Reproduction strategies and distribution of larvae and juveniles of benthic soft-bottom invertebrates in the Kara Sea (Russian Arctic) The influence of river discharge on the structure of benthic communities: a larval approach Ingo Fetzer Vorgelegt im Fachbereich 2 (Biologie/Chemie) der Universität Bremen als Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) Bremen 2004 1. Reviewer: Prof. Dr. Wolf Arntz Alfred-Wegener-Institute/University of Bremen 2. Reviewer: Ass. Prof. Dr. Sigrid Schiel Alfred-Wegener-Institute/University of Kiel Contents 1 Introduction 11 1.1 Life-history traits in marine invertebrates . 11 1.2 Definition of ’larva’ . 14 1.3 Historical background . 15 1.4 ’Thorson’s rule’ . 17 1.5 Ecological implications of reproduction modes . 19 1.6 Aims of the study and hypotheses . 20 2 Material and Methods 23 2.1 Study area - environmental conditions . 23 2.2 Sampling areas . 27 2.3 Sampling gear and treatment of samples . 27 2.4 Data handling . 29 3 Results and Discussion 33 3.1 Sampling . 33 3.2 Kara Sea ecology . 34 3.2.1 Zoobenthos . 34 3.2.2 Juveniles . 35 3.2.3 Meroplankton . 35 3.3 Influence of river discharge . 42 3.3.1 Influence of river discharge on plankton and benthos . 42 3.3.2 Influence of hydrography on the distribution of larvae . 43 3.4 Reproduction modes and zoogeographic affiliation . 49 4 Conclusion and future perspectives 55 5 Publications 57 5.1 Publication I . 61 5.2 Publication II . 85 5.3 Publication III . 121 5.4 Publication IV . 141 5.5 Publication V . 177 6 Acknowledgements 217 7 Reference List 221 SUMMARY Summary Reproduction strategies strongly influence distribution patterns and abundance of marine benthic invertebrates. Most of them exhibit rather complex and diverse life cycles that are adapted to the environment the species live in. The great diversity of life history patterns found has generated intense debates among ecologists on classification of different development types and their rela- tionship to given biotic and abiotic environments. In the light of new findings from polar seas much interest is given to the potential geographical shift in main life history traits of benthic in- vertebrates. However, until now little is known about the reproduction strategies of the majority of Arctic invertebrates. Most species in temperate areas reproduce with pelagic larvae, which often act as passive drifting particles in the water column. Their distribution is therefore mainly determined by local hydrographic patterns, which can either transport them away or retain them close to their spawning ground, the distribution of their adults (=place of release) and the du- ration of their stays in the water column. Direct development ensures that the offspring stays on approved sites where adults already survived and guarantees sufficient recruitment within the community since larvae are not endangered to be transported away by currents. The main aims of this work are to determine the reproductive patterns of benthic invertebrates in the Kara Sea and to analyse possible adaptations of reproduction strategies to polar conditions. The structuring influence of river discharge and hydrography on the spatial distribution of larvae and settled juveniles in relation to the distribution of their adults is investigated. Given the specific characteristics of the Kara Sea, special emphasis is put on the role of the pycnocline in separating meroplankton communities. The Kara Sea is a shallow shelf sea with an average depth of 50 m located in the Russian Arctic. Besides strong fluctuations in light, temperature and ice coverage, hydrography and ecosystems are strongly affected by the immense freshwater input of the two adjacent rivers Ob and Yenisei. The outflow creates a pronounced bilayered pelagic habitat with a confined pycnocline. Analyses of zooplankton samples from three years revealed a strong structuring effect of river discharge on pelagic communities. River run off varied significantly between years. Benthic communities are clearly shaped by the influence of freshwater input but also by the deposition of imported organic material, which can be utilised as a food source. Pelagic larvae and juveniles of marine benthic invertebrates of the Kara Sea were sampled, identified and their quantity and dispersal patterns in relation to the presence and distribution of their adults analysed. At each sampling station, three plankton samples were taken: one below the pycnocline, one across and one above it. Additionally, sediment samples were collected using a large box corer and a multicorer to monitor adult and juvenile distribution, respectively. During the investigation period in 2000 and 2001, 44 larval and 54 juvenile species were identified. For 23 of the larval species adults were present in benthos samples. For the remaining 21 larval species, adults were reported from the adjacent Barents and Petchora Sea, indicating a strong larval supply from the neighbouring seas. Most larvae were found in all water layers, although highest abundances were present in the upper low salinity layer, revealing a high accli- matisation potential of most larvae to low salinities. Notably, the ophioplutei of the brittle star Ophiocten sericeum, whose adults are very sensitive to lowered salinity, showed high concentra- V SUMMARY tions within low salinity meltwater plumes. No differences in meroplankton densities were found between the surface layer and the pycnocline, but surface and bottom layer differed significantly. The pycnocline seems to act as a physical barrier for most larvae. Meroplankton densities of individual species were generally <1 ind. m-3, but ophioplutei of O. sericeum reached densities of 200 ind. m-3. The hydrographical regime strongly influences larval distribution both verti- cally and horizontally. Generally, lowest concentrations were found in the wake of the rivers, although along a transect out of the Yenisei River local accumulation of larvae in the estuary was found. Retention is most likely caused by circulation patterns created by the strong river run off. Retention of larvae of benthic invertebrates within nursery grounds and/or the return to their parental grounds is challenging for species in areas with strong riverine output. The importance of retention in the study area was demonstrated for five exemplary species. Most benthic species of the study area show an Arctic zoogeographic distribution, but a considerable number of Arctic-boreal, boreal and cosmopolitan species were also found. The river run off may not only foster the survival of euryhaline species but through its thermal input also creates favourable conditions for boreal species. Most invertebrate species in the Kara Sea seem to reproduce directly. This large proportion can be explained in some parts by the high share of peracarid crustaceans (Cumacea, Isopoda and Amphipoda) in the species composition. While other taxa display a huge spectrum of reproduction modes, which vary strongly between species and geographic regions, peracarids show a direct reproduction trait all over the world. Their elimination from the dataset in this study reveals for the Kara Sea a larger share of species reproducing with pelagic larvae. It is assumed that due to its variability in both biotic and abiotic factors, the environment of the Kara Sea shelf often creates unfavourable conditions for benthic species. Species with pelagic larvae or highly mobile species like most peracarid crustaceans may have an advantage in reoccupying defaunated habitats. The numerous larval types found in this study indicate that planktonic development is impor- tant in the Kara Sea ecosystem. There is still a considerable lack of knowledge on reproductive strategies of marine invertebrates, which especially holds true for organisms of the Arctic Ocean. Better knowledge on reproduction traits and dynamics of polar benthic invertebrates is not only a fundamental aspect for understanding Arctic ecosystems, but also a prerequisite for the inter- pretation of their reaction to future global change. VI ZUSAMMENFASSUNG Zusammenfassung Reproduktionsstrategien haben einen starken Einfluss auf Abundanzen und Verbreitungsmuster mariner benthischer Evertebraten. Die meisten Evertebraten zeigen relativ komplexe und diverse Lebenszyklen, die an ihre jeweilige Umwelt angepasst sind. Die große Diversität von Entwick- lungsmustern ist Anlass für rege Diskussionen zwischen Ökologen über mögliche Klassifizie- rungen der unterschiedlichen Entwicklungsstrategien und ihre Beziehungen zu den biotischen und abiotischen Lebensbedingungen. Angeregt durch neue Erkenntnisse aus polaren Gewässern vor allem im Hinblick auf Klimaänderungen ist das Interesse an einer möglichen geographischen Verschiebung der wichtigsten Charakteristika der Lebensgeschichte benthischer Evertebraten in den letzten Jahren gestiegen. Allerdings ist bis heute nur wenig über die Reproduktionsstrategien eines Großteils der arktischen Evertebraten bekannt. Die meisten Arten der gemäßigten Breiten pflanzen sich über pelagische Larven fort. Diese verhalten sich meist wie passiv driftende Partikel in der Wassersäule. Ihre Verbreitung ist deshalb hauptsächlich durch lokale hydrographische Prozesse bestimmt, die sie entweder forttransportie- ren oder in der Nähe ihres Ursprungsgebiets halten. Für die Verbreitung der Larven spielt außer dem Vorkommen und der Verbreitung der Adulten (Ort der Reproduktion) sowie den Strömun- gen die Dauer des Aufenthalts im Wasser eine Rolle. Direktentwicklung