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Trophodynamics of Salps in the Atlantic Southern Ocean

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Trophodynamics of Salps in the Atlantic Southern Ocean TROPHODYNAMICS OF SALPS IN THE ATLANTIC SOUTHERN OCEAN DISSERTATION zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) am Fachbereich 2 (Biologie/Chemie) der Universität Bremen LENA VON HARBOU Bremen, Dezember 2009 1. Gutachter: Prof. Dr. U. Bathmann, Alfred Wegener Institut, Bremerhaven 2. Gutachter: Prof. Dr. W. Hagen, Universität Bremen Diese Arbeit ist gewidmet meiner Großmutter Eva Zimen. Auch wenn ich ihre Begeisterung für die Humangenetik nicht „geerbt“ habe, hat sie mich trotzdem begleitet, all die Jahre, vor und nach meiner Polarsternfahrt. “We issue a call to ecologist to consider all avenues of inquiry, whether those avenues require a laboratory coat, a computer, or a pair of boots.” Drake et al. (1996) A short introduction Salps are often considered as “gelatinous zooplankton” and thus grouped with ctenophores, cnidarians, or chaetognaths, all characterised by their delicate body tissues containing high percentages of water. The salp’s transparent, barrel shaped body makes them easily confounded with gelatine when clogging fishing nets or beaching as slimy mats. In fact, when asked what animals I am studying, I often had to explain: “I study salps; they look like small jellies but are not jellies.” “And what are they?” “They are urochordates, a group of their own, but closely related to the vertebrates. I’m studying mainly two species of salps in Antarctic waters and especially what they are eating” – a point, where most questions found their end, but some of the questioners where eager enough to ask why on earth I might study such unknown creatures at the end of the world… Table of contents Table of contents Summary........................................................................................................................... 1 Zusammenfassung ............................................................................................................ 4 1 General Introduction...................................................................................................... 7 1.1 Salps and their Relatives: “From Genomes to Aquatic Invasions”................ 7 1.3 The salp’s feeding mode............................................................................... 17 1.4 The Southern Ocean: A hostile feeding ground?.......................................... 22 1.5 Salps in the Southern Ocean......................................................................... 25 1.6 Aims, questions and outline of this thesis .................................................... 27 2 Studies ......................................................................................................................... 31 Declaration on the contribution of each study............................................................. 31 Study I ............................................................................................................................ 33 The salp Salpa thompsoni in an iron fertilised diatom bloom in the Southern Ocean Polar Frontal Zone in late austral summer: I. Demographic response ............................ Study II ........................................................................................................................... 85 The salp Salpa thompsoni in an iron fertilised diatom bloom in the Southern Ocean Polar Frontal Zone in late austral summer: II. Feeding Dynamics.................................. Study III........................................................................................................................ 149 Pelagic tunicates in the Lazarev Sea, Southern Ocean.................................................... Study IV........................................................................................................................ 191 Seasonal feeding dynamics of salps in the Lazarev Sea, Southern Ocean...................... Study V......................................................................................................................... 253 Pelagic tunicates in the Lazarev Sea, Southern Ocean: Biochemical composition......... 3 Synoptic discussion .................................................................................................. 275 3.1 Feeding dynamics of Salpa thompsoni and Ihlea racovitzai or “Is less more”? ........................................................................................................ 276 3.2 Will salps invade Antarctica and oust krill populations? ........................... 283 3.3 General aspects of salp blooms .................................................................. 285 3.4 Deep populations: Seeding populations?.................................................... 287 4 Perspectives for future research................................................................................. 288 4.1 Feeding dynamics of salps.......................................................................... 288 4.2 The particles export mediated by Southern Ocean salps............................ 290 4.3 Thermophysiological limits of salps .......................................................... 291 5 References ................................................................................................................. 292 Appendix ...................................................................................................................... 300 Eidesstattliche Erklärung Summary Summary This thesis focusses on effects of the food regime on the feeding dynamics, bio- elemental composition and community structure of the two Southern Ocean salps Salpa thompsoni (FOXTON 1961) and Ihlea racovitzai (VAN BENEDEN 1913). Emphasis is also put on ecological impacts of the salp feeding. The feeding behaviour of S. thompsoni in response to a fast developing diatom bloom was studied during a mesoscale iron fertilisation experiment in the Southern Ocean Polar Frontal zone by means of incubation experiments. Results of this study confirmed high individual ingestion and egestion rates for this species observed in previous studies (e.g. Pakhomov et al. 2002). Yet, a previously reported direct harm of the salp’s feeding mechanism through phytoplankton concentrations of >1.5 μg chl-a L-1 was rejected by this study. Accordingly, in situ gut pigment contents of S. thompsoni sampled in the iron-induced phytoplankton bloom were significantly higher than those of individuals in the non-fertilised area. Nevertheless, the enhanced ingestion did not generally result in a higher food uptake by the salps. Detailed gut pigment and fatty acid analyses of the salps’ gut contents and biomass revealed a low degradation efficiency of the diatom rich food inside the bloom. Smaller salps (<30 mm body length) that constituted the majority of the late summer population had no benefit from the increasing food concentrations in the bloom situation as inferred from carbon budgets of estimated ingestion and egestion rates. Apparently, only large salps (>30 mm body length, including aggregate and solitary generation) profited from the higher food supply in the fertilised area and showed slightly higher assimilation rates than large salps outside the bloom area. Seasonal feeding dynamics of Salpa thompsoni and Ihlea racovitzai were investigated during three surveys in the Lazarev Sea in summer, fall, and winter to examine the salps’ year-round feeding activity in the upper epipelagic zone of the Antarctic Ocean. High individual feeding rates were determined for both species. Pigment concentrations in the salp guts of both species revealed significant positive correlation to ambient surface chlorophyll concentrations. Gut chlorophyll concentrations had a much smaller range than ambient chl-a concentrations, i.e. salps were able to highly concentrate ingested material in low food environments. Fatty acid analyses revealed a high 1 Summary contribution of flagellates to the diet of both salp species throughout the year. The proportion of diatoms in the diet was lower, but did not decrease in winter for I. racovitzai. This finding reveals active feeding on phytoplankton throughout the year by this species. In comparison, the winter feeding activity of solitary I. racovitzai was significantly higher than that of S. thompsoni. However, there was no major seasonal effect on bioelemental composition of both salps. Apparently, salps do not use lipid reserves or body tissues as energy supply in low food situations. The high Antarctic salp I. racovitzai has a three times higher protein and slightly higher lipid content per dry mass than S. thompsoni. The population structure and demographic development of Salpa thompsoni was intenvsively studied during the iron fertilisation experiment. In summer and fall, S. thompsoni is dominated by the aggregate stage as seen in previous studies. This sexual aggregate stage showed a faster maturation at high feeding conditions inside the phytoplankton bloom. Apparently, maturing S. thompsoni were capable of channelling the energy gain of the higher food supply in an enhanced reproduction. In earlier studies, an effect of high food conditions on reproduction was only observed for the asexual stage of S. thompsoni. This study points to an opportunistic nature of S. thompsoni in both generations. Even in the relatively cold Southern Ocean waters, the salp’s reproductive response to variable environmental feeding conditions was fast (i.e. within weeks). On the other hand, in early fall in the Polar Frontal zone, the entire S. thompsoni population showed a
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