Journal of Experimental Marine Biology and Ecology,
239 (1999) 259–272
L
Habitat-related differences in the responses to oxygen
deficiencies in Idotea baltica and Idotea emarginata
(Isopoda, Crustacea)
Ralf-Achim H. Vetter*, Heinz-Dieter Franke, Friedrich Buchholz
Biologische Anstalt Helgoland, Meeresstation, P.O. Box 180, D-27483 Helgoland, Germany
Received 5 August 1998; received in revised form 20 March 1999; accepted 23 March 1999
Abstract
Two apparently ecologically similar sublittoral isopod species, Idotea baltica and Idotea
emarginata, were studied with respect to their abilities to cope with deficiencies in environmental
oxygen concentration. In a first series of experiments, respiration rates of both species were
measured, at different temperatures (5, 10, 158C), as a function of oxygen partial pressure.
Whereas I. baltica showed the characteristics of an oxyconformer, I. emarginata regulates oxygen
consumption from normoxia down to distinct hypoxic conditions. In a second series of
experiments, anoxia survival times (LD 50 ) were determined for different types of individuals of
both species (mancas, juveniles, adult females, adult males). In both species, survival times
increased with developmental stage. Adult males were more resistant to anoxia than adult females.
In all types of individuals, the LD 50 values of I. emarginata were significantly higher than those of
I. baltica. The interspecific differences are clearly adaptive, correlating with respective habitat
differences. Idotea baltica is associated with seaweed drifting at the water surface where oxygen is
in the normoxic range. In contrast, I. emarginata lives among accumulations of macroalgal debris
on the seabed where hypoxia is common. The different abilities of the species to sustain periods of
hypoxia may contribute to the maintenance of habitat segregation.  1999 Elsevier Science B.V.
All rights reserved.
Keywords: Habitat-related adaptations; Hypoxia tolerance; Idotea; Marine isopods; Oxygen
consumption
1. Introduction
The ecologically very similar sublittoral isopod species, Idotea emarginata (Fabr.) and
*Corresponding author. Tel.: 149-472-581-9326; fax: 149-472-581-9369.
E-mail address: [email protected] (R.-A.H. Vetter)
0022-0981 / 99 / $ – see front matter  1999 Elsevier Science B.V. All rights reserved.
PII: S0022-0981( 99 )00049-0
260
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
Idotea baltica (Pallas), live associated with macroalgae which provide them with both
food and shelter (Naylor, 1955a). In areas where the species co-occur (e.g. Helgoland,
and other localities of the North and Irish Sea), they are largely separated by (micro-)habitat (Franke and Janke, 1998; Naylor, 1955a,b; Tully and O’Ceidigh, 1986). Idotea
baltica occurs predominantly among drift seaweed at the water surface, whereas I.
emarginata is found mostly on the seabed (6–20 m), at localities where large amounts of
broken decaying macroalgae accumulate, brought along with tidal and other currents.
This habitat is characterized by periods of temporary hypoxia.
Among the possible factors maintaining habitat segregation, are habitat selection and
interspecific competition. Habitat selection experiments indicated, however, that both I.
emarginata and I. baltica prefer the same habitat, namely the seabed, which is typical of
the former (Franke and Janke, in preparation). It is intense interspecific interference
competition, with I. emarginata being the superior competitor, which causes habitat
segregation, excluding I. baltica from zones of potential overlap (Franke and Janke,
1998). Therefore, habitat segregation of the species does not reflect ecological
differences with respect to resource utilization, but in contrary results from extreme
ecological similarity, which makes coexistence in the same micro-habitat impossible.
The habitats typically occupied by I. emarginata and I. baltica, when in competition,
differ in a number of important factors. This raises the question whether and to what
extent habitat differences are already reflected by differences in physiological, behavioural and / or other characters of these relatively ‘young’ species. Two habitat
differences are particularly obvious: (1) The habitat of I. emarginata is permanent, with
food usually not becoming limiting due to a continuous supply. Drift seaweed, in
contrast, represents an ephemeral microhabitat. Food becomes rapidly limiting, and
animals have to search repeatedly for new habitats and food. (2) In their habitats, the
species experience different conditions of oxygen supply. Among drift seaweed at the
water surface, oxygen levels are in the normoxic or even supersaturated range and
probably never limiting. Among accumulations of decaying organic material on the
seabed, however, ambient oxygen concentrations may decrease considerably, at least
temporarily in the summer, due to high microbial activity.
Habitat-related physiological adaptations to oxygen supply have been described for
numerous species (for review see Vernberg, 1972, 1983). Respective differences in
hypoxia tolerance among species have been invoked occasionally as a relevant factor
controlling distributional patterns, e.g. in Palaemon species (Berglund and Bengtsson,
1981), in haustoriid amphipods (Grant, 1981), and in cirolanid isopods (Bally, 1987).
The aim of the present study was to look for possible habitat-related differences in the
abilities of I. emarginata and I. baltica to cope with conditions of hypoxia, and to reveal
whether such differences contribute substantially to maintaining the distributional
patterns of the species observed.
2. Material and methods
2.1. Origin of specimens
All experimental animals were taken from flow-through laboratory mass cultures
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
261
(original material from Helgoland). In these cultures, the animals are maintained
separated by species, under identical conditions (nearly ambient seawater temperature,
ambient photoperiod, diet consisting of brown algae and occasional supply with dead
fish). The experiments were performed during summer, when the temperatures in the
mass cultures were at 15–178C. Prior to the respiration experiments the isopods were
starved for 24 h.
2.2. Oxystat system
Oxygen consumption was measured at constant oxygen partial pressures (PO 2 ) in a
thermostated, feedback-controlled system, known as mono-phase oxystat system (Noll et
al., 1986; Eriksen and Iversen, 1997; Stumpe and Schrader, 1997). The measurements
were performed at three different temperatures (5, 10 and 158C), reflecting the range of
temperature which sublittoral animals normally experience over the annual cycle at
Helgoland (Radach and Bohle-Carbonell, 1990). Regulation of PO 2 occurred in the
following way: The actual PO 2 in the chamber was measured with an unshielded micro
electrode, type MT-1-ACS (Eschweiler, Kiel). The value was transmitted to a PO 2
¨
¨
monitor (designed by Baum & Muller,
Dusseldorf)
which read the sensor signal and
compared it with the preselected value. As long as the actual PO 2 was below the
preselected value, the monitor activated a titrator, type TTT 80 (Radiometer,
Copenhagen) which controlled the flow rate of a 10-ml auto-burette ABU 80 (Radiometer) pumping oxygen-saturated seawater from a reservoir into the respiration chamber.
As soon as the PO 2 reached the preselected value, the burette stopped. This regulation
mechanism kept the PO 2 in the respirometer in a steady state close to the preselected
value. Actual PO 2 and burette activity were simultaneously recorded on a BD-112
two-channel recorder (Kipp and Zonen, Solingen).
For a single experimental series, approximately seven adult specimens of both sexes
in a representative mixture of size (15–25 mm in length, ¯ 1 g in total) were placed in
the 0.67-l respiration chamber. A perspex bottom-plate with perforations of 2 mm in
diameter prevented the isopods from constant swimming. At each temperature, three
independent experimental series were run. The measurements were started at normoxic
PO 2 after at least 1 h of acclimation, and were continued for at least 3 h. Then, without
removing the specimens from the chamber, lower PO 2 values were preselected.
Accordingly, the burette stopped pumping oxygenated water, and the PO 2 values in the
chamber gradually declined due to respiration of the isopods. The new steady state was
usually achieved after 1–2 h of acclimation at 158C (up to 5 h at 5 and 108C). Then,
oxygen consumption was measured for at least 3 h at each selected PO 2 . After the final
of a series (measurement at the lowest PO 2 ), the specimens were immediately deepfrozen and the fresh weight of the frozen sample was determined.
Oxygen consumption was calculated from the amount of oxygenated water added per
minute (flow rate (F ), expressed as ml per min) and the difference in the oxygen
concentration between respiration chamber ([O 2 ] C ) and reservoir ([O 2 ] R ). The weight
specific oxygen consumption (MO 2 ) was calculated per gram tissue (W ) after the
formula
F ? ([O 2 ] R 2 [O 2 ] C
MO 2 5 ]]]]]]
W
262
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
The flow rate was determined from the cycle time used by the burette to pump one
volume of 10 ml. The analysis was limited to those cycles where the PO 2 in the
respirometer and the pumping rate of the burette were constant for the whole cycle time
according to the chart recording. Each calculated MO 2 value was averaged from usually
20 of those cycles resulting in mean6S.D. at each PO 2 as given in the graphs. Increased
S.D. values at high consumption rates are due to shorter cycle times thus resulting in
higher relative errors of the measurement.
For each temperature, a regression line of PO 2 dependent MO 2 was calculated based
on all values of the three separate experimental series. Values which showed deviations
from the calculated regression line of more than 4*S.D. were marked as outliers and
were not included in regression according to Sachs (1984). The results were compared
(F-test) for best fit to the non-linear (MO 2 5 A*(PO 2 )C 1 B) and linear regression
(MO 2 5 A*PO 2 1 B). The statistical program (Prism V2.01, GraphPad, San Diego, CA,
USA) selected the equation of linear regression as best fit unless the more complicated
relationship fitted significantly better at p,0.03. A comparable MO 2 value was
calculated for all data sets from the regression at PO 2 515 kPa. In addition, linear
regression was performed on values of the range, in which I. emarginata proved to
regulate oxygen consumption (PO 2 .5 kPa). All regression analyses were performed
with Prism V2.01 (GraphPad, San Diego, CA, USA).
2.3. Anoxia tolerance
Anoxia experiments were conducted at 158C. Four types of individuals of each species
were tested separately: mancas I (about 2 mm in length, 2–5 days old), juveniles (6–8
mm, 5–6 weeks), adult (marsupial) females (16–18 mm, 15–16 weeks), and adult males
(20–25 mm, 15–16 weeks). 25 specimens each (same species and type) were incubated
in 100-ml Winkler flasks with filtered natural seawater (32‰) from which all oxygen
had been removed by nitrogenation for half an hour. Incubation caused a short period
(2–3 min) of highly increased swimming activity; then the animals came to rest on the
bottom of the flasks. After a defined period of anoxia, the animals were released from
the flasks into aerated seawater to allow for recovery. Specimens which regained full
mobility within 30 min were considered survivors. Preliminary tests had shown that
animals which did not recover completely within 30 min, never did so. Animals in open
flasks with air saturated seawater served as controls.
The experiments were performed on 8 successive days. Every day 120 flasks were
prepared, all stocked with animals of the same type and species (e.g. mancas I of I.
baltica). Every 30 min, five flasks were opened to release the experimental animals
(n5125). Maximum incubation time was 12 h. Experiments on a certain type of
individual were carried out within two successive days each.
From the experimental data, sigmoidal (Boltzmann) survival rate (SR) curves were
calculated iteratively (Prism V2.01; GraphPad, San Diego, CA, USA) following the
formula
100
SR 5 ]]]]
LD 50 2t
]]]
1 1 e inclination
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
263
with LD 50 representing the point of time when mortality reached 50%, and ‘inclination’
representing the negative reciprocal value of the slope of the curve at LD 50 . Differences
in LD 50 and inclination values between I. baltica and I. emarginata of the same type of
individuals, as well as between the different types of individuals of the same species,
were analysed for statistical significance with the alternate (Welch) t-test assuming
Gaussian populations with different S.D. values (InStat 2.05; GraphPad).
3. Results
3.1. Oxygen consumption
The dependence of oxygen consumption on oxygen partial pressure (PO 2 ) was
different in I. baltica and I. emarginata. In I. baltica, oxygen consumption always
decreased linearly when PO 2 was experimentally reduced, regardless of temperature
(Fig. 1a–c). The slopes of the linear regression were significantly different at each
temperature and differed also from zero (Table 1). In contrast, respiration rates in I.
emarginata were found to be less dependent on PO 2 . At all temperatures, a non-linear
curve provided the best fit (Table 2). Oxygen consumption was at a rather constant level
from the normoxic range down to distinct hypoxia, and decreased at lower oxygen
concentrations (Fig. 1d–f). In order to qualify the reduced dependency of oxygen
consumption on PO 2 , we reanalysed those data only with PO 2 .5 kPa. This was due to
the findings that below this value even in I. emarginata oxygen consumption dropped
with decreasing PO 2 . In I. emarginata, linear regression of the data in the hypoxic range
(PO 2 .5 kPa) resulted in slopes which were not significantly different from each other.
Additionally, at 5 and 158C the slopes were not significantly different from zero (Table
2).
In I. emarginata, oxygen consumption clearly depended on temperature; it was
highest (for all PO 2 ) at 158C and decreased from 10 to 58C (Fig. 1d–f). At 15 kPa, MO 2
values increased from 5 to 108C and 158C by a factor of 2.5 and 3.1, respectively (Table
2). The situation in I. baltica was different, in that oxygen uptake did not change
considerably with temperature (Table 1, Fig. 1a–c).
3.2. Anoxia tolerance
No significant mortality (,5%) occurred in controls of both I. emarginata and I.
baltica. In contrast, after 12 h of anoxia, only some adult males of I. emarginata
survived (SR522.5%). Individuals of all experimental groups survived in oxygen-free
medium for some period of time. However, significant differences were evident between
the species as well as among the different types of individuals. For all these types
(mancas, juveniles, adult females, and adult males), the survival rate curves of I.
emarginata were shifted to the right compared to those of I. baltica (Fig. 2).
Consequently, LD 50 values calculated from these curves were always higher in I.
emarginata, with statistical significance ( p ,0.0001; Fig. 3). In addition, the absolute
values of inclination were usually higher in I. emarginata (Table 3).
264
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
Fig. 1. Oxygen consumption (nmol O 2 per g fresh weight and min) as a function of oxygen partial pressure
(PO 2 ), in Idotea baltica (left, a–c) and Idotea emarginata (right, d–f), at different temperatures (5, 10, and
158C). Each experimental series is represented by a special symbol. Data marked by asterisks (d) were not
included in regression analysis. When S.D. (see explanation in the Material and Methods section) are not
shown, they are smaller than symbol size.
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
265
Table 1
Linear regression parameters of the PO 2 -dependent oxygen consumption rates (MO 2 ) of Idotea baltica with
MO 2 5 A*PO 2 1 B (n5number of data, r5regression coefficient.)
58C
108C
158C
All values
A
B
r2
p
n
Calculated MO 2 at 15 kPa
30.73
98.60
0.87
,0.001
20
557
24.51
142.5
0.63
,0.001
19
501
41.42
90.43
0.66
,0.001
17
713
Values a with PO 2 .5 kPa
A
B
r2
n
Slope: deviation from zero?
31.67
81.70
0.80
17
Significant
14.30
278.5
0.30
16
Significant
40.77
96.40
0.54
14
Significant
a
a
Top: all values included in the linear regression; bottom: only values of weak hypoxia (with PO 2 .5 kPa)
were included in the calculation. The differences among the slopes of all temperatures are significant
( p50.047).
Survival times of both species depended, in exactly the same way, on the stage of
development: The more advanced the developmental stage, the higher the LD 50 values.
In adults, females had lower LD 50 values than males (Fig. 3). All differences were
statistically significant at p ,0.0001. In addition, the absolute values of inclination
Table 2
Non-linear (top) and linear (bottom) regression parameters of the PO 2 -dependent oxygen consumption rates
(MO 2 ) of Idotea emarginata
58C
108C
158C
All values
A
B
C
r2
p
n
Calculated MO 2 at 15 kPa
129.1
0.306
21.928
0.63
,0.001
19
293
366.5
0.250
22.619
0.44
,0.001
25
719
516.9
0.207
9.823
0.58
,0.001
26
916
Values a with PO 2 .5 kPa
A
B
r2
n
Slope: deviation from zero?
6.73
189.2
0.15
13
Not significant
21.72
412.7
0.34
15
Significant
12.41
728.6
0.08
18
Not significant
a
a
Top: all values included in the non-linear regression with MO 2 5 A*(PO 2 ) C 1 B (n5number of data,
r5regression coefficient). Bottom: only values of weak hypoxia (with PO 2 .5 kPa) were included in the linear
regression with MO 2 5 A*PO 2 1 B (n5number of data, r5regression coefficient.). The differences among the
slopes (of linear regression) of all temperatures are not significant.
266
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
Fig. 2. Survival rates as a function of the time period of anoxic incubation, for mancas, juveniles, adult
females, and adult males of Idotea baltica (j) and Idotea emarginata (s).
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
267
Fig. 3. LD 50 values of anoxic incubation for different types of individuals of Idotea baltica and Idotea
emarginata. Data (LD 50 6S.E.) were calculated iteratively from survival rates (n525). *** Significant
differences with p ,0.0001 between species.
increased in both species from mancas through juveniles to adults (Table 3). I. baltica
adult males and females did not differ with respect to the inclination values, whereas the
inclination value of I. emarginata males was almost twice as high as that of females
(Table 3).
4. Discussion
In the open sea, the concentration of dissolved oxygen is generally not a limiting
factor. However, oxygen deficiencies may occur (permanently or temporarily) at
locations where circulation is low and an abundance of organic material results in a high
rate of oxygen utilisation through bacterial activity. At rocky coasts large amounts of
broken seaweed are continuously thrown up the coast line but also accumulate at certain
localities on the seabed. Accumulations of macroalgal debris on the seabed are attractive
habitats to a number of animal species, providing, through tidal and other currents, a
steady supply of food.
In laboratory experiments, both Idotea emarginata and Idotea baltica preferred this
type of habitat (Franke and Janke, in preparation), although in natural areas where the
species occur sympatrically, they are largely separated by habitat. I. baltica is found
typically among seaweeds floating on the water surface, whereas I. emarginata is the
typical species among decaying macroalgae on the seabed (Naylor, 1955a; Jones, 1974).
Table 3
Values and standard errors of inclination (negative reciprocal slope at t5LD 50 ) calculated iteratively from the
survival rates of mancas, juveniles, adult males, and adult females of Idotea baltica and Idotea emarginata
I. baltica
I. emarginata
Mancas
Juveniles
Adult females
Adult males
20.2860.01
20.5660.04
20.4460.01
20.6860.06
21.0260.09
20.9560.05
21.0160.05
22.1860.17
268
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
It is thus I. emarginata which dominates the habitat preferred by both species. Actual
interspecific competition with I. emarginata being the dominant competitor is probably
important to the maintenance of habitat segregation and thus to the coexistence of the
species on a larger spatial scale (Franke and Janke, 1998). Other factors, of course, may
be relevant as well. Among decaying organic material, animals probably experience, at
least temporarily, conditions of hypoxia (Wieser, 1962). Differences in the species’
abilities to withstand periods of oxygen deficiencies thus might interfere with distributional patterns of the species.
Examples of physiological adaptations to hypoxic habitats are numerous (Vernberg,
1972). There is usually a close relationship between an animal’s capacity to tolerate
conditions of reduced oxygen availability, and the range of oxygen partial pressures that
is typical of its habitat. Species inhabiting well aerated waters may not be expected to
exhibit special physiological adaptations to sustained low oxygen environments. In
contrast, species living where hypoxic conditions are common are likely to have adapted
to this situation with an increased tolerance to hypoxia. The shore crab Carcinus maenas
lives in a variety of habitats where hypoxic conditions frequently occur. C. maenas can
regulate its oxygen consumption down to a critical value below which the energy
demand cannot be ensured by aerobic metabolism alone (Taylor, 1976). In contrast,
Pachygrapsus crassipes, lives in a strict normoxic environment and neither regulates its
respiration rate nor shows any significant lactate production (Burke, 1979). The
burrowing crabs Callianassa californiensis and Upogebia pugettensis are both oxyregulators. However, C. californiensis, which is more affected by hypoxia, has the lower
critical PO 2 and is more tolerant of anoxia (Thomson and Pritchard, 1969). In addition,
the hypoxia tolerant isopod Natatolana borealis also shows a low critical PO 2 (Taylor
and Moore, 1995). In the xanthid crabs Panopeus herbstii and Menippe mercenaria, and
the blue crab Callinectis sapidus, oxygen consumption drops with ambient oxygen
partial pressure. The xanthid crabs are more often associated with muddy habitats and,
correspondingly, the decrease in oxygen uptake was found to be less pronounced in
these species than in the blue crab (Leffler, 1973).
The limited ability of organisms to regulate oxygen uptake and to withstand hypoxia
can be one factor determining distributional patterns. Haustoriid amphipod species, for
instance, show a vertical zonation pattern in sediments with species in the deeper,
hypoxic layers showing significantly greater anoxia tolerance than species living in the
upper, oxidised layers (Sameoto, 1969; Grant, 1981). Furthermore, differences in
hypoxia tolerance are mainly responsible for differences in distributional patterns of
closely related marine crustacea, such as the amphipods Echinogammarus pirloti and E.
obtusatus (Agnew and Taylor, 1985), and the prawns Palaemon adspersus and P. squilla
(Berglund and Bengtsson, 1981).
The present study of I. emarginata and I. baltica was designed to look for differences
between the species’ capabilities to cope with oxygen deficiencies, which might reflect
habitat differences. It was not intended to give, for each species, a precise analysis of the
respective physiological characteristics and their dependence on individual parameters.
As previously shown, oxygen consumption and hypoxia tolerance of these isopods
depend on a large variety of factors such as stage in the life cycle, body size, (Strong
and Daborn, 1979), sex, acclimation, food, temperature, stage in the moult cycle
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
269
(Vernberg, 1972), and the tidal cycle (Wieser, 1962). The present experiments on
oxygen uptake were performed with experimental groups with a representative mixture
of individuals with different sizes and both sexes. With respect to the stage in the moult
cycle, however, the groups were composed at random. This procedure might account for
a certain amount of variation in the data. The relatively high values of absolute oxygen
consumption compared to results from measurements in closed systems (i.e. Strong and
Daborn, 1979) can be explained by the higher activity of the specimen in the larger
flow-through respirometer used in our experiments. A comparison of the results obtained
in open and closed systems will be discussed in an additional paper. Anoxia experiments
did not allow for acclimation and thus represent a somewhat artificial condition.
Our results indicate pertinent differences between the species. I. baltica showed no
ability to regulate its oxygen consumption rate when environmental oxygen content
decreased (Fig. 1a–c). I. emarginata, however, maintained at all temperatures a
relatively constant or only slight decreasing rate of oxygen uptake over a wide range of
oxygen tensions from normoxia down to severe hypoxia (Fig. 1d–f). Therefore, there is
more evidence of regulation in I. emarginata than in I. baltica. In addition, oxygen
consumption in I. emarginata increased continuously with temperature. This effect was
not evident in I. baltica, where respiration rates were very similar at 5 and 108C, and
only increased at 158C. Details of respiratory responses to temperature and their
biological significance will be dealt with in a separate paper.
Respiration rates are usually altered by changes in temperature in such a way that the
rate decreases when temperature drops (as to crustacea, see Vernberg, 1983). Respiration
in I. emarginata clearly showed this type of temperature dependence. At all PO 2 values,
oxygen consumption increased with temperature. The response of I. baltica to declining
temperature was different, in that the respiration rate at 58C was higher than at 108C.
Such a deviation from the general pattern has also been described for various intertidal
species, indicating a homeostatic mechanism in poikilotherms which allows the rates of
metabolic reactions to proceed at a relatively constant rate (Newell, 1979).
Mortality in our anoxia experiments was clearly due to the lack of oxygen, since
survival rates in controls did not decrease significantly within the experimental period. In
both species, anoxia tolerance clearly increased ontogenetically (Fig. 2). This result
conforms to expectation, since early developmental stages have a lower storage capacity
of fuels as well as a higher rate of relative basal metabolism due to smaller body size. As
previously shown for isopods, weight specific oxygen consumption decreases with body
weight (Bulnheim, 1974). Accordingly, the higher survival rate of adult males compared
to females, evident in both I. baltica and I. emarginata, might be also due to differences
in body size (males 20–25 mm, females 16–18 mm). Apart from these similarities,
anoxia experiments showed a number of significant differences between the two species.
First, for all types of individuals studied (mancas, juveniles, adult females, and adult
males), tolerance of anoxia was always higher in I. emarginata, with statistical
significance ( p ,0.0001). Furthermore, the interspecific differences of LD 50 values
increased from mancas over juveniles and adult females to adult males (Fig. 3). Second,
survival rate curves at LD 50 were usually steeper (smaller absolute values of inclination)
in I. baltica (Table 3).
In I. baltica and I. emarginata, nothing is known presently of the physiological
270
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
mechanisms underlying the interspecific differences demonstrated above. Possible
mechanisms known from other crustaceans to explain different regulatory abilities with
respect to oxygen consumption under varying oxygen partial pressures include (a)
variation in heart rate (e.g. Taylor and Butler, 1973), (b) differences in hemocyanin
composition and saturation (e.g. Taylor, 1976; Mangum, 1980), and (c) modulation of
hemocyanin oxygen affinity by numerous effectors (e.g. Bridges and Morris, 1986;
Morris and Bridges, 1986). Differences in anoxia tolerances, however, might be due to
glycolytic rate depression by covalent modification of key regulatory enzymes (e.g.
phosphofructokinase, pyruvate kinase) via reversible enzyme phosphorylation (e.g.
Storey, 1994) or by decreased levels of enzyme activators such as fructose-2,6bisphosphate (e.g. Storey, 1988).
The adaptive nature of the interspecific differences in the responses to decreasing
oxygen availability, and in anoxia tolerance, is obvious. The differences clearly correlate
with the conditions of the habitats the species are typically found in. I. emarginata and I.
baltica compete for the same permanent habitat (broken decaying seaweed on the
seabed) where oxygen deficiencies may develop at times. In the presence of I.
emarginata, however, I. baltica is excluded from this habitat, probably due to direct
interference with the superior competitor I. emarginata. (Franke and Janke, 1998).
Competition with I. emarginata confines I. baltica to living among surface drift weed
where the species normally does not encounter hypoxia. In addition to direct competitive
interference, the ability to withstand periods of hypoxia might be relevant to distributional patterns. As demonstrated above, I. emarginata appears to be better adapted
than its congener to living among decaying seaweed. If oxygen concentration drops, the
conditions will become more rapidly unfavourable to I. baltica than to I. emarginata.
While I. baltica has to leave the habitat in order to escape environmental hypoxia,
special physiological adaptations allow I. emarginata to stay in this habitat as a more
permanent resident. This may confer an additional advantage to I. emarginata in
competition for an attractive habitat.
Acknowledgements
Special thanks are due to Professor Dr M. Grieshaber for generously making available
his oxystat system. We are also grateful to M. Janke and K. Grau for technical assistance
and to Dr L. Franklin for correcting the English. This project was partly supported by
the BMBF grant no. 03F0153A / 18.
References
Agnew, D.J., Taylor, A.C., 1985. The effect of oxygen tension on the physiology and distribution of
Echinogammarus pirloti (Sexton and Spooner) and E. obtusatus (Dahl) (Crustacea: Amphipoda). J. Exp.
Mar. Biol. Ecol. 87, 169–190.
Bally, R., 1987. Respiration of three isopods from different intertidal zones on exposed sandy beaches of the
west coast of South Africa (Flabellifera, Cirolanidae). Comp. Biochem. Physiol. 87A, 899–905.
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
271
Berglund, A., Bengtsson, J., 1981. Biotic and abiotic factors determining the distribution of two prawn species:
Palaemon adspersus and P. squilla. Oecologia 49, 300–304.
Bridges, C.R., Morris, S., 1986. Modulation of haemocyanin oxygen affinity by L-lactate: a role for other
cofactors. In: Lintzen, B. (Ed.), Invertebrate Oxygen Carriers, Springer, Berlin, pp. 341–352.
Bulnheim, H.-P., 1974. Respiratory metabolism of Idotea balthica (Crustacea, Isopoda) in relation to
¨
environmental variables, acclimation process and moulting. Helgolander
Wiss. Meeresunters. 26, 464–480.
Burke, E.M., 1979. Aerobic and anaerobic metabolism activity and hypoxia in two species of intertidal crabs.
Biol. Bull. 156, 157–168.
Eriksen, N.T., Iversen, J.J.L., 1997. On-line determination of respiration rates of aquatic organisms in a
mono-phase oxystat at steady-state dissolved oxygen tensions. Mar. Biol. 128, 181–189.
Franke, H.-D., Janke, M., 1998. Mechanisms and consequences of intra- and interspecific interference
competition in Idotea baltica (Pallas) and Idotea emarginata (Fabricius) (Crustacea: Isopoda): A laboratory
study of possible proximate causes of habitat segregation. J. Exp. Mar. Biol. Ecol. 227, 1–21.
Grant, J., 1981. Factors affecting the occurrence of intertidal amphipods in reducing sediments. J. Exp. Mar.
Biol. Ecol. 49, 203–216.
Jones, M.B., 1974. Survival and oxygen consumption in various salinities of three species of Idotea
(Crustacea, Isopoda) from different habitats. Comp. Biochem. Physiol. 48A, 501–506.
Leffler, C.W., 1973. Metabolic rate in relation to body size and environmental oxygen concentration in two
species of xanthid crabs. Comp. Biochem. Physiol. 44A, 1047–1052.
Mangum, C.P., 1980. Respiratory function of the hemocyanins. Am. Zool. 20, 19–38.
Morris, S., Bridges, C.R., 1986. Novel non-lactate cofactors of haemocyanin oxygen affinity in crustaceans. In:
Lintzen, B. (Ed.), Invertebrate Oxygen Carriers, Springer, Berlin, pp. 353–356.
Naylor, E., 1955a. The ecological distribution of British species of Idotea (Isopoda). J. Anim. Ecol. 24,
255–269.
Naylor, E., 1955b. The life cycle of the isopod Idotea emarginata (Fabricius). J. Anim. Ecol. 24, 270–281.
Newell, R.C., 1979. Biology of Intertidal Animals, 3nd ed, Marine Ecological Surveys Ltd, Faversham, Kent,
UK.
Noll, T., deGroot, H., Wissemann, P., 1986. A computer supported oxystat system maintaining steady-state O 2
partial pressures and simultaneously monitoring O 2 uptake in biological systems. Biochem. J. 236,
765–769.
Radach, G., Bohle-Carbonell, M., 1990. Strukturuntersuchungen der meteorologischen, hydrographischen.
¨
Nahrstoffund Phytoplankton-Langzeitreihen in der Deutschen Bucht bei Helgoland. Ber. Biol. Anst.
Helgoland 7, 1–425.
Sachs, L., 1984. Angewandte Statistik, 6th ed, Springer, Berlin.
Sameoto, D.D., 1969. Physiological tolerances and behavior responses of five species of Haustoriidae
(Amphipoda: Crustacea) to five environmental factors. J. Fish. Res. Bd Can. 26, 2283–2298.
Storey, K.B., 1988. Suspended animation: The molecular basis of metabolic depression. Can. J. Zool. 66,
124–132.
Storey, K.B., 1994. Analysis of enzyme regulation via reversible phosphorylation and enzyme binding
interactions with macromolecules. In: Hochachka, P.W., Mommsen, T.P. (Eds.), Biochemistry and Molecular
Biology of Fishes, Vol. 3, Elsevier, Amsterdam, pp. 603–614.
Strong, K.W., Daborn, G.R., 1979. Growth and energy utilisation of the intertidal isopod Idotea baltica (Pallas)
(Crustacea: Isopoda) J. Exp. Mar. Biol. Ecol. 41, 101–123.
Stumpe, T., Schrader, J., 1997. Phosphorylation potential, adenosine formation and critical PO 2 in stimulated
rat cardiomyocytes. Am. J. Physiol. 273, H756–H766.
Taylor, A.C., 1976. The respiratory responses of Carcinus maenas to declining oxygen tension. J. Exp. Biol.
65, 309–322.
Taylor, A.C., Moore, P.G., 1995. The burrows and physiological adaptations to a burrowing lifestyle of
Natatolana borealis (Isopopda: Cirolanidae). Mar. Biol. 123, 805–814.
Taylor, E.W., Butler, P.J., 1973. The behaviour and physiological responses of the shore crab Carcinus maenas
during changes in environmental oxygen tension. Neth. J. Sea Res. 7, 496–505.
Thomson, R.K., Pritchard, A.W., 1969. Respiratory adaptations of two burrowing crustaceans, Callianassa
californiensis and Upogebia pugettensis (Decapoda, Thalassinidea). Biol. Bull. 136, 274–287.
272
R.-A.H. Vetter et al. / J. Exp. Mar. Biol. Ecol. 239 (1999) 259 – 272
Tully, O., O’Ceidigh, P., 1986. The ecology of Idotea species (Isopoda) and Gammarus locusta (Amphipoda)
on surface driftweed in Galway Bay (West of Ireland). J. Mar. Biol. Assoc. UK 66, 931–942.
Vernberg, F.J., 1972. Dissolved gases-animals. In: Kinne, O. (Ed.), Marine Ecology, Vol. I, Wiley-Interscience,
New York, pp. 1491–1526, part 3.
Vernberg, F.J., 1983. Respiratory adaptations. In: Vernberg, F.J., Vernberg, W.B. (Eds.), The Biology of
Crustacea, Vol. 8, Academic Press, New York, pp. 1–42.
Wieser, W., 1962. Adaptations of two intertidal isopods. I. Respiration and feeding in Naesa bidentata (Adams)
(Sphaeromatidae). J. Mar. Biol. Assoc. UK 42, 665–682.