Spiders on a treadmill: influence of running activity on metabolic rates in Pardosa lugubris (Araneae, Lycosidae) and Marpissa muscosa (Araneae, Salticidae)
Institute for Zoology, Rheinische Friedrich-Wilhelms-University Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany
e-mail: ankeschmitz{at}uni-bonn.de
Accepted 12 January 2005
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Summary |
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Key words: respiration, tracheal system, book-lungs, Araneae, spider
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Introduction |
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For testing this hypothesis, comparative investigations of wolf and jumping
spiders have been made (Prestwich,
1983a,b
;
Schmitz, 2004
). Spiders of
these two families have similar life styles and, additionally, they possess
well-developed lungs with similar diffusing capacities (Schmitz and Perry,
2001
,
2002
). While wolf spiders only
possess four simple tube tracheae that are restricted to the opisthosoma,
jumping spiders have well-developed tracheae that reach into the prosoma and
provide about 30% additional capacity for diffusive gas exchange via
the walls of the entire tracheal system (Schmitz and Perry,
2001
,
2002
). Looking at the
metabolic rates during maximum exercise, differences between wolf and jumping
spiders are striking: Prestwich
(1983b
) found greater aerobic
scopes, shorter recovery periods and smaller anaerobic dependence after
maximum activity in a jumping spider (Phidippus audax) compared with
a wolf spider (Lycosa lenta). Looking at the jumping spider
Marpissa muscosa and the wolf spider Pardosa lugubris, the
maximum mass-specific CO2 release and the factorial scopes during
and after maximum activity were greater while recovery periods were shorter in
the well-tracheated jumping spider
(Schmitz, 2004
).
Thus previous studies are consistent with the hypothesis that tracheated
spiders have greater aerobic capabilities during exercise. Conversely,
tracheae of jumping spiders do not directly supply the prosomal muscles
(Schmitz and Perry, 2000). The
direct oxygen supply via terminal diffusion from the tracheal endings
into the muscles, which would be the most effective pathway, is therefore not
possible (Schmitz and Perry,
2000
). Thus, tracheae could increase oxygen delivery to the
muscles only by gas exchange over the walls of the entire tracheal system and
via an oxygen transport by the haemolymph. But in jumping spiders
most tracheae run bundled through the petiolus into the prosoma where they
mostly end in the nervous system and the gut epithelium. This reduces the
lateral diffusing capacity of the entire tracheal system (diffusive
conductance of the tracheal walls) by about 20%
(Schmitz and Perry, 2001
). For
these reasons, the role of the tracheae of jumping spiders in gas exchange
during exercise is still unclear and it can be hypothesized that tracheae
alone are not responsible for the greater aerobic capabilities in this spider
group. This hypothesis was tested in the present study by measuring the
CO2 release of M. muscosa and P.
lugubris during constant running on a treadmill and under selective
elimination of respiratory organs. The elimination of the tracheae or of one
lung by sealing in comparison with intact animals should reveal the role of
tracheae and lungs in gas exchange during physical exercise in differently
tracheated spiders.
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Materials and methods |
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Respirometry treadmill
An open-flow system was used to measure rates of CO2 release
during activity on a miniature airtight custom-made treadmill. Animals moved
in the horizontal plane in an experimental chamber that was an upright
oriented cylinder of about 3 cm3. At the bottom of the chamber, an
axle-driven rubber treadmill belt was moved by a step-less motor support,
which could vary the speed of the treadmill between 0 and 8 cm
s1. Outside air was pumped through the system with a flow
rate of 100 ml min1, adjusted by an Aalborg flow meter
(Orangenburg, NY, USA). The air initially passed through a series of
containers filled with NaOH and a Soda lime scrubbing column to remove both
CO2 and water. Air was then rehydrated by a saturated NaCl solution
to 60% r.h., passed through the reference chamber of the gas analyser and the
animal chamber, and was finally drawn into the CO2-analyser (URAS
14, ABB; ABB Process Industries GmbH, Frankfurt, Germany). The CO2
analyser interfaced with a PC for data-acquisition; the sampling rate was 1
sample per second.
CO2 (mass
specific CO2 release per time) was calculated from fractional
concentrations of CO2 entering (FI) and leaving
(FE) the animal chamber using the equation (from
Withers, 1977
):
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Animals were tested at a constant temperature of 20°C at three different speeds. As P. lugubris has longer legs than M. muscosa, these speeds differed between the species. The lowest speed was that speed at which animals just walked in a constant manner (fast walking; 1.45 cm s1 in P. lugubris and 1.0 cm s1 in M. muscosa). The medium speed was a slow running (2.3 and 1.8 cm s1, respectively). The highest speed was the maximum speed that animals could sustain for at least five minutes (fast running; 3.35 and 2.5 cm s1, respectively). The final speed of each run was adjusted within the first 10 s of the experiment. Animals were watched during the entire run and the treadmill was stopped as soon as the animal stopped and tried to hold fast to any part of the animal chamber.
All experiments started with the lowest speed and ended with the highest one, to accustom animals to the treadmill and to the enforced running. Between the runs at least 2 h ofrecovery were inserted. Individuals were tested with unimpaired respiratory organs (intact animals) and if possible the same animals were tested with eliminated tracheae or with one eliminated lung. As not all animals could be tested in all states, the numbers of tested animals were not the same for all measurements (Tables 1, 2, 3, Figs 3, 4, 5). The single spiracle of the tracheal system or one of the both spiracles of the lungs was sealed the day before the experiment. We used the rubber cement Fixogum (© Marabu; GmbH & Co. KG, Tamm, Germany) for sealing, which could be removed after the experiment without injuring the animals. Animals were first anesthetised with CO2 and then fixed to a soft plate with strips of plasticine. After animals were awake and the respiratory organs were allowed to refill with fresh air, the respective spiracles were glued, after which animals were released. Some animals were tested twice with intact respiratory organs to test for individual differences between different days.
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The steady state
CO2 (nmol
s1 g1) during treadmill running was
calculated from the individual CO2 release traces. It was
determined as mean value of the recorded data in periods when CO2
release did no longer increase or decrease. Minimal costs of transport
(Cmin, nmol cm1 g1) were
determined by regression of the steady state CO2 release during
treadmill running to the speed and by calculating the mean slope of all
individual regression lines. The costs of transport (COT, nmol
cm1 g1) were calculated from the steady
state values divided by the speed. As not all animals reached steady state
CO2 release at all speeds, another evaluation with the data was
carried out that calculates the CO2 release per distance (nmol
cm1 g1) and the metabolic rate
(
CO2, nmol
s1 g1) using the amount of CO2
released during the period of running. Differences between animal groups were
tested using ANCOVA statistics.
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Results |
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Sealing of both lung spiracles in P. lugubris, and of both lung spiracles and of the tracheal spiracle in M. muscosa, caused the death of the animal within less than 1 h. M. muscosa lived for at least 1 day with sealed lung spiracles when animals were in rest, but died within hours when animals were enforced to move. Sealing of one lung and the tracheae in M. muscosa caused the animals to show only very short and inconstant runs on the treadmill so that these experiments were not incorporated in the evaluation.
Intact animals of both species mostly started with a burst-like maximum CO2 release, which than decreased to the steady state value or decreased constantly (Figs 1, 2, Table 1). Sealing of one lung decreased the maximum values by more than 30% in P. lugubris and eliminated the initial peaks, while in M. muscosa the effect was slightly smaller with one lung sealed and only remarkable at the highest speed when the tracheae were blocked (Table 1).
At the lowest speed, most individuals of intact P. lugubris
reached a steady state
CO2 (nmol
s1 g1)
(Fig. 1A, Table 1). But when one lung
spiracle was sealed, CO2 release values were in steady state or
slightly decreased over the running time
(Fig. 1D). At the medium speed,
only 70% and at the highest speed 10% of the tested intact P.
lugubris reached a steady state CO2 release while the other
individuals showed a decreasing
CO2 over the
running time (Fig. 1B,C,E,F).
M. muscosa normally reached a steady state gas exchange at low and
medium speeds (Fig. 2A,B,
Table 1), and 30% of the
animals also did so at the highest speed. When tracheae were sealed, steady
state was reached by all individuals at the lowest speed
(Fig. 2G), by 70% of the
individuals at the medium speed and by about 20% of the individuals at the
highest speed. Sealing of one lung resulted in steady state or in decreasing
values over the time at the first two speeds
(Fig.
2DF,Table
1).
The steady state
CO2 increased
with the three speeds tested in intact P. lugubris and in intact
M. muscosa (Table 1)
and in M. muscosa with sealed tracheae (ANCOVA, P<0.01).
In M. muscosa with one sealed lung, there was also an increase in
steady state
CO2
between the two lower speeds (ANCOVA, P<0.01). Sealing of one lung
in P. lugubris caused a reduction in steady state
CO2 or a
complete lacking of this feature (Table
1). But in M. muscosa only lung sealing at the medium
speed and tracheal sealing at the highest speed caused a significant reduction
of steady state
CO2
(Table 1).
The minimal costs of transport (Cmin) were calculated from the
steady state values and were determined from 23 speeds depending
whether the individuals reached a steady state at the highest speed
(Table 2). Cmin is
higher in intact M. muscosa compared with P. lugubris
(ANCOVA, P<0.01). Sealing of the tracheae or one lung caused a
reduction of Cmin in M. muscosa, while sealing of the
tracheae in P. lugubris had no effect on Cmin. As steady
state CO2 release did not occur at the two higher speeds,
Cmin was not calculable in P. lugubris with one sealed
lung. The calculated y-intercepts
(Table 2) in all test groups
were 56 times greater than the resting rates, which are 1.8 nmol
s1 g1 in P. lugubris and 1.4 nmol
s1 g1 in M. muscosa (data for
resting rates taken from Schmitz,
2004). The costs of transport (COT, nmol cm1
g1) calculated from the steady state
CO2 decreased
with increasing speed in both species evaluating intact animals
(Fig. 3A,B). COT were greater
in the jumping spider and were influenced by sealing of the respiratory organs
as described before for the steady state
CO2 values.
As not all animals reached steady state CO2 release at all
speeds, another evaluation with the data was carried out that calculates the
CO2 release per distance (nmol cm1
g1) and the
CO2 (nmol
s1 g1) using the amount of CO2
released during the entire period of running. The data are given in Figs
4 and
5. The CO2 release
per distance decreased with increasing speed in both species and in all test
groups with sealed lungs or tracheae. In addition, the values were greater in
M. muscosa in comparison with P. lugubris (ANCOVA,
P<0.01). The calculated
CO2 increased
with the three speeds in intact animals of both species (Figs
4B,
5B), but not in P.
lugubris when one lung was sealed
(Fig. 4D). In M.
muscosa, the
CO2 increased
between the low and the medium speed when one lung or the tracheae were sealed
(Fig. 5D,F). The values for
CO2 release per distance were different at all speeds in P.
lugubris between the intact animals and the animals with the sealed lung
(reduction of 3348%) (Fig.
4A,C). In M. muscosa sealing of one lung reduced the
entire CO2 release for 1438% at all three speeds
(Fig. 5A,C), but sealing of the
tracheae showed only an effect at the highest speed
(Fig. 5A,B,E,F).
Evaluation of the running times and the ON- and OFF-responses revealed differences between the species and between intact and impaired animals (Table 3). The ON-response was calculated for the period from the onset of running until the animal reached half of the maximum CO2 value (ON-I). In addition, a second ON-response was calculated for animals that reached steady state CO2 release and was calculated from the onset of running until the animal reached half of the steady state value (ON-II). The OFF-response was calculated as the period between end of running and the time when animals reached half of the steady state CO2 value. Looking at the interspecific comparison, only the OFF-response was different being shorter in M. muscosa (P<0.01). Sealing of one lung in P. lugubris caused a decrease in running time and an increase in the OFF-response (Fig. 1, Table 3) compared with the intact animals. The ON-response increased in the impaired P. lugubris at the lowest speed but not at the medium and high speed which resulted from the reduced maximum CO2 release and the reduced entire CO2 release at these two speeds. In M. muscosa the same effects can be found when one lung was sealed but as the percentage of difference is smaller in the jumping spider, effects seemed to be weaker than in P. lugubris (Fig. 2, Table 3). Sealing of the tracheae in M. muscosa had no effects on the OFF-response and the running time was only influenced at the highest speed. The ON-response was reduced at the highest speed because of the lower values for steady state and maximum CO2 release (Table 1).
Individual comparisons of intact animals that were tested for two
consecutive days showed differences in steady state
CO2, in COT, in
running times, and in the ON and OFF responses between two runs of ±10%
in both species.
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Discussion |
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In general, spiders rely to a large extent on anaerobic metabolism during
activity (Prestwich,
1983a,b
).
Therefore, if anaerobic metabolism in P. lugubris and in M.
muscosa also occurs, the interpretation of the CO2 release
patterns is complicated by the production of lactic acid and the following
release of CO2 from solution in the haemolymph for buffering the
metabolic acidosis. During running activity, animals will rapidly need more
energy. Especially at the onset of activity, these energy demands might be
extremely high as animals will be more excited and the running performance
will be more erratic than later during activity. The initial CO2
peaks during running activity might therefore be caused by an increasing
CO2 release because of increasing aerobic or anaerobic metabolism
or a combination of both and effects will have different proportions at the
different running speeds tested. The initial peaks differed largely between
the tested individuals, especially in M. muscosa
(Table 1), and without
measuring the lactic acid concentration interpretation of the peaks is
difficult. In the tarantula Eurypelma californicum, the proportion of
CO2 release for buffering after intensive exercise, which causes a
strong metabolic acidosis, is 34% of the total CO2 release
(Paul and Fincke, 1989
).
Values for P. lugubris and M. muscosa will certainly be
lower in the speeds tested in the present paper.
Decreasing CO2 release over the time (e.g.
Fig. 1B,C) might result from a
depletion of fluid-stored CO2 during activity, the course of which
is unknown in spiders, but could also be caused by a decreasing dependence on
anaerobic metabolism secondary to circulatory adaptations. It can be assumed
that in the tested spiders the lowest speed is supported mainly by aerobic
metabolism. But the
CO2 might be
increased by CO2 released from the haemolymph, which is remaining
from the initial anaerobic metabolism. Increasing speeds most probably caused
higher aerobic metabolism, but caused also higher anaerobic contributions to
energy supply. This is supported by the results for the percentage of animals
reaching steady state CO2 release at the different speeds. Steady
state metabolic rates themselves and increasing values with the speed indicate
a great proportion of aerobic metabolism
(Herreid, 1981
;
Shillington and Peterson,
2002
). But tarantulas on a treadmill, performing strenuous
activity, may reach a steady state metabolic rate even with considerable
anaerobic contributions (Herreid,
1981
). Because of the chosen speeds, steady state CO2
release in the present study will presumably result mainly from aerobic
contributions and the calculated COT and Cmin might therefore be
used for the investigation of aerobic capabilities. Conversely, the fact that
not all spiders reached a steady state CO2 release might be a
function of the duration of running
(Herreid, 1981
). Thus it is
possible that if runs would last long enough all animals would reach a low but
steady state CO2 release at the end.
Running on the treadmill under steady state
CO2 caused
factorial scopes of 10 in P. lugubris and of 18 in M.
muscosa (resting rates from Schmitz,
2004
). For other wolf and jumping spiders and also for tarantulas,
aerobic scopes during running were reported to be normally 310
(Miyashita, 1969
;
Seymour and Vinegar, 1973
;
Ford, 1977
;
Humphreys, 1977
;
Herreid, 1981
;
Prestwich, 1983b
;
Shillington and Peterson,
2002
). All reported values higher than 68 are based on
measurements of
CO2, indicating
considerable anaerobic proportions. But, conversely, Shillington and Peterson
(2002
) reported factorial
scopes up to 16 during aerobic running in the tarantula Aphonopelma
anax.
The COT were greater in M. muscosa compared with P.
lugubris, which could be a function of generally improved aerobic
capabilities in the jumping spider. But as shown above, the anaerobic
contributions to the steady state CO2 release are not known in
P. lugubris and in M. muscosa and have to be tested in these
species before final conclusions can be made. Furthermore, the COT declined
with speed in both species. This is true in most other pedestrian
invertebrates and vertebrates, as well, and is a function of the
y-intercept value. For animals with large y-intercepts of
more than two times the resting rate, e.g. the cockroach species
Periplaneta americana and the tarantula Aphonopelma anax
(Herreid, 1981;
Herreid and Full, 1984
;
Full et al., 1990
;
Shillington and Peterson,
2002
), the decline of cost of transport with speed is striking.
Large y-intercepts might be explained by a considerable excitement
and resulting experimental stress, by increasing anaerobic contributions with
increasing speed, by postural costs or a non-linearity between metabolic rate
and speed (Herreid, 1981
;
Berrigan and Lighton,
1994
).
Mass-specific minimal cost of terrestrial locomotion (Cmin) is a
useful value for comparing the metabolic costs of pedestrian locomotion of
animals with different body mass and with different numbers and length of legs
that run at different speeds and have different standard metabolic rates
(Taylor and Heglund, 1982;
Taylor et al., 1982
;
Full, 1987
;
Full et al., 1990
;
Gatten et al., 1992
). In
addition, Cmin can also be used as a unit of measurement for the
comparison of intact and restricted animals with sealed respiratory organs.
Cmin can be predicted for vertebrates and arthropods according to
the equation: Cmin=10.8 M0.31, where
Cmin is in J kg1 m1 and M is in
kg (Full et al., 1990
). The
confidence interval for this equation is quite large so that costs of
transport may vary 6-fold at a given body size and smaller animals with short
legs should have higher metabolic costs per unit mass than larger animals.
This is because of the necessary greater number of steps to travel a given
distance (Full et al., 1990
).
Mass specific prediction for M. muscosa and P. lugubris
(mean body mass 30 mg) would result in a Cmin of 4.05 nmol
CO2 cm1 g1. The determined
values for the intact animals thus fit well with this prediction within the
confidence interval, indicating that body mass, leg length and resulting
metabolic costs coincide with the mean value for running animals.
Cmin is smaller in P. lugubris compared with M.
muscosa which will be a function of the longer legs in the wolf spider
and additionally because of a possible higher anaerobic contribution.
Moreover, the Cmin in spiders can be extremely low when spiders run
at very high speeds and the anaerobic contributions to metabolism are high.
This was found in tarantulas in which the Cmin was only about 15%
of the predicted value (Herreid,
1981
). However, testing the Cmin at aerobic speeds it
fits well in the predicted values, as evaluated for Aphonopelma anax
(Shillington and Peterson,
2002
).
The comparison of the COT with the calculated CO2 release per
distance and of the steady state
CO2 with the
CO2 release per time during the entire activity
(Table 1, Figs
3,
4,
5) reveals very similar values.
This is probably a function of the equalization of the peak CO2
values by the delay in CO2 increase. Thus, calculation of the
entire CO2 release might be useful for the evaluation of metabolism
during running activity and might be used for the determination of anaerobic
contributions in the case that lactic acid concentrations are measured in
forthcoming studies.
The running times decreased with increasing speeds, indicating increasing anaerobic contributions with speed. Running times were about 1015 min at the low and medium speed. Even if there is lactic acid production it is probably not overwhelming in which case clearly shorter activity times would be expected. Running times were longer in P. lugubris, but M. muscosa was often more active after the treadmill experiments. Thus interpretation of this point is difficult as animals stopped running voluntarily and thus in many cases it could hardly be decided whether animals stopped running because of exhaustion or because they did not like to continue running.
Fast ON-responses of CO2 release and peak CO2 values during activity reveal an ongoing circulation during activity, which makes a fast CO2 release possible. Assuming a dominating aerobic metabolism during steady state CO2 release, a short OFF response is a good indicator for a low O2 debt. But considerable anaerobic contribution would result in a depletion of fluid-stored CO2 and thus in a low CO2 release from the animal although O2 consumption is high because of a large O2 debt.
The influence of the elimination of respiratory organs
The elimination of the tracheae in P. lugubris has no influence on
the CO2 release or all other measured parameters, indicating that
tracheae have no influence on the metabolic rate during running. By contrast,
the elimination of one lung caused significant differences in running time,
OFF-response, the COT and the overall CO2 release. Additionally,
the CO2 release did not increase with speed in restricted animals.
Assuming predominate aerobic metabolism at the lowest speed, these results
indicate that the single lung already worked at its limit at the lowest speed
and anaerobic contributions became more important at increasing speeds.
Lacking initial peaks in the first phase of running might be due to the
lacking respiratory surface by blocking one lung. Conversely, as the peak
CO2 values are most probably caused by a combination of increasing
anaerobic and aerobic metabolism in the restricted animals, even if more
CO2 is driven out from he haemolymph, the reduced CO2
production by the reduced lung capacity will reduce the overall CO2
release value.
The morphological oxygen diffusing capacity (diffusive conductance) of both
lungs of P. lugubris is about 10 nmol s1
g1 kPa1
(Schmitz and Perry, 2002).
Thus, using an RQ of 0.7, the calculated steady state
CO2 at the
highest speed is 26 nmol O2 s1
g1 and a
PO2 of 2.6
kPa over the lungs is necessary. Sealing of one lung resulted in maximum
steady state values of 16.6 nmol O2 s1
g1 which needs a
PO2
of 1.7 kPa at the single lung. Heart rate thus should not have been elevated
during running and the O2 deficit can be paid back after a
shortened running and a prolonged recovery period.
In M. muscosa, sealing of one lung resulted in reduced
CO2 and running
times and caused prolonged OFF-responses. For the lowest, presumably mainly
aerobic, speed this would indicate increasing anaerobic proportions. Initial,
but reduced, CO2 peaks often occurred, indicating that the gas
exchange capacity of the tracheae are responsible for these results compared
with P. lugubris. Lungs in the jumping spider, Salticus
scenicus, have an oxygen diffusing capacity of about 9 nmol
s1 g1 kPa1
(Schmitz and Perry, 2001
).
Assuming similar values in M. muscosa, the highest steady state
metabolic rate in intact animals would need a
PO2 of about 4 kPa at the lungs. Sealing
of one lung would result in a necessary
PO2 of 8.7 kPa. But tracheae deliver an
additional oxygen diffusing capacity of about 4 nmol s1
g1 kPa1 via the tracheal walls.
Thus the entire oxygen diffusing capacity of the intact animals is 13 nmol
s1 g1 kPa1 and about 8.5
nmol s1 g1 kPa1 in
animals with one sealed lung. This would result in a
PO2 of 2.8 kPa at the respiratory organs
in intact animals and in animals with one sealed lung at the respective
maximum steady state metabolic rates. The metabolic rates with one sealed lung
therefore can be reached by compensation via the tracheae or
alternatively by an increased heart rate to increase the
PO2 at the lungs.
Sealing of the tracheae in M. muscosa did not influence the
CO2 and the
running time at the low and the medium speed. Thus tracheae seem to be not
involved in gas exchange at low and mean activity and the greater
CO2 of M.
muscosa in comparison with P. lugubris will be independent of
the tracheae. At the highest speed, however, sealed tracheae reduced the
CO2, but values
were still greater than in P. lugubris. Taking into account that the
lungs of both species have similar diffusing capacities, these results
indicate that tracheae only partly support the higher
CO2 in M.
muscosa compared with P. lugubris. Moreover, eliminated
respiratory organs reduced the Cmin in M. muscosa which
indicates higher anaerobic contributions. The effect was greater with one
sealed lung (75% reduction) than with the sealed tracheal system (40%
reduction). Because in one-lunged P. lugubris, Cmin cannot
be calculated at all, this is another hint that tracheae in M.
muscosa can be used for compensation when lung capacity is not
sufficient. But results of Cmin should be interpreted with care, as
in many individuals with sealed spiracles it was calculated only from two
speeds, which might have produced diverging results.
Comparative testing of the maximum activity in wolf and jumping spiders
revealed that the corresponding jumping spider (P. audax, M. muscosa)
showed higher maximum metabolic rates, shorter ON- and OFF-responses and lower
anaerobic contributions than the wolf spider (L. lenta, P. lugubris)
(Prestwich, 1983b;
Schmitz, 2004
). Together with
the data shown in the present paper it can be assumed that the investigated
jumping spiders have greater aerobic capabilities than the respective wolf
spiders, but that tracheae alone are not responsible for these differences.
Tracheae in jumping spiders seem not to change in principal the strategy of
using anaerobic capabilities during fast running in spiders (Prestwich,
1983a
,b
),
but the role of anaerobic metabolism in small spiders, as P. lugubris
and M. muscosa, is still a matter of speculation and should be tested
for a better understanding of the presented results. In addition, also other
factors have to be considered as playing a role in aerobic capabilities. Such
factors are the morphology and physiology of the circulatory system, the
function of the respiratory pigment hemocyanin in the haemolymph, and the
number and density of mitochondria in the exercise muscles that all have not
been investigated to date.
How do tracheae in jumping spiders function during physical exercise?
Tracheae in jumping spiders end in the nervous system, the gut epithelium
or in the haemolymph (Schmitz and Perry,
2000). But 7080% of the tracheal surfaces are in contact
with the haemolymph (Schmitz and Perry,
2001
), in which haemocyanin is available as respiratory protein
(Markl et al., 1986
;
Schmitz and Paul, 2003
). The
gas exchange from the tracheal system to the tissue may therefore function
according to two principles: (1) the principle of lateral diffusion in which
gas exchange takes place via the walls of the entire tracheal system,
(2) the principle of terminal diffusion in which gas exchange takes place at
the distal endings in the haemolymph or in the tissue itself. Jumping spiders
most probably use a mixture of the two principles. Tracheae seem to be not
necessary in maintaining metabolic rates of the exercising muscles during low
and medium activity. But they support the local oxygen supply to the gut,
which should be of no importance during exercise, and to the nervous system,
which is of great importance for the support of the eyes. Jumping spiders have
excellent visual capabilities which are essential during exercise, and could,
in addition, be one reason for the higher metabolic rates in these spiders.
The importance of the tracheae for the eyes is also demonstrated by the
refusal to run constantly on the treadmill when one lung and the tracheae were
sealed. At low and medium activity and when tracheae are sealed, lungs can
provide enough oxygen, also for the eyes, via the haemolymph,
probably supported by an increased engagement of the circulatory system. At
high activity, however, tracheae seem to be necessary for maintaining
metabolic rates and the lacking tracheal capacity can only be partly
compensated by the lungs.
In conclusion, the results of the present paper are consistent with the hypothesis that tracheae partly support the enhanced aerobic capabilities of jumping spiders compared with the two-lunged wolf spiders. Looking at the anatomy, tracheae might be mainly responsible for the local oxygen supply, especially of the nervous system. Physiological results, however, revealed a joint responsibility of the tracheae for the metabolic rates during strong physical exercise, which could be a combination of the needs for muscular activity and for the processing of visual input. Tracheae can fulfil both demands because of the possibilities of gas exchange via the tracheal system, which may function in local oxygen delivery by penetrating organs and by global oxygen delivery by gas exchange via the tracheal walls incorporating the haemolymph in gas transport. Further investigations have to reveal the exact role of aenaerobic metabolism and the role of the circulatory system in maintaining the metabolism during exercise in small araeneomorph spiders.
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Acknowledgments |
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References |
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