Reproductive Trade-Offs in Benthic Decapod Crustaceans of High Southern Latitudes: Tolerante of Cold and Food Limitation

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Reproductive Trade-Offs in Benthic Decapod Crustaceans of High Southern Latitudes: Tolerante of Cold and Food Limitation Reproductive trade-offs in benthic decapod crustaceans of high southern latitudes: tolerante of cold and food limitation Reproduktionsstrategien benthischer Zehnfußkrebs hoher südlicheBreitengrade: Toleranz von Kält und Nahrungsmangel Sven Thatje Ber. Polarforsch. Meeresforsch. 483 (2004) ISSN 1618 - 3193 The most beautiful thing we can experience is the mysterious. It is the source of all true art and science. Albert Einstein Die vorliegende Arbeit ist die kaum verändert Fassung einer kumulativen Dissertation, die in der Sektion "Vergleichende Ökosystemforschung bei Prof. Dr. Wolf E. Arntz angefertigt und dem Fachbereich 2 (BiologieIChemie) der Universitä Bremen im April 2003 vorgelegt wurde. CONTENTS Summary .................................................................................................................... I11 Zusammenfassung ......................................................................................................IV 1 INTRODUCTION ......................................................................................................1 1. 1 DECAPOD CRUSTACEANS IN POLAR AREAS ................................................1 1.2 SYSTEMATICS AND SPECIES STUDIED .........................................................2 1.3 PHYSIOLOGICAL BACKGROUND ....................................................................4 1.4 AIM OF THIS STUDY .........................................................................................4 2 MATERIALS AND METHODS ...................................................................................6 2.1 SAMPLING AND STUDY AREAS ......................................................................6 2.1 .1 Study areas ......................................................................................................6 2.1.2 Plankton sampling ............................................................................................6 2.1.3 Capture and maintenance of ovigerous females ...............................................8 2.1.4 Rearing of larvae ............................................................................................9 22SAMPLE TREATMENT .....................................................................................10 2.2.1 Morphological studies .....................................................................................10 2.2.2 Total lipid content and fatty acid analyses .......................................................10 2.2.3 Protein analyses............................................................................................. 11 2.2.4 Analyses of elemental composition, dry mass (W), carbon (C), hydrogen (H), nitrogen (N).............................................................................. 11 2.3 DATA ANALYSES ............................................................................................12 2.3.1 Cluster analyses .............................................................................................12 2.3.2 Statistics ........................................................................................................12 3 RESULTS AND DISCUSSION .................................................................................14 3.1 PLASTICITY IN CARIDEAN REPRODUCTION: A LATITUDINAL VIEW ............14 3.2 REPTANT DECAPODS IN THE SOUTHERN OCEAN ......................................17 3.2.1 Antarctic reptant decapods: only a myth? .......................................................17 3.2.2 Reproductive modes in Southern Ocean lithodid anomurans ..........................21 3.2.3 Challenging the cold: the return of crabs to the Antarctic? ...............................29 3.3 FUTURE PERSPECTIVES ...............................................................................31 4 PUBLICATIONS ......................................................................................................33 Publication I: Thatje. S., 2003 . Campylonotus arntzianus. a new species of the Campylonotidae (Crustacea: Decapoda: Caridea) from the Scotia Sea (Antarctica) . Polar Biology 26: 242-248............................................................. 36 Publication 11: Thatje. S., Bacardit. R., 2000 . Morphological variability in larval stages of Nauticaris magellanica (A . Milne Edwards. 1891) (Decapoda: Caridea: Hippolytidae) from South American waters. Bulletin of Marine Science 66 (2): 375-398 ........................................................................................................... 43 Publication III: Thatje. S., Bacardit. R., Romero. M.C., Tapella. F., Lovrich. G.A., 2001 . Description and key to the zoeal stages of the Campylonotidae (Decapoda: Caridea) from the Magellan Region. Journal of Crustacean Biology. 21 (2): 492-505 ................................................................................................67 CONTENTS Publication IV: Thatje, S., Lovrich, G.A., Anger, K., 2004. Egg production, hatching rates, and abbreviated larval development of Campylonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea) in subantarctic waters. Journal of Experimental Marine Biology and Ecology DOI 10.1016/J.JEMBE.2003.09.101..................... 81 Publication V: Thatje, S., Lovrich, G.A., Hagen, W., Torres, G., Anger, K., 2004. Changes in biomass, lipid, fatty acid and elemental composition during the abbreviated larval development of the subantarctic shrimp Campylonotus vagans. Journal of Experimental Marine Biology and Ecology D01 10. 1016/J.JEMBE.2003.09.019........................................................................ 94 Publication VI: Thatje, S., Schnack-Schiel, S., Arntz, W.E., 2003. Developmental trade-offs in Subantarctic meroplankton communities and the enigma of low decapod diversity in high southern latitudes. Marine Ecology Progress Series 260: 195-207.................................................................................................. 1 1 0 Publication VII: Lovrich, G.A., Thatje, S., Calcagno, J.A., Anger, K., Kaffenberger, A., 2003. Changes in biomass and chemical composition during lecithotrophic larval development of the Southern king crab Lithodes santolla (Molina). Journal of Experimental Marine Biology and Ecology 288: 65-79 .................... 123 Publication VIII: Anger, K., Thatje, S., Lovrich, G.A., Calcagno, J.A., 2003. Larval and early juvenile development of Paralomis granulosa reared at different temperatures: tolerance of cold and food limitation in a lithodid crab from high latitudes. Marine Ecology Progress Series 253: 243-251 ................................ 138 Publication IX: Thatje, S., Fuentes, V., 2003. First record of anomuran and brachyuran larvae (Crustacea: Decapoda) from Antarctic waters. Polar Biology 26: 279-282 ................................................................................................... I47 5 ACKNOWLEDGEMENTS ......................................................................................151 6 REFERENCES .................................................................................................. .... 153 SUMMARY Caridean shrimps comprise the only decapod infraorder in the markedly impoverished high Antarctic decapod fauna. Their presence, with about a dozen species only, was previously assigned to their capability of down-regulating high haemolymph magnesium ([Mg2+IHL)concentrations at low temperatures. This regulation is missing or insufficient in reptant decapods, affecting in particular their scope of activity. This deficiency has been hypothesised as one important factor explaining their extinction during Antarctic cooling in the Tertiary, as evidenced by the fossil record. The present work demonstrates an ecological adaptation in the early life history of decapods to ecophysiological constraints in the cold, primarily a mismatch between reproductive traits and a marked seasonality of primary production and low temperatures increasing with latitude, It is shown that on a macroecological scale, natant decapods show remarkable plasticity in changing their early life history Patterns with latitude and decreasing water temperature. These changes include, for example, an increase in egg size, hatching of large and advanced larvae and a reduction of fecundity with latitude. Energy saving traits to abbreviate larval developments such as a strong suppression of the number of instars, low metabolic losses in very thin exuviae during fewer moults, and a loss of highly variable developmental pathways compared to lower latitides, are ouserved already in the Subantarctic realm of southernmost America. Early larvae generally present a high resistance to starvation, which in combination with an abbreviated larval development allows for a better synchronisation with peaks in food availability. However, caridean larvae rely on primary production, and the evolutionary step towards complete endotrophic larval development, possibly due to phylogenetic constraint, is almost unknown in marine shrimps. The need for food in planktotrophic and extended larval development of ancestor reptants, and the lacking resistance of larvae to starvation as well as their low tendency of suppressing the number of larval instars, is herein supposed to have selected against Reptantia at high latitudes. However, it is shown that lithodid crabs, which evolved fairly recently about 13 to 25 Ma ago, did develop early life history adaptations to cold environments. Two lithodid crab species from the Subantarctic Magellan region (Lithodes santolla, Paralomis granulosa) developed complete food
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