The early life history of tissue oxygenation in crustaceans: the strategy of the myodocopid ostracod Cylindroleberis mariae
Laboratoire d'Ecophysiologie et Ecotoxicologie des Systèmes Aquatiques, UMR 5805 Université Bordeaux 1, France and CNRS, Place du Dr B. Peyneau, 33120 Arcachon, France
* Author for correspondence (e-mail: jc.massabuau{at}epoc.u-bordeaux1.fr)
Accepted 1 December 2004
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Summary |
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Key words: respiration, evolution, crustacea, control of breathing, oxygen regulation, hypoxia, hyperoxia, circadian rhythm
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Introduction |
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Water-breathers are usually tolerant to water oxygenation changes. In
hypoxia, the general rule is an increase branchial water flow, and many also
increase their blood flow rate. Both adaptations allow the animals to maintain
their oxygen consumption independent of water oxygenation. Importantly, it
also allows an adaptation strategy whereby O2 partial pressure,
PO2, in the arterial blood is maintained within
a low and narrow range of 1-3 kPa, largely independent of inspired
PO2
(Massabuau, 2001). This has
been reported in fish, crustacean, mollusc and annelid. Interestingly, in
mammalian tissues the most frequently measured
PO2 is also in the same low range. Based on the
postulate that basic cellular machinery has been established since the early
stages of evolution, it has been proposed that this similarity in oxygenation
status is the consequence of an early adaptation strategy that, subsequently,
throughout the course of evolution, maintained cellular oxygenation in the low
and primitive range at which eukaryotic cells appeared two billions years ago
(Massabuau, 2001
,
2003
). Podocopid ostracods,
which represent the largest ostracod group, are heart- and gill-less
crustaceans although they do possess ventilatory appendages. They have existed
on earth for at least 500 million years and they also follow the same
regulation strategy. However, and contrary to most water-breathers, podocopids
lack any regulatory mechanism of ventilatory adaptation to face changes in
water oxygenation. Instead, they adjust their tissue oxygenation status by
migrating into sediment O2-gradients to find low water
PO2 niches
(Corbari et al., 2004
). Thus,
the podocopid data set reinforced the ideas that: (1) the level of oxygenation
at individual tissue or cellular levels is a fundamental problem of
homeostasis irrespective of species difference; and (2) it could have been
held constant during the evolution of life to retain the original oxygenation
status.
To get more insights into this evolutionary theory we studied myodocopid
ostracods. Myodocopid ostracods appear, from a morphofunctional perspective,
to be more evolved by comparison with podocopid ostracods. Indeed, they
possess not only a ventilatory system, composed of two scaphognathites
ventilating a domiciliar cavity, but also a cardiovascular system composed of
a well-differentiated heart and, in the Cylindroleberid family, 6-8 lamellar
gills (Vannier et al., 1996;
Horne et al., 2002
). Based on
previous evidence, the homeostasis of their internal milieu, in terms of
oxygen, should be maintained by some regulatory mechanisms involving an
autonomous or behavioural adaptive process. Consequently, our aim was to study
how tissue oxygenation status is regulated in Cylindroleberid myodocops.
During evolution, myodocops have acquired a large variety of lifestyles either
benthic, nektobenthic or exclusively planktonic. They are confined to
seawaters where they colonized the shallowest coastal as well as the deepest
bathyal and abyssal environments worldwide
(Horne et al., 2002
). The
species we studied, Cylindroleberis mariae, is a nektobenthic
representative of Cylindroleberid myodocop. It displays nocturnal upward
migrations (Macquart-Moulin,
1999
; Fenwick,
1984
) and rests during the daytime at the sea bottom where many
species inhabit burrows or nests built with sand particles and phytodetritus
(Cohen, 1982
;
Smith and Horne, 2002
). Our
approach was based on a combination of anatomical, physiological and
behavioural analyses to determine the oxygenation strategy of this
species.
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Materials and methods |
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Morphofunctional anatomy
The study was performed on three C. mariae measuring 1.7, 1.8 and
2.0 mm. Whole animals were immersed in a fixative for electron microscopy (6%
glutaraldehyde buffered with 0.4 mol l-1 sodium cacodylate, pH 7.4,
osmotic pressure 1100 mosmol l-1) for 12 h at 4°C and
subsequently rinsed in cacodylate buffer (0.4 mol l-1, NaCl 4%).
They were embedded separately in Araldite. Serial sections were performed with
a Reichert automatic ultra-microtome (Depew, NY, USA). The observations were
measured on enlarged pictures (semi-thin preparations) after visual inspection
using a microscope LEICA TCS 4D.
Maintenance conditions
The animals, together with their natural sediment and phytodetritus, were
placed in an aquarium with a running flow system in a dark thermostated room
set either at 10 or 18°C (Aquarium size: L, 50 cm; W, 50 cm; H, 50 cm).
The aquaria were all supplied with seawater from the bay of Arcachon (water
PO220-21 kPa; water pH
7.8; salinity
28-32%
). Considering the animal size and the amount of organic
material and microfauna naturally present in the sediment, no external food
was added. When required, specimens were isolated on binocular microscope
before experiments. To minimise external disturbances, experimental tanks were
isolated from laboratory vibrations with anti-vibrating benches.
Physiological analysis of ventilatory and circulatory activity by video recording
We analysed the myodocopid ostracod ventilatory system of animals exposed
to various steady water PO2 conditions at
10°C by visual inspection after or during video recording activity. All
video observations were achieved during daytime (i.e. between 9 am and 5 pm)
under dim light by using infra-red light (=880 nm) to limit animal
disturbance. Recordings were performed by using an X-Y driven Leitz MZ12
binocular microscope (Oberkochen, Germany) equipped with a B/W Ikegami camera
(CDD Camera, ICD42B; Maywood, USA). Data were displayed on a Sony TV monitor
(HR Trinitron PVM 1453MD; Tokyo, Japan). They could be either analysed on line
and/or, stored on a JVC tape recorder (S-VHS, HRS75000MS; Tokyo, Japan) or a
Panasonic tape recorder (VHS, NV/SD45; Osaka, Japan). As animals were mostly
moving, no attempt was made to use any automatic frequency counting
device.
Experimental procedure
One week before experimentation started (the systematic acclimation period
before any experiment), myodocops were transferred to an experimental
micro-aquarium (Fig. 1A,B;
volume 1.2 ml; L, 20 mm; W, 3 mm; H, 20 mm; water renewal rate 60-100 µl
min-1). It was hand-made with a microscopic slide fixed by using
SYLGARD (Dow Corning, Michigan, USA) on a laboratory made thermostated glass
plate (10x6x0.5 cm). It was equipped with muddy sand and
phytodetritus from the Bay of Arcachon to mimic a `natural-like' environment
in which animals could move freely, dig and hide. This aquarium was part of a
1 l closed re-circulatory system with constant entry and exit levels. It was
set at 10±0.1°C for all experiments by means of a
laboratory-constructed thermoelectric device. During experiments,
PO2 varied from 2-40 kPa (27-540 µmol
l-1 or 0.9-17.3 mg l-1). The CO2 partial
pressure (PCO2) was maintained at 0.1 kPa, a
value typical of water PCO2 in air-equilibrated
environments. The gas mixtures bubbled through the reservoir of seawater
feeding bottles, which was connected to the aquarium by means of glass tubes
to avoid gas leaks. The N2/O2/CO2 gas mixture
was obtained via mass flow controllers (Tylan General, model FC-260;
San Diego, CA, USA) driven by a laboratory-constructed programmable control
unit.
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Different subtypes of experiments were performed at 10°C in this set-up: analysis of reference ventilatory pattern in normoxia; ventilatory and cardiac responses to 2-15 h exposure periods at various O2 partial pressures ranging from 40 to 2 kPa; respiratory adaptation to 3 day exposure periods at 4 kPa.
Short-term adaptation ability at various oxygenation levels
These experiments were done on a group of 12 animals from the Bay of
Arcachon, which was exposed to 10 plateau levels of different water
PO2 presented in the following order: 21
(Reference), 10, 6, 4, 6, 4, 2, 21 (Recovery 1), 40 kPa and 21 kPa (Recovery
2; Fig. 1C). The duration of
exposure for each oxygen level was ranging from 2 to 15 h, with the exception
of the reference normoxic condition that lasted 7 days. Ventilatory
frequencies within ventilatory bouts (min-1) and cardiac
frequencies (min-1) were measured during the last 30 min of
exposure time. Each animal was identified based on location in the aquarium,
size and shell marks to avoid replicate analysis on the same individuals.
Three-day exposure periods at water PO2=21 and 4 kPa
The analysis of reference ventilatory pattern in normoxia (21 kPa, 282
µmol l-1) and 3 day exposure under hypoxia, 4 kPa (53 µmol
l-1), was performed in March 2002 on one group of seven animals.
After acclimation, myodocops were first studied in reference normoxic
conditions (21 kPa) during 3 days in the mini-aquarium, then under hypoxia
during 3 days (PO2=4 kPa, hypoxic test) and
finally in normoxia after 2 days of recovery. When the analysis started, the
experiment consisted of focussing on an individualized specimen and to study
it during a 1 h period. Thus, for each animal, its ventilatory pattern was
described during the reference days 1, 2 or 3 and the test days 4, 5 or 6. For
each animal, the percentage of active ventilation during the studied hour
(hourly duration, %), the mean ventilatory bout duration (min-1),
the bout number (h-1), the ventilatory frequency within bouts
(min-1) and the cardiac frequency (min-1) were
determined. As no significant difference was observed between animals (paired
t-test), all data were pooled together for each water
PO2. Consequently, comparisons were performed
on paired analysis.
Behavioural regulation of organism oxygenation status during the diurnal rhythm
Many myodocops exhibit a clear diurnal activity rhythm (they are active at
night and resting in nests during daytime,
Macquart-Moulin, 1999;
Smith and Horne, 2002
) whereas
the above analyses were essentially performed during daytime. To get more
insights into the organism's oxygenation strategy at various activity levels,
we thus turned to an analysis of (1) activity pattern and (2) oxygenation
status in nests.
Diurnal rhythm of activity in C. mariae
The analysis was performed on 50 specimens of C. mariae (measuring
1.9±0.1 mm) in August 2003, following a 15 day acclimation period in
the laboratory. The temperature in the room was set at 18°C to enhance
oxidative metabolism and oxygen dependency by comparison to the above
experiment that were performed at 10°C. After being collected, animals
were placed in a glass aquarium (10x5x30 cm, Lxlxh)
whose bottom was covered by a natural substrate (sand, mud and phytodetritus;
thickness, 1 cm). The acclimation period was 7 days. The aquarium was exposed
to natural day light cycles and, to permit nocturnal camera recording, an
infrared floodlamp (=870 nm) was added. The floodlamp was facing the
camera (camera Watec WAT-902H equipped with a macro zoom lens, Computar
MLH-10X) to allow animal counting at night and it was continuously switched
on. A total of 10 diurnal activity rhythms were recorded. One picture was
caught per second by driving the videocamera with a PC (software, PVR
Perception player; Enfield, UK). On each picture, the total number of animals
present in the water column was then determined. The activity index we derived
(expressed as arbitrary unit, a.u.) was the number of animals present in the
water column during a 30 min observation period.
Oxygenation status in myodocops nests
To characterize the partial pressure of oxygen into a myodocop nest, 15
C. mariae were placed in a mini-aquarium
(Fig. 1B) during one week. The
aquarium was perfused with normoxic-normocapnic water and
O2-profiles (N=5) were measured with an O2
polarographic microelectrode (UNISENSE Microsensors) driven with a PRIOR
micromanipulator (steps, 0.2 mm). The microelectrode was impaled in the
central part of the nest, close to the animals.
Statistical analysis
Values are reported as mean values ±1 standard error of the mean
(M.E.M.) or 1 standard deviation
(M.D.). Differences were evaluated using a Mann-Whitney
U-test, a two-tailed Student's t-test, a Fisher test and/or
analysis of variance (ANOVA). P<0.05 was taken as the fiducial
limit of significance.
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Results |
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Characterisation of the ventilatory pattern at various PO2 levels
In resting C. mariae, a typical ventilatory pattern in
air-equilibrated water (PO2=21 kPa) was
characterized by spontaneous switch from active ventilation to transient
pauses (Fig. 3). Interestingly,
a continuous ventilatory activity was occasionally observed during at least 1
h periods (2/7 studied animals) and the longer pause we recorded was 8 min.
Note finally, that either scaphognathite could work alone although this was
rarely observed. The mean ventilatory bout number was 3 h-1
(minimum-maximum, 1-8 h-1) and the total ventilatory duration per
hour varied from 31-60 min. During active ventilation periods, called
ventilatory bouts, the mean-recorded ventilatory frequency was 90
min-1 (see Table 1; minimum 30 min-1; maximum 168 min-1). Cardiac pauses
were never observed and the mean cardiac frequency was
40 min-1
(minimum 38 min-1; maximum 54 min-1,
Table 1).
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The existence of ventilatory and/or circulatory regulatory mechanisms was tested by exposing animals to various water oxygenation levels during exposure periods ranging from 2-15 h (Fig. 1C). The result of our experiments is presented in Fig. 4. The striking observation was that, when the frequencies under hypoxic (2<PO2<10 kPa) and hyperoxic (PO2=40 kPa) conditions were compared with normoxia during reference and recovery conditions (PO2=20.5-21.5 kPa,), no change of ventilatory and cardiac frequency could be noticed (Fig. 4 upper panels). Specifically, in hypoxia, no hyperventilatory response was recorded. The relationship between the ventilatory frequency, fR and water PO2 was: fR=0.028 water PO2+96.08 (r2=0.00121, P<0. 76). The relationship between the cardiac frequency, fH, and water PO2 was: fH=0.092 water PO2+54.75 (r2=0.0072, P<0. 89; Fig. 4 lower panels). Note finally that despite a 23 h exposure at PO2<6 kPa, no recovery impairment was discernible. Indeed, this mid-term hypoxic exposure did not lead to any statistical difference between recovery and reference frequencies for both ventilatory (ANOVA, F7,116=0.99, P=0.44) and cardiac (ANOVA, F7,57=1.58, P=0.16) aspects. To reinforce this observation, especially facing hypoxic challenge, we then exposed the Cylindroleberis to water PO2=4 kPa during 3 days and we analysed all characteristics of the corresponding respiratory activity. The results are presented in Table 1. Clearly, the mean number of bouts, bout duration, hourly duration of ventilation and ventilatory frequency within bout per hour did not significantly change as a function PO2 (no different values, paired t-tests). Fig. 5 extends on this theme by comparing the distribution frequencies of these parameters. Without a doubt, both ventilatory patterns were similar. Thus, even during long-term exposure to hypoxia, no significant ventilatory and circulatory adaptability could be observed in C. mariae. Consequently, it strongly suggested that at constant temperature and metabolic level, the PO2 value in their milieu intérieur should vary passively - as a dependent variable - following changes of PO2 in the inspired water.
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Numerous myodocops are reported to emerge at dust from the sediment and
swim in the water column, i.e. in air-equilibrated water. By contrast, during
daytime Cylindroleberids rest in burrows or nests on the sea bottom. To
analyse if this particular diurnal behaviour applies to C. mariae and
whether it participates to a rhythm of tissue oxygenation, we then turned to a
behavioural study of animals free to move in a water column and build nests.
Fig. 6 demonstrates first the
existence of a very marked daily rhythm of activity in this species. It
summarizes the result obtained during 10 daily cycles through a summer season.
Clearly, no specimen (0/50) was recorded in the water column during daytime
while it was only at night that animals were active. At night, maximum
swimming velocities of 20 mm s-1 were recorded, while during
daytime, in the sediment, it was only 0.7 mm s-1 as animals
were mostly inactive in the nests. Fig.
7A1-A4 illustrate the different phases of a nest building. On
Fig. 7A2, a specimen is shown
surrounded by filaments of mucus-like slime and
Fig. 7A3 shows two animals
gliding into a nest. Finally, Fig.
7A4 illustrates the density that can be reached within a nest in
which 15 individuals were observed. Fig.
7B presents an oxygen profile performed during daytime in this
nest. Clearly, the nest water was confined as illustrated by the measurements
of hypoxic PO2 values ranging from 8-10 kPa.
Thus depending on their activity level, Cylindroleberis are either
rebreathing a hypoxic and hypercapnic water in nests when there are resting
during daytime, or breathing a normoxic-normocapnic water, when they are
actively swimming in the water column at night.
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Discussion |
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Comparison with previous data
To date very little data are available concerning respiratory properties
and evolution in early crustaceans and arthropods although the evolution of
their cardiovascular system has been reviewed by Wilkens
(1999). Horseshoe crabs,
Limulus polyphemus, are certainly an exception
(Watson, 1980
;
Mangum and Ricci, 1989
). They
probably existed since the Silurian period (410-440 million years ago) and,
interestingly, as reported here for myodocops, their ventilatory pattern has
also been reported as highly variable. Moreover, an absence of ventilatory
rate change in response to oxygenation changes has been reported
(Mangum and Ricci, 1989
) which
fits quite well with present observation in Cylindroleberis. In
podocopid ostracods (Corbari et al.,
2004
), the ventilatory pattern is also highly variable, but
numerous statistically significant differences exist when bout characteristics
- number, mean, hourly duration and ventilatory frequencies - are directly
compared (see Table 1).
However, a major difference is certainly that one never observed ventilatory
arrest, or apnoea, longer than 8 min in Cylindroleberis while it was
quite frequent in podocopids as they can stop breathing for periods >1 h.
This ability in podocopids could be associated to their activity and metabolic
level. Indeed, the velocity of podocopids in the sediment is slower than in
Cylindroleberis (1-2 mm min-1 vs 40 mm
min-1; podocopid values from
Corbari et al., 2004
). The
ability of Cylindroleberis to build nests was already reported by
Cannon (1933
). He noted that
when a specimen is placed in a dish of clean seawater without any mud, in a
minute or two, it is found to be surrounded by a mass of mucus like slime.
Fage (1933
) reported that
Cylindroleberis can stick together sand particles by using secretory
glands and stay in one centimetre long nests for days or weeks under
laboratory conditions. Finally, Vannier and Abe
(1993
) reported that another
member of the myodocopid ostracod family, the Cypridinidae Vargula
hilgendorfii can also stay within the upper layers in the sediment and
that they also produce some sticky substance that could be a kind of slime.
Thus, in myodocops, nest building appears as a very general behaviour.
Extensive studies on the respiratory physiology in another type of
millimetre-sized crustacean, Daphnia magna, were already performed.
Daphnia are equipped with a cardiovascular system but no ventilatory
plates. They are planktonic filter feeders and ventilate their filtering
chamber with thoracic appendages. In Daphnia, the existence of both
cardiocirculatory (Paul et al.,
1997) and ventilatory responses
(Pirow and Buchen, 2004
) were
reported following changes in water oxygenation levels. In addition, there is
haemoglobin in Daphnia (Kobayashi
and Hoshi, 1984
) and, although Fox
(1957
) reported that it also
occurs in Cypria and Pseudocypris (freshwater ostracods),
the question certainly requires further investigation
(Hourdez et al., 2000
;
Weber and Vinogradov, 2001
).
Again, any explanation about these differences remains highly speculative but
it is worth noting that Daphnia were only reported from the Permian
(250-300 million years ago; Schram,
1982
). Respiratory control mechanisms could have logically evolved
from Cambrian to Permian.
The respiratory control system in ostracods
In ostracods, the rhythmic movement of the scaphognathites is controlled by
four muscles innervated by nerves originating from the circumoesophageal
ganglia (Hartmann, 1967).
Although of primitive aspect by comparison to decapod crustaceans, the central
nervous system is already well-differentiated as a cerebrum, a
circumoesophageal ring, a chain of ventral ganglia and a network of motor
nerves connecting to various muscles were described
(Rome, 1947
;
Hartmann, 1967
). Remarkably,
in present decapods, the scaphognathite beating movement is fairly similar to
what is observed in myodocops (present data) and podocops
(Corbari et al., 2004
). In
crabs like Carcinus maenas, these movements are driven by a set of
five levator and five depressor muscles
(Young, 1975
), innervated by
motor neurones arising from a central pattern generator (CPG;
Simmers and Bush, 1980
). By
analogy, this strongly suggests that a respiratory CPG also exists in
myodocops (Harris-Warrick et al.,
1992
; Marder and Bucher,
2001
). Indeed, there is now considerable evidence from a variety
of different invertebrates that the motor patterns underlying rhythmic
behaviour are essentially determined by CPG within the central nervous system
(Harris-Warrick et al., 1992
;
Marder and Bucher, 2001
). This
would be coherent with the demonstration that the heartbeat in Vargula
hilgendorfii is neurogenic and driven by a CPG located in a cardiac
ganglion. Interestingly, the Vargula cardiac CPG is composed of a
single neuron (Ando et al.,
2001
; Ishii and Yamagishi,
2002
) when in many decapods, it is composed of nine neurons. It
illustrates the level of complexity that could be expected for an early
ventilatory CPG.
Ventilatory pattern and evolution of central nervous mechanisms controlling ventilatory activity in crustaceans
In ostracods, the ventilated water flows backwards, i.e. from the anterior
to the posterior aspects of the animals. Remarkably, in present decapod
Crustaceans, the predominant mode is opposite: the scaphognathites draw water
forwards via openings located at the base of the walking limbs and
chelae and expel it through the hydrostomes, that are excurrent openings
located on the anterior part, below antennae. Occasionally, the system
reversed the direction of ventilatory currents and water is inhaled
via the anterior aspect
(Arudpragasam and Naylor, 1964;
Hughes et al., 1969
). Backward
pumping (alternatively called, reversals) were only reported to be a
predominant mode (1), in the crabs Corystes cassivelaunus, which
normally live buried in sand (Arudpragasam
and Naylor, 1966
) and (2) in the shore crabs C. maenas,
which, when exposed to progressive hypoxia in shallow water, partially emerge
into air and aerate their branchial cavities by reversing the direction of
their irrigation (Taylor et al.,
1973
). Simmers and Bush
(1983
) studied the neuronal
basis of bimodal beating in Carcinus. They reported that a single
pattern-generating network produces the motor programmes appropriate for both
forward and backward beating. Switching between beating modes originates from
selective inputs, which either inhibit one or the other pattern.
Thus, in decapods, a single ventilatory CPG produces two different motor
patterns (forward and backward) when in ostracods, the backward motor pattern
is the only observed ventilatory mode. What could be the origin of such an
apparent divergence? Is it the result of evolution? Decapods have a fossil
record dating back to the Permian (286-245 millionyears ago;
Benton, 1993) when ostracods
are dated from the early Paleozoic (400-500 million years ago). We propose
then that the backward ventilatory pattern could have preceded the forward
pattern. In Carcinus, Arudpragasam and Naylor
(1964
) shows that during
backward flow, water only irrigates the upper surface of the posterior gills,
which is evidently of limited efficiency. On the contrary, during forward
flow, water irrigates most of the gill lamellae. Finally and importantly, when
crustaceans are facing hypoxic challenges, an increase of forward flow is the
major adaptation to maintain the oxygen consumption and blood oxygenation
status (Taylor, 1982
;
McMahon, 2001
). The above
observations could then explain why to our knowledge no large crustacean is
currently relying on backward ventilatory activity: in large crustaceans
facing an hypoxic stress or an increased O2-demand, forward flow is
of higher adaptative value as it allows a better gill ventilation efficiency
than the backward flow. Regarding C. cassivelaunus
(Arudpragasam and Naylor,
1966
), which appears as an exception in this scheme, one must keep
in mind that it is normally living in sand. The causal explanation for their
extensive use of a backward mode is likely that a forward flowing current
could carry sand into their gill chambers.
To summarize, following the above hypothesis regarding the genesis of ventilatory motor pattern generation in crustaceans, we propose that the backward ventilatory mode should be considered as the early ventilatory mode and the forward mode, as a more recent acquisition, appearing later during evolution. It certainly allowed an increased O2-uptake ability and, thus, possibly facilitated the evolution of larger animals. In this view, the backward mode should be considered as a vestigial motor pattern in decapods, having an accessory role in gill chamber cleaning.
The strategy of tissue oxygenation in Cylindroleberids
In the present report we show an absence of ventilatory and circulatory
adaptation ability facing water oxygenation changes
(Fig. 4). Nevertheless, the
demonstration of a different positioning, depending on the level of activity
strongly suggests that Cylindroleberids adjust their tissue oxygenation level
at set values. Indeed, this observation recalls previously described behaviour
in the crayfish Astacus leptodactylus during the circadian rhythm of
activity (Sakakibara et al.,
1987; Forgue et al.,
2001
) as well as numerous data on metabolic modulation by
O2 and CO2 (Busa and
Nucitelli, 1984
; Hochachka and
Somero, 1984
; Malan,
1993
; Guppy and Withers,
1999
; St-Pierre et al.,
2000
). In A. leptodactylus, it has been shown that
changes of activity at night compared with daytime are associated with changes
in arterial blood PO2 and
PCO2. These changes are performed by
ventilatory adjustments that ensure the autonomous homeostasis of the internal
milieu, in terms of O2
(Massabuau et al., 1984
) as
well as to the blood and tissue acid-base balance regulation. In
Cylindroleberids, the ability of ventilatory adjustments obviously did not
exist, but a social behaviour could play this role on the blood and tissue gas
composition as the water PO2 in a nest is
hypoxic and the water PCO2 must be hypercapnic,
due to rebreathing in a confined space
(Fig. 7). Interestingly, when
the crayfish A. leptodactylus
(Forgue et al., 2001
) is
experimentally exposed to a water PO2 of 10 kPa
(remember that the measured value in the Cylindroleberid nest was very close,
8 kPa) during a 24 h exposure period, it remains inactive and stops exhibiting
a circadian rhythm of activity. By analogy, this depression effect in the
crayfish, is thus a first indication that the oxygenation status found in the
Cylindroleberid nests could participate to the shaping of a resting behaviour
and that, in this way, these animals do possess an
O2-chemosensitivity. In Crustacea, the existence of three types of
hypoxia-induced metabolic rate depressions were proposed
(Forgue et al., 2001
). The
first one is an environmentally induced `deep' hypoxia during which the water
PO2 is so low (
3-4 kPa), that the
gas-exchange processes are limited and the resting O2-consumption
cannot be maintained. It imposes a strict limit to the oxidative metabolism
and forces its depression. Under these conditions, which we suggest are
extreme, any increase of activity relies on anaerobiosis. The second type is
observed in `mild' hypoxic environments (water
PO2
6-10 kPa). Under these conditions, the
animals spontaneously limit their activity in a medium in which excessive
exercise could become O2-limited. Finally, the third type is a
behaviourally self-imposed blood hypoxia by hypoventilation, which allows a
limited O2-metabolism even in normoxic or hyperoxic environments.
In the crayfish, it limits the aerobic scope at rest during daytime and forms
part of the normal physiological repertoire of the animal comportment. Forgue
et al. (2001
) demonstrated
that it did not limit the global animal's oxidative metabolism but typically
the locomotor muscle O2-consumption. It has been proposed to
participate to the shaping of the resting behaviour of crayfish via
direct action on the locomotor muscles themselves. We demonstrate in this
report that, contrary to decapods, the ostracods are unable to control
directly the oxygenation status of their internal milieu as they cannot adjust
their ventilatory activity according to PO2
(see Fig. 4). We suggest that
the behaviour of Cylindroleberids breathing in the confined environment of a
nest (as reported here) corresponds to a strategy of metabolic depression that
underpins the daytime Cylindroleberid resting behaviour.
As stated above, in Astacus leptodactylus, a circadian rhythm of
acid-base balance in the internal environment was reported
(Sakakibara et al., 1987). The
animal's blood is hypercapnic during daytime when animals are resting, and
hypocapnic at night when animals are active. Arguments in favour of a role of
pH in changing the activity of metabolic pathways were largely developed and
it is agreed that acidification is associated with a lowering of metabolic
rate while alkalinisation is linked to its enhancement
(Busa and Nucitelli, 1984
;
Bickler, 1986
;
Malan, 1993
). In addition,
Malan (1985
) proposed that
changing blood PCO2 is a fast and economical
means to change cellular acid-base balance and Forgue et al.
(2001
) reported that
increasing PCO2 favours metabolic depression in
the locomotor muscle of the crayfish. Thus, the modulation of metabolic
activity by O2 and CO2 has been extensively studied. The
mechanisms described above offer a guideline strongly suggesting that in
Cylindroleberids, and possibly in other myodocopid ostracods, self-imposed
changes of water gas composition could contribute to the shaping of the
diurnal behaviour rhythm. These physiological mechanisms should depress their
metabolic activity during daytime and help them to reach a kind of torpor.
In conclusion, Cylindroleberids are unable to regulate the oxygenation
status in their internal environment autonomously by respiratory adjustments.
They build nests in which they are resting during daytime, certainly to
protect themselves against predators, but an additional consequence is that
they are breathing under hypoxic and hypercapnic conditions. By contrast, when
they are active in the water column, they inspire in a normoxic and
normocapnic environment. The net result is that they experience changes in
respiratory conditions, which are similar to what have been extensively
described in the literature on metabolic modulation by O2 and
CO2. Consequently, Cylindroleberids are early crustaceans
illustrating a remarkable stasis since the Paleozoic, both in morphological
(Siveter et al., 2003) and
physiological terms (present data). Indeed, we illustrate here how a single
basic set of principles of respiratory physiology could apply to the behaviour
and life history of an animal that has existed over an impressive time
scale.
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Acknowledgments |
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References |
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