Prey quantity and quality effects on larval Atlantic herring (Clupea harengus L.) growth in the western Baltic Sea Dissertation with the aim of achieving a doctoral degree at the Faculty of Mathematics, Informatics and Natural Sciences Department of Biology Institute for Hydrobiology and Fisheries science at the University of Hamburg Matthias Paulsen Hamburg, 2016 Supervisors: Prof. Dr. habil. Cornelius Hammer, Thünen-Institute of Baltic Sea Fisheries, Rostock Prof. PhD. Myron A. Peck, University of Hamburg Dr. Catriona Clemmesen-Bockelmann, Helmholtz-Centre for Ocean Research Kiel (GEOMAR) Dissertation evaluation commission: Prof. PhD. Myron A. Peck, University of Hamburg Dr. Catriona Clemmesen-Bockelmann, Helmholtz-Centre for Ocean Research Kiel (GEOMAR) Examination commission: Prof. Dr. Kathrin Dausmann (chair of commission), University of Hamburg Prof. Dr. habil. Cornelius Hammer, Thünen-Institute of Baltic Sea Fisheries, Rostock Prof. PhD. Myron A. Peck, University of Hamburg Prof. Dr. Christian Möllmann, University of Hamburg Date and location of the oral defense: 03.02.2017 Institute for Hydrobiology and Fisheries Science, University of Hamburg Contents Summary 1 Zusammenfassung 5 General introduction and thesis outline 9 Chapter 1: Nutritional situation for larval Atlantic herring (Clupea harengus L.) 35 in two nursery areas in the western Baltic Sea Chapter 2: Food-limited growth of larval Atlantic herring Clupea harengus 65 recurrently observed in a coastal nursery area Chapter 3: Preliminary insights into effects of protozooplankton on growth 95 of spring-hatched herring larvae Chapter 4: Size-dependent growth in larval fish is not an issue in a world 111 of plenty Chapter 5: Spatial variability of larval Atlantic herring (Clupea harengus L.) 117 growth rates in the western Baltic Sea Chapter 6: Effects of the Baltic Sea Index (BSI) on larval herring growth 135 and copepod abundance in the western Baltic Sea General discussion and outlook 151 Declaration on oath 181 Individual scientific contributions 183 Danksagung 185 Summary Recruitment in many marine fish populations is subject to a strong inter-annual variability and larval survival is seen as one of its key drivers. Apart from predation, nutrition constitutes one of the most influential factors on larval survival rates as it determines growth and, hence, influences the duration time that a larva remains in the highly sensitive larval stage. In light of the enduring low recruitment of western Baltic spring spawning herring (WBSSH), the studies conducted in the framework of this thesis aim at providing information about the relation between the nutritional situation and the growth of Atlantic herring larvae in three important nursery areas of the western Baltic Sea (Kiel Canal, Greifswalder Bodden, Kiel Fjord). First, food quantity and its quality in terms of essential fatty acid (EFA) concentrations were analyzed and related to larval growth rates in the Kiel Canal and the Greifswalder Bodden in 2011. The results indicated that both prey quantity and its quality affect larval growth rates. In the study, highest EFA concentrations in the prey were reflected in highest EFA concentrations in the larvae; the latter of which positively correlated with larval growth. Over the course of the season, both habitats provided beneficial and unfavorable growth conditions for the larvae in, however, opposing temporal order. Analyses of a six-year time series of the Kiel Canal revealed a consistent seasonal pattern of prey availability and larval herring growth in this watershed. Larval growth correlated positively with the abundance of the dominant copepod species (Eurytemora affinis), of which highest abundances occurred throughout May. Moreover, by the end of May/ beginning of June, with increasing water temperatures (≥ 15°C) the copepod abundance and subsequently larval growth rates strongly decreased. In contrast, larval growth linearly increased in the Greifswalder Bodden with increasing temperature. The coinciding decline of copepod abundance and larval growth was recurrently observed, which indicates that herring larvae in the Kiel Canal undergo food-limited growth by the end of each spring season. Potential effects of protozooplankton (PZP) biomass on growth of spring-hatched herring larvae were investigated in the Kiel Canal in 2014. No effects of PZP biomass on larval herring growth rates were detected. However, the abundance of copepods – which 1 Summary are known to represent the preferred prey of larval herring – was high during the investigation period. It is therefore possible that PZP is only of minor importance to larval herring, if larger prey items occur at adequate concentrations. Size-dependent larval growth is frequently observed in marine larval fish. In contrast, larval herring growth and size data in combination with seasonal mean zooplankton abundance during a six-year time series from the Kiel Canal revealed a decreasing size-dependency in larval growth with increasing prey abundance. This outcome suggests that size-dependent larval growth may function as an indicator for suboptimal feeding conditions particularly for small larvae. Spatial variability in larval growth was investigated in the Greifswalder Bodden in 2010 and a comparison between seasonal mean growth in the Greifswalder Bodden and the Kiel Canal was conducted between 2010 and 2012. With one exception (large larvae in the channel-like Strelasund area of Greifswalder Bodden), temporal variability was higher than spatial variability in larval growth, both within the Greifswalder Bodden and between habitats. This finding was supported by the results of coastal mesozooplankton surveys which suggested that variability in prey was greater temporally as opposed to spatially. Changes in larval growth and copepod abundance were analyzed in the Kiel Canal (2007-2012), the Kiel Fjord (2007-2012) and the Greifswalder Bodden (2010-2012) with respect to changes in the Baltic Sea Index (BSI), a broadscale, atmospheric climate index. Changes in the winter BSI were unrelated to changes in larval growth rate or copepod abundance. Only a negative trend between the abundance of the copepod Pseudocalanus spp. and the winter BSI existed with decreasing abundance at increasing BSI. Moreover, a highly significant correlation between the growth rates of small larvae (< 14 mm) and the mean seasonal copepod abundance from all investigation areas was observed, whereas this was not found for larger larvae (14 mm – 20 mm). Based on 9 years of data, a significant correlation between WBSSH recruitment and the yearly mean abundance of the copepod Pseudocalanus spp. was found. In the 1990´s, WBSSH recruitment was on average twice as high as between 2000 and 2012. In line with that, peak abundances of copepods and cladocerans were twice as high in 1991- 1995 and 1999 compared to the period thereafter. Weight-at-age 1 did not change over time and was significantly lower compared to same-age conspecifics from the Kattegat/Skagerrak area, independent of recruitment strength. The findings suggest that 2 Summary herring recruitment is close to the carrying capacity of the pelagic ecosystem in the western Baltic Sea. Overall, this thesis provides comprehensive insight into the relationship between food quantity/ food quality and larval Atlantic herring growth. Food quality significantly affected larval growth; however, food quantity appeared to be of paramount importance especially for smaller, less developed larvae. The outcome of the thesis indicates that WBSSH stock recruitment is significantly affected by prey availability, both due to effects on larval growth/survival and density-dependence during the juvenile stage. 3 4 Zusammenfassung Die Rekrutierung von marinen Fischbeständen ist durch starke inter-annuelle Variabilität gekennzeichnet. Die Überlebensrate der Larven spielt dabei als einer der Haupttreiber eine zentrale Rolle. Neben Prädation ist die Ernährungssituation der Larven von übergeordneter Bedeutung: sie beeinflusst das Larvenwachstum und damit die Dauer, die die Larven in der hoch sensiblen Larvalphase verbringen. Angesichts der andauernden niedrigen Rekrutierung des frühjahrslaichenden Heringsbestandes der westlichen Ostsee (engl. western Baltic spring spawning herring, WBSSH) wurden die Studien dieser Thesis durchgeführt. Dies geschah mit dem Ziel weitergehende Erkenntnisse über die Beziehung zwischen der Ernährungssituation der Heringslarven und deren Wachstum in drei wichtigen Aufwuchsgebieten der westlichen Ostsee (Nord-Ostsee-Kanal, Greifswalder Bodden, Kieler Förde) zu gewinnen. In der Frühjahrssaison 2011 wurden Nahrungsquantität und Nahrungsqualität in Form der Konzentration der essentiellen Fettsäuren (engl. essential fatty acids, EFA) im Greifswalder Bodden und im Nord-Ostsee-Kanal analysiert und zum Heringslarvenwachstum in Beziehung gesetzt. Es zeigte sich, dass sowohl Nahrungsquantität als auch –qualität das Larvenwachstum beeinflussen. Die höchsten EFA-Konzentrationen in den Larven wurden beobachtet, als auch die EFA- Konzentrationen in der Beute am höchsten waren; die EFA-Konzentrationen in den Larven korrelierten signifikant mit deren Wachstum. Im Laufe der Saison boten beide Habitate sowohl gute als auch schlechte Nahrungsbedingungen, jedoch in diametraler zeitlicher Anordnung. Die Analysen einer sechsjährigen Zeitserie des Nord-Ostsee-Kanals zeigten ein wiederkehrendes saisonales Muster von Futterverfügbarkeit und Larvenwachstum in diesem Habitat. Im Mai eines jeden Jahres wurden