was
driven primarily not by a change in the mean value for each mode but by the
proportion of time spent in each mode. Most likely an increase in vagal tone
with age (Katona et al., 1980
)
enabled older animals to spend a greater proportion of time in the lower heart
rate mode. In younger pups, the ability to attain a lower heart rate was
periodic, whereas in older pups, this lower heart rate was reached but not
strictly maintained, as evident from periodic escapes in vagal control to the
higher mode. Greaves et al. (in press
b
) determined that young pups attempted to reduce their heart rate
every 310 s during a dive. Consistent with Greaves et al.
(in press a
), by the time pups
were weaned (
4 weeks of age), they exhibited a degree of cardiovascular
control comparable to that of adults (Fig.
5).
As first hypothesized by Castellini
(1995), the rate of
cardiorespiratory control development was quicker in the harbour seal,
compared to elephant and Weddell seals. Although similar changes in
cardiorespiratory patterns have been reported for these species
(Table 1;
Kenny, 1979
;
Blackwell and Le Boeuf, 1993
;
Castellini, 1996
;
Burns et al., 1996
), the
maturation of cardiorespiratory control mechanisms typically takes longer to
develop because of their extended lactation and/or post-weaning fast periods
(Castellini et al., 1994a
;
Burns et al., 1996
;
Castellini, 1996
;
Falabella et al., 1999
).
Unlike harbour seals that enter the water the day they are born
(Newby, 1973
) and begin
foraging before (J.L.L., personal observation) or within days of weaning
(Muelbert et al., 2003
),
northern elephant seals are essentially land bound for 4 months
(Thorson and Le Boeuf, 1994
).
It is during this extended terrestrial fast that cardiorespiratory patterns
stabilize (Castellini et al.,
1994b
; Castellini,
1996
; Falabella et al.,
1999
). Weddell seals begin serious diving around 2 months of age,
and as such exhibit a rate of development intermediate to that of harbour and
elephant seals (Castellini,
1995
,
1996
). Despite their different
developmental strategies, elephant, Weddell and harbour seal pups appear to be
capable divers, physiologically, by the time they must begin to forage
independently (Castellini et al.,
1994b
; Burns et al.,
1996
; Castellini,
1996
; Falabella et al.,
1999
). Species that begin to forage independently prior to 1 month
of age, such as the bearded seal (Gjertz
et al., 2000
), may show even more rapid cardiorespiratory control
development.
Unfortunately, harbour seal pups could not be studied while resting in
their natural habitat. Unlike other phocids that haul-out on land or ice for
extended periods of time and can be approached relatively easily while
sleeping (Castellini, 1991;
Blackwell and Le Boeuf, 1993
;
Castellini et al., 1994b
;
Falabella et al., 1999
),
harbour seals haul-out on coastal reefs or isolated rocks that flood with the
rising tides (Lesage et al.,
1995
). They are very vigilant and wary
(Venables and Venables, 1955
;
Terhune and Brillant, 1996
),
fleeing to the water immediately upon approach (J.L.L., personal observation;
Terhune and Almon, 1983
;
Henry and Hammill, 2001
). In
addition, harbour seal pups are extremely agile and capable of coordinated
movement from a very young age
(Dubé et al., 2003
);
therefore, restraint was necessary during our observations. However, we are
confident that the effects of our experimental protocol were minimal, as many
of the physiological measurements made in this study were quantitatively
similar to those obtained by Greaves et al.
(in press a
) from
free-ranging, diving harbour seal pups.
From electrophysiological studies on a variety of captive phocid species,
it is apparent that prolonged terrestrial apnoeas are associated with sleep,
and that profound cardiovascular and respiratory adjustments occur during the
sleep cycle (Ridgway et al.,
1975; Huntley,
1984
; Castellini et al.,
1994a
; Skinner and Milsom,
2001
). Lyamin et al.
(1993
) studied sleep in harp
seal pups and found that there are developmental changes in sleep parameters.
Therefore, in addition to the changes in cardiorespiratory patterns observed
in harbour seal pups throughout this study, it is likely that sleep
ontogenesis was also occurring during this time. Future studies incorporating
both sleep state and apnoea physiology during this critical period of
development would be of great interest, as Castellini
(1996
) has suggested.
In conclusion, developmental changes in the cardiorespiratory patterns
associated with terrestrial apnoeas in harbour seal pups were comparable to
those reported for elephant and Weddell seals
(Castellini et al., 1994b;
Castellini, 1996
;
Falabella et al., 1999
).
However, due to the early onset of independent foraging, maturation of
cardiorespiratory control mechanisms occurred more rapidly in harbour seals.
This parallels the development of diving activity
(Greaves et al., in press a
)
and total body oxygen stores (Burns et
al., 1999
; Clark,
2004
), which together enable harbour seal pups to be proficient
divers and successful foragers upon weaning.
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Acknowledgments |
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Footnotes |
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