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Life in cold oceans: activity dependent on extracellular ion regulation? [Elektronische Ressource] = Die Rolle der extrazellulären Ionenregulation in der Kältetoleranz mariner Crustaceen / vorgelegt von Astrid C. Wittmann

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Life in cold oceans: activity dependent on extracellular ion regulation? Die Rolle der extrazellulären Ionenregulation in der Kältetoleranz mariner Crustaceen Dissertation zur Erlangung des akademischen Grades – Dr. rer. nat – dem Fachbereich 2 Biologie/Chemie der Universität Bremen vorgelegt von Astrid C. Wittmann Diplom-Biologin Bremen 2010 Gutachter: 1. Gutachter: Prof. Dr. Hans-Otto Pörtner Alfred-Wegener-Institut für Polar- und Meeresforschung Am Handelshafen 12, 27570 Bremerhaven 2. Gutachter: Prof. Dr. Ulrich Saint-Paul Leibniz-Zentrum für Marine Tropenökologie Fahrenheitstraße 6, 28359 Bremen Prüfer: Dr. Franz J. Sartoris Alfred-Wegener-Institut für Polar- und Meeresforschung Am Handelshafen 12, 27570 Bremerhaven Prüfer: PD Dr. Holger Auel Universität Bremen, Fachbereich 2, Marine Zoologie Leobener Straße NW2, 28359 Bremen Tag des Promotionskolloquiums: 5. November 2010 TABLE OF CONTENTS TABLE OF CONTENTS LIST OF ABBREVIATIONS ....................................................................................................................................II LIST OF FIGURES................................................................................................................................................... III LIST OF TABLES..........................................................

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Publié par
Publié le 01 janvier 2010
Nombre de lectures 20
Langue Deutsch
Poids de l'ouvrage 13 Mo


Life in cold oceans: activity dependent on extracellular ion
regulation?


Die Rolle der extrazellulären Ionenregulation in der
Kältetoleranz mariner Crustaceen



Dissertation
zur Erlangung des akademischen Grades
– Dr. rer. nat –




dem Fachbereich 2 Biologie/Chemie
der Universität Bremen
vorgelegt von


Astrid C. Wittmann
Diplom-Biologin




Bremen 2010









































Gutachter:

1. Gutachter: Prof. Dr. Hans-Otto Pörtner
Alfred-Wegener-Institut für Polar- und Meeresforschung
Am Handelshafen 12, 27570 Bremerhaven


2. Gutachter: Prof. Dr. Ulrich Saint-Paul
Leibniz-Zentrum für Marine Tropenökologie
Fahrenheitstraße 6, 28359 Bremen


Prüfer: Dr. Franz J. Sartoris
Alfred-Wegener-Institut für Polar- und Meeresforschung
Am Handelshafen 12, 27570 Bremerhaven


Prüfer: PD Dr. Holger Auel
Universität Bremen, Fachbereich 2, Marine Zoologie
Leobener Straße NW2, 28359 Bremen


Tag des Promotionskolloquiums: 5. November 2010

TABLE OF CONTENTS

TABLE OF CONTENTS
LIST OF ABBREVIATIONS ....................................................................................................................................II
LIST OF FIGURES................................................................................................................................................... III
LIST OF TABLES......................................................................................................................................................IV
SUMMARY................................................................................................................................................................... V
ZUSAMMENFASSUNG..........................VII
1. INTRODUCTION.................................... 1
1.1. BIOGEOGRAPHY OF CRUSTACEANS AND THE SUB-ANTARCTIC AND ANTARCTIC THERMAL REGIMES............ 1
1.2. TEMPERATURE EFFECTS AND THERMAL TOLERANCE ........................................................................................ 2
1.3. THE MAGNESIUM HYPOTHESIS............................................................................................................................ 4
1.4. ION REGULATION AND THERMAL TOLERANCE ................................................................................................... 6
1.5. ONTOGENY AND THERMAL TOLERANCE............................................................................................................. 8
1.6. KEY QUESTIONS.................................................................................................................................................11
2. MATERIALS AND METHODS ..........................................................................................................................13
2.1. ACQUISITION AND MAINTENANCE OF ANIMALS...............................................................................................13
2.2. HAEMOLYMPH COLLECTION .............................................................................................................................14
2.3. ION CHROMATOGRAPHY.....14
2.4. EXPERIMENTS ON EARLY DEVELOPMENTAL STAGES OF PARALOMIS GRANULOSA...........................................15
2.4.1. CHN contents and dry mass.....................................................................................................................15
2.4.2. Oxygen consumption ................................................................................................................................15
2.4.3. Spontaneous swimming activity of zoeal stages at culture temperatures .............................................16
2.4.4. Activity of zoea I and crab I during acute cold exposure ......................................................................16
2.5. CARDIORESPIRATORY PHYSIOLOGY AND ACTIVITY OF ADULT P. GRANULOSA...............................................18
2.5.1. Preparation of animals and experimental protocol ...............................................................................18
2.5.2. Haemolymph PO .....................................................................................................................................20 2
2.5.3. Righting response......20
2.5.4. Analyses of heart and scaphognathite activity .......................................................................................21
2.6. EXPERIMENTS ON CARCINUS MAENAS ...............................................................................................................21
2.6.1. Spontaneous walking activity, food consumption and extracellular ion regulation ............................21
2.6.2. Cardiorespiratory physiology of C. maenas............22
2.7. STATISTICS.........................22
3. PUBLICATIONS....................................................................................................................................................24
PUBLICATION I..........................................................................................................................................................25
PUBLICATION II ........................................................................................................................................................49
PUBLICATION III ............................................................................................................................82
PUBLICATION IV........................111
4. DISCUSSION ........................................................................................................................................................132
4.1. HOW COLD TOLERANT ARE SUB-ANTARCTIC LITHODID CRABS? ..................................................................132
4.2. WHAT IS THE ROLE OF MAGNESIUM IN COLD TOLERANCE?...........................................................................137
4.3. WHY ARE “REPTANT” DECAPODS NOT PART OF THE ANTARCTIC SHELF FAUNA? ........................................143
4.4. CONCLUSIONS..................................................................................................................................................147
5. REFERENCES....................................150
6. APPENDIX ....................................................................................................................163
6.1. ADDITIONAL RESULTS......163
6.1.1. Effects of season, temperature and magnesium on Carcinus maenas ................................................163
6.1.1.1. Haemolymph ion composition, walking activity and food consumption ...................................................... 163
6.1.1.2. Haemolymph PO , ventilation and heart frequency in response to acute cold exposure ............................. 163 2
6.1.1.3. Seasonal effects on extracellular ion composition of C. maenas? ................................................................. 164
6.2. ADDITIONAL PUBLICATION .............................................................................................................................166
DANKSAGUNG........................................................................................................................................................169
ERKLÄRUNG GEM. § 5 (1) NR. 3 PROMO ......................................................................................................171


List of abbreviations
ASW artificial sea water
2+ASW –Mg artificial sea water with reduced magnesium concentration
-1 -1ßO oxygen solubility (mol L Torr ) 2
bpm beats per minute
CI crab I, first juvenile instar
CII crab II, second juvenile instar
C:N ratio Carbon to nitrogen ratio, is a proxy for the lipid:protein ratio
DW dry weight
frqfrequency
FW fresh weight
-1CO oxygen concentration (mol L ) 2
HLPO haemolymph oxygen partial pressure (kPa) 2
ind individual
M megalopa stage
-1 -1MO oxygen consumption, respiration, metabolic rate (molO h ind ) 2 2
Mya million years ago
n number of individuals
n.d. not determined
NSW natural sea water
2+ 2+NSW +Mg natural sea water of increased [Mg ]
P barometric pressure (Torr) B
PH O water vapour pressure (Torr) 2
Q temperature-velocity relationship, is a measure of thermal sensitivity 10
sc scaphognathite
s.d. standard deviation
s.e.standard error
t time
T temperature
T0 time point directly after hatching of larvae
V volume of the respiration chamber (L)
ZI zoea I, zoeal stage I
ZII zoea II, zoeal stage II
II




List of figures
Figure 1.1: Map of Antarctica and the Southern Ocean. .................................................................... 2
Figure 1.2: Oxygen- and capacity-limited thermal tolerance in ectothermic animals. ................ 4
Figure 1.3: Magnesium hypothesis for the biogeography of marine decapod crustaceans in
the Southern Ocean. .......................................................................................................................... 6
Figure 1.4: Lifecycle of Paralomis granulosa (Jaquinot). .....................................................................10
Figure 2.1: Experimental setup for measurement of temperature-dependent cardiorespiratory
parameters.........................................................................................................................................19
+ 2+ -1Figure 2.2: Na and Mg concentrations (mmol L ) of 4°C-acclimated adult P. granulosa
2+incubated in ASW –Mg ................................................................................................................20
+ 2+ -1Figure 2.3: Na and Mg concentrations (mmol L ) of adult C. maenas incubated in ASW –
2+Mg at 10°C......................................................................................................................................22
Figure 4.1: Thermal tolerance of Paralomis granulosa. .....................................................................136
Figure 4.2: Schematic comparison of hypothesis (A) and results of current study (B). ..........140
Figure 4.3: Change of deep-sea temperature and ice-sheet coverage in the northern and
southern hemispheres in the last 70 My. ..................................................................................146
-1Figure 6.1: Haemolymph ion composition (mmol L ) of Carcinus maenas.................................164
-1 -1Figure 6.2: Spontaneous walking activity (m h ) and food consumption (mg fresh weight )
of Carcinus maenas..........................................................................................................................164
Figure 6.3: Arterial haemolymph PO (kPa), ventilation and heart rates (bpm) of resting 2
Carcinus maenas dependent on temperature and magnesium concentration. ..................165
-1Figure 6.4: Haemolymph concentration of divalent ions (mmol L ) in Carcinus maenas........166
III


List of tables
-1Table 2.1: Ion composition (mmol L ) of incubation media............................................................ 14
Table 2.2: Overview of experiments and of parameters determined in the respective
developmental stages of P. granulosa. ......................................................................................... 17
IV


Summary
It has been hypothesized that the capacity for extracellular ion regulation of marine
crustaceans is a factor that is key in determining their cold tolerance and biogeography in the
Southern Ocean. Groups exhibiting low extracellular magnesium concentrations (e.g.
caridean shrimps, amphipods and isopods) are thought to be more cold tolerant and able to
thrive in extremely cold waters of the Antarctic shelf (-1.8°C). Groups displaying high
extracellular magnesium concentrations (brachyuran and anomuran lithodid crabs) are
constrained to the warmer regions of the sub-Antarctic and Antarctic (> 0°C). This thesis
investigates whether there is a relationship between extracellular ion regulation, activity and
thermal tolerance in a temperate brachyuran crab (Carcinus maenas, Decapoda, Brachyura,
Carcinidae) and in crustaceans from the Southern Ocean. In the sub-Antarctic stone crab
Paralomis granulosa (Decapoda, Anomura, Lithodidae) lecithotrophic larvae as well as
juvenile stages were considered, as thermal tolerance of larval development may strongly
influence the distribution of decapod crustaceans. To test the hypothesis that cold tolerance
is dependent on haemolymph magnesium concentration, haemolymph magnesium
concentration was experimentally altered. Adult specimens were incubated in artificial sea
water with a reduced magnesium concentration similar to a level of that of caridean shrimps
-1(6 mmol L ). Larval P. granulosa did not develop in artificial sea water irrespective of the
magnesium concentration, thus it was only possible to study effects of increased magnesium
-1concentration (97 mmol L ).
Haemolymph ion composition was determined in an array of Antarctic and sub-
Antarctic crustaceans. Antarctic amphipods hyporegulated extracellular magnesium to the
same extent as their temperate counterparts. Antarctic isopods exhibited similarly high
haemolymph magnesium concentrations as the sub-Antarctic lithodids. Therefore, high
haemolymph magnesium concentration does not represent a constraint for isopods to occur
at water temperatures below 0°C.
In early stages of P. granulosa effects of low temperature and increased ambient
magnesium concentration on survival, developmental time, organic (C, H and N)
composition, oxygen consumption, spontaneous and forced activity, heart and ventilation
rates as well as haemolymph ion composition were determined. The results suggest that low
temperature and high magnesium concentration synergistically impede larval survival and
development. The temperature-dependent effect of magnesium was most prominent during
forced swimming activity of the zoea I, but was hardly detectable in the resting juvenile. This
may indicate that highly active larval stages, despite their higher haemolymph magnesium
concentrations, are more susceptible to magnesium than the more advanced life stages.
V


Thermal tolerance at two ambient magnesium concentrations was determined in
adult male specimens of P. granulosa using an acute stepwise temperature protocol. Arterial
and venous haemolymph oxygen partial pressure, heart rate, ventilation rate and
haemolymph cation composition were measured at rest and after a forced activity (righting)
trial. The data suggest that within the experimental time frame neither magnesium
concentration nor oxygen delivery set limits to cold tolerance in the adult stage of P.
granulosa. Significantly increased extracellular potassium concentrations after activity at the
lowest temperatures, may denote difficulties to maintain cellular potassium homeostasis.
Effects of temperature and reduced magnesium concentration on haemolymph ion
composition, spontaneous walking speed and food consumption of the shore crab C. maenas
were studied using a step-wise temperature protocol. Whereas walking speed was not
significantly affected by magnesium concentration, food consumption remained significantly
higher at reduced magnesium concentration than under control conditions at low
temperature. Acute cold exposure and online recording of arterial oxygen partial pressure,
ventilation and heart beat frequency at rest revealed a significant effect of reduced
magnesium concentration on ventilation and heart rates, but this translated only into an
insignificant increase of arterial oxygen partial pressure at low temperatures. There was no
evidence for seasonal effects on haemolymph ion composition in C. maenas. In this study,
besides the change in food consumption, there was no clear indication for an effect of
magnesium concentration on cold tolerance of C. maenas.
As seen in isopods, life in the extremely cold continental shelf areas of the Antarctic is
generally possible despite high haemolymph magnesium concentrations. The most active
first larval stage of P. granulosa seems to be most susceptible to magnesium, but it is doubtful
that the high haemolymph magnesium concentration of this species plays a role in its
geographic distribution. Other decapod crustaceans might however be constrained by low
temperature, if their lifecycle includes planktotrophic larvae with a low capacity for
magnesium regulation.
VI