The Asian clam Corbicula fluminea was one of many non-native species, which invaded Lake Constance in the last decades. Since its first observation in 2003, the clam established a huge population, mostly in the eastern part of the lake in the vicinity of its first observation (ANEBO ; Werner 2008). From there, C. fluminea spread along the southern and northern shore of Lake Constance and now, nine years after its first observation, has invaded almost the complete basin of upper Lake Constance. However, in comparison to the invasion of D.
polymorpha in the late 60s, the invasion and dispersal of C. fluminea occurred rather slowly (ANEBO ; Siessegger 1969). Dispersal of bivalves can be attributed to crawling and to larval drift via mucus draglines, although C. fluminea has no pelagic stage (Prezant and Chalermwat 1984). Werner (2008) speculated that apart from natural drift of larvae the attachment on boats and bird legs has contributed to the establishment in remote areas of the lake.
The successful spread of C. fluminea is presumably favored by many autecological traits such as early sexual maturity, high fertility, brood care and a wide tolerance to various environmental factors (Rajagopal et al. 2000; McMahon 2002; Sousa et al. 2008). Nowadays, numbers of non-native species in freshwater ecosystems increase rapidly, quite often with impacts on the stability of ecosystems and global species diversity (Sala et al. 2000).
Introduction of alien species can have severe effects, e.g. on the species composition, ecosystem processes and modified nutrient flows and trophic interactions within a community. To predict and assess such impacts, a thorough knowledge of the autecology and life cycle of the alien species is required. We are only beginning to understand effects resulting from invasions of non-native species (Sala et al. 2000; Walther et al. 2009). In this context, nutritional requirements of species have to be considered. In general, nutritional requirements of freshwater bivalves are poorly investigated, in particular with regard to essential biochemicals.
Due to their high filtration rate bivalve populations are able to influence phytoplankton community composition (Lauritsen 1986; Cahoon and Owen 1996; Bastviken et al. 1998;
Welker and Walz 1998). Likewise, annual succession of phytoplankton is associated with changes in the availability of elemental and biochemical nutrients for filter-feeding organisms (Wacker and Von Elert 2001; Hartwich et al. 2012; see chapter 4). This is often reflected in the lipid content of benthic organisms and can provide clues to the ecology of those organisms (Cavaletto and Gardner 1999). Seasonality in seston development and short term depletion of food quantity and quality might influence clams variously, and at least temporarily they might be affected by the supply of food and by the supply of nutrients. Co-limitation and interactions between potentially limiting nutrients, as discussed for
filter-feeding cladocerans (Martin-Creuzburg et al. 2009; Hartwich et al. 2012), are likely to happen in the field and also to affect also the performance of benthic organisms. However, with their internal storages adult clams might temporarily overcome unfavourable conditions.
For growth season in oligotrophic Lake Constance my study revealed a strong impact of water temperature on growth and survival of C. fluminea (chapter 4), thereby confirming previous assumptions (Werner 2008; Werner and Rothhaupt 2008). Plankton succession and seston nutrient parameters were also strongly controlled by temperature regime. Seston was dominated by high proportion of PUFA and sterol containing algae resulting in favourable growth conditions for C. fluminea during spring and summer months. In winter months clams were faced low carbon and low essential lipid supply resulting in growth stagnation and massive die-off events (chapter 4). Clam growth was affected by other seston parameters (i.e. C:P ratio, seston green algae- diatom-, carbon- or ARA- content), however, many of these factors were also influenced by water temperature (co-linearity) and hardly separable from temperature effects in our experimental dataset.
Invasion of C. fluminea in lower Lake Constance probably will take place in the next years (see Fig. 1, Werner pers. communication), with unpredictable consequences for benthic (and pelagic) communities. Lower Lake Constance provides the warmer habitat, has a higher phosphorus load in comparison to the upper basin of Lake Constance and the sediment is dominated by soft substrate (IGKB 2010), factors which all favour C. fluminea. Laboratory findings (chapter 2, 3), showing that C. fluminea growth is constrained by limitation in essential lipids, might impair in habitats, where nutrient load is higher (eutrophic systems) or in times of massive bloom formation, when temperature is sufficient for clam growth and plankton succession and composition might regulate clam growth performance, possibly present in lower Lake Constance.
However, in upper Lake Constance temperature was the main driver for seston dynamics as well as clam growth (chapter 4). For lotic ecosystems, temperature regimes have been shown to support clam establishment and to favour the spread of C. fluminea (Schöll 2000).
Beneficial effects of increased temperatures on clam growth were observed in European water ways at cooling water outflows of power plants, which are often inhabited by invasive species (Cairns and Cherry 1983; French and Schloesser 1991). With ongoing dynamics of global warming multiple factors will bias ecosystems processes. In aquatic ecosystems, changing temperature regimes will affect plankton succession and species composition, lake water exchange and vertical mixing, ice cover in winter, nutrient recycling and eutrophication symptoms (Mooij et al. 2005; Jöhnk et al. 2008; Adrian et al. 2009).
Additionally, the invasion of non-native species is favoured by global warming (Stachowicz et al. 2002; Walther et al. 2009).
For Lake Constance, recent monitoring indicates that the duration of thermal stratification and therefore the phytoplankton growing season is prolonged by climate change (Straile et al. 2003). In addition, expected milder winter temperatures will reduce thermal stress
organisms have to cope with (Straile et al. 2010). For C. fluminea, an increase in water temperature will increase the reproductive success and potentially may facilitate a second reproduction event per year (Mouthon 2001; Sousa et al. 2008; Werner 2008). If clams are supported by increasing temperature, this may result in an enhanced top-down control of phytoplankton by filter feeding clams. Additionally, C. fluminea itself may possibly be shifted from temperature- to nutrient-regulated performance regarding growth, reproduction and mortality. Mortality of C. fluminea may change from low temperature determined winter die-off to heat stress regulated summer mortality. In combination with low or even limiting carbon supply during summer months, thermal stress may result in higher summer mortality (Weitere et al. 2009; Vohmann et al. 2010).
Mortality of clams can tremendously change habitat structure as shown by Werner et al.
(2008) for Lake Constance during winter in 2005/2006, when the majority of the C. fluminea population suffered from low water level and extremely cold water temperatures. Massive clam die-off events result in an accumulation of bare shells on the ground, whereas shells are typically covered with sand. The clam-mediated structural modification of the habitat at the Rohrspitz bay (Fig. 1) increased substrate diversity and settlement surface for benthic macroinvertebrates, like D. polymorpha or G. roeselii (Werner and Rothhaupt 2007; Werner 2008; Gergs et al. 2011; personal observations).
Due to its filtration capacity bivalves can shift a substantial part of pelagic primary production as biodeposition material, i.e. either as digested faeces or undigested pseudofaeces, to the benthic food web (Gergs et al. 2009; Atkinson et al. 2011). Bivalves act as a food ‘donor’ and food quality ‘converter’ for benthic invertebrates by altering the bioavailability of food and its elemental and biochemical (fatty acids, sterols) composition in biodeposition material (Gergs et al. 2009; chapter 5). The impact of this transformation process itself and the role of essential biochemical nutrients have not been considered as a mechanism determining trophic interactions between benthic herbivores and its phytoplankton food source. My results show, for the first time, that filter-feeding bivalves not only provide a crucial link between the pelagic and benthic food web by increasing the bioavailability of pelagic resources in comparison to sedimented algae (chapter 5), but that clam conditioning also is associated with changes in the biochemical composition of pelagic food sources. Especially the modification in essential lipids (sterols, PUFAs) improves growth conditions for gammarids, that are constrained by a low availability of dietary lipids when fed cyanobacterial carbon. In a tritrophic food chain ‘trophic upgrading’ by intermediary protists has shown to improve cyanobacterial carbon for filter-feeding cladocerans (Klein Breteler et al. 1999; Martin-Creuzburg et al. 2005a). In my setup, sterol-depleted food sources might have also been biochemically ‘upgraded’ during clam conditioning for subsequent use by benthic consumers via the incorporation of clam-derived lipids in biodeposition materials. Hence, my results will help to elucidate the importance of bivalves in mediating a benthic-pelagic coupling and to assess effects of food quality on the benthic community.
However, apart from carbon transfer via pelagic-benthic coupling also during bloom conditions huge biomass is introduced into benthic food web. Diatom blooms settling to the sediment are considered to be the main sources of high quality food for benthos (Fitzgerald and Gardner 1993), whereas cyanobacterial carbon has been reported to be of minor nutritional quality for benthic invertebrates (Karlson et al. 2008; Nascimento et al. 2009;
Suikkanen et al. 2010). Aquatic cyanobacteria often form extensive blooms, both in freshwater and marine systems, and tend to increase with global warming. The accumulation of cyanobacterial biomass may severely affect herbivorous consumers. C.
fluminea growth rates were significantly lower when juveniles were fed cyanobacterial diets instead of eukaryotic algae (chapter 2). My results present first insight into food quality effects on C. fluminea nutrition which can be related to essential dietary substances missing in former laboratory studies (Foe and Knight 1986). However, correlations of nutritional parameters with somatic growth rates are a first step towards the identification of mechanisms affecting clam fitness. Based on results from chapter 2, the diet of clams was experimentally manipulated in chapter 3 to assess the significance of lipid substances for clam nutrition. The absence of essential lipids in cyanobacteria (sterols, PUFAs) has been identified as a major food quality constraint for filter-feeding Daphnia and herein for Corbicula as well (Müller-Navarra et al. 2000; Von Elert et al. 2003; chapter 2, chapter 3).
Whereas C. fluminea could not benefit from PUFA supplementation when fed with cyanobacteria (data not presented here), sterols enrichment improved growth conditions for clams (chapter 3), indicating strong dependency on dietary sterols. For the first time, I attributed growth conditions of C. fluminea to nutritional lipids (chapter 2) and identified sterols as determining factor in clam nutrition on cyanobacterial diets (chapter 3).
In times of insufficient nutritional supply filter feeding bivalves might suffer from seston composition, especially in times of cyanobacterial blooms. In contrast to other filter feeding bivalves, C. fluminea is regarded as a non-selective suspension feeder (Way et al. 1990;
Vaughn and Hakenkamp 2001) and thus might not be able to discriminate against nutritionally inadequate food particles. However, other mechanisms might help C. fluminea to overcome unfavourable nutritional conditions. It remains to be tested if C. fluminea is able to adjust filtration or assimilation rate in order to increase utilization of food sources and gain more specific limiting nutrients (compensatory feeding) or switch from filtration to deposition feeding to obtain its food from the sediment (pedal feeding) and thus avoid nutritionally inadequate food sources present in the water column. However, as organic carbon concentrations in sediments of Lake Constance are very low (1 - 5%, not presented;
Deutzmann pers. communication; Van Der Velden and Schwartz 1976), I assume that additional carbon will not completely satisfy clam maintenance. Nevertheless, pedal feeding might contribute to the dietary provisioning with essential nutrients and therefore might improve the performance of clams and possibly provide advantage over exclusively filter-feeding bivalves.
Certainly, it would be very interesting to see whether differences between C. fluminea and native/established bivalves in their ability to persist and survive cyanobacterial blooms affect
the invasion success. Investigating and comparing the physiological demands of native and invasive species may help to understand invasion patterns and to improve risk assessment of upcoming invasions. Additionally, mechanisms to avoid unfavourable nutritional conditions are known in bivalve filtration (selective feeding), it remains to be tested if pedal feeding might allow C. fluminea to decouple their performance from (unfavourable) seston composition.
Aquatic herbivores face a multitude of nutritional challenges in natural environments. Sterol limitation might be one factor with the potential to affect the structure of aquatic food webs, at least seasonally and in certain habitats. Apart from sterols, biochemical food quality depends on a multitude of other factors such as PUFAs, amino acids, vitamins and presumably their elemental stoichiometric composition. Over the last years, considerable advance has been made in identifying food quality aspects and their role in invertebrate performance. Food quality research has mainly focused on elemental nutrients and polyunsaturated fatty acids as potentially limiting resources. This thesis provided data showing that the dietary sterols should also be taken into account when analyzing nutritional constraints and their effects on trophic interactions in freshwater food webs.
Following studies with C. fluminea might investigate co-limitation aspects of factors mediating food quality in cyanobacteria and other eukaryotic algae under field and laboratory conditions. Apart from growth performance of juvenile clams, reproduction in adult specimen, larval development and juvenile recruitment might face different nutritional demands, necessary for understanding the life history of C. fluminea. My data might help to improve our knowledge on the consequences of cyanobacterial mass developments for benthic filter-feeders and highlights the importance of sterols as potentially limiting nutrients in aquatic food webs.
Abstract
The Asian clam Corbicula fluminea, originating from East Asia, has become a widespread benthic invertebrate in many freshwater ecosystems throughout Europe and North and South America. With the introduction of invasive bivalves drastic changes in established benthic communities often occur. Knowing the nutritional demands in ecosystem processes is crucial for understanding the flow of energy in food webs, and for investigating species interactions within the food web. In this context, nutritional requirements of species have to be considered, which are poorly investigated for freshwater bivalves, in particular with regard to essential biochemicals. Therefore, the aim of my study was to gain knowledge on nutritional demands of C. fluminea. In particular, I examined the role of essential lipids (sterols, polyunsaturated fatty acids) for juvenile clams both in the laboratory and in the field, i.e. in Lake Constance. Further on, I focused on the benthic-pelagic coupling mediated by C. fluminea, and the possible nutrient transfer and modulation of food quality effects onto detritivorous benthic invertebrates.
Laboratory growth experiments with C. fluminea raised on eukaryotic and prokaryotic food sources revealed strong dependency of clam growth rates on lipid composition of food sources. Somatic growth rates were significantly higher when juveniles were fed eukaryotic algae instead of cyanobacteria. Linear regression analyses revealed significant positive relationships between clam somatic growth rates and dietary sterol and polyunsaturated fatty acid content. Based on these results, a supplementation approach was conducted, in which C. fluminea was fed again with pro- and eukaryotic food sources. Additionally, sterol depleted cyanobacterial food was enriched with sterols. The growth rate improvement of clams fed with enriched food sources revealed sterol limited growth on cyanobacteria. I have shown for the first time that a benthic freshwater invertebrate is constrained by an absence of dietary sterols and I pointed out growth enhancing effects by sterols addition when feeding on cyanobacterial food sources. Cyanobacteria, as prokaryotic phototrophs, lack essential lipids (sterols, long chain PUFAs) and are already known as nutritional inadequate food source for pelagic filter-feeding organisms. The accumulation of cyanobacterial biomass may severely affect the performance of aquatic consumers, not only pelagic zooplankton, but also benthic filter feeding bivalves might be affected by cyanobacterial carbon and be limited by low sterol and PUFA supply.
Filter feeding clams are largely affected by seston dynamics in the pelagial. Thus, seasonal variation in water temperature and seston composition may determine the growth performance of benthic clams. To elucidate C. fluminea somatic growth under natural conditions, a field study of clam growth and survival was conducted in Lake Constance throughout 2010. Temperature and food quantity and quality effects were investigated and correlated with clam fitness parameters. Analyses showed that the growth and survival of C.
fluminea in Lake Constance is basically determined by water temperature, with high
mortality rates during winter and increased growth rates during summer when temperature and carbon supply favour growth of C. fluminea. Concomitant laboratory experiments confirmed the dominant influence of temperature on growth of C. fluminea. The field study also revealed that the conditions favouring clam growth are restricted to only seven months of the year, when temperature exceeded 10°C. Hence, the C. fluminea population in Lake Constance may benefit from the expected climate change resulting in milder winter temperatures and an earlier onset of thermal stratification in spring because of reduced winter mortality and an extended growing season, i.e. the period in which water temperatures exceed 10°C.
Apart from nutritional aspects, I investigated the role of C. fluminea as mediator between phytoplankton dynamics and benthic detritus feeders, via the establishment of a laboratory experimental food chain consisting of different pelagic primary producers (algae, cyanobacteria), the freshwater clam C. fluminea as primary consumer, and Gammarus roeselii as omnivorous consumer feeding on biodeposition material produced by C. fluminea.
The clam was used as benthic-pelagic coupler and the produced biodeposition material was collected and fed to G. roeselii. Data showed that the survival and growth of gammarids significantly increased when autotrophs were offered to G. roeselii as biodeposition material compared to sedimented autotrophs. This upgrading of food quality was hypothesised to derive from an increased accessibility of pelagic food for G. roeselii and to a clam-mediated dietary enrichment with essential elemental and biochemical (fatty acids, sterols) nutrients.
My results show that filter-feeding clams not only provide a crucial link between the pelagic and benthic food web by changing energy fluxes, but also transform pelagic resources and increase the bioavailability of pelagic resources in comparison to sedimented algae.
Furthermore, data suggest that this pelagic-benthic coupling is constrained by a low availability of essential biochemical nutrients; in particular during cyanobacterial blooms dietary lipids are scarce for gammarids.
Thus, my findings contribute significantly to our understanding of the consequences associated with cyanobacterial mass developments, which are expected to be favoured by global warming, for benthic filter-feeding clams. They also highlight the importance of considering sterols as potentially limiting nutrients in aquatic food webs. My results suggest that the growth of C. fluminea is partially dependent on the availability of essential lipids in the diet. Additionally, C. fluminea has the potential to mediate nutritional effects from pelagic to benthic food webs and may therefore play an important trophic role in the benthic food web.
Zusammenfassung
Die aus Ostasien stammende asiatische Körbchenmuschel Corbicula fluminea hat sich in den letzten Jahrzenten zu einem weitverbreiteten benthischen Wirbellosen in vielen Süßwasser-Ökosystemen entwickelt. Mit der Einführung der invasiven Muscheln in neue Lebensräume sind oftmals drastische Veränderungen in etablierten Lebensgemeinschaften verbunden. Um Wechselwirkungen und Energieflüsse zwischen Organismen im Nahrungsnetz zu verstehen, ist im Besonderen die Kenntnis des Nährstoffbedarfs der verschiedenen Arten wesentlich.
Dieser wurde bisher für Süßwassermuscheln kaum untersucht, insbesondere im Hinblick auf essentielle biochemische Makromoleküle. Ziel meiner Arbeit war es daher, Erkenntnisse über den Nährstoffbedarf von C. fluminea zu gewinnen. Im Besonderen untersuchte ich die Rolle von essentiellen Lipiden (Sterole, mehrfachungesättigte Fettsäuren) für juvenile Muscheln im Labor und unter natürlichen Bedingungen im Jahresverlauf des Bodensees.
Außerdem beschäftigte ich mich mit der bentisch-pelagischen Kopplung durch C. fluminea, sowie mit einem möglichen Nährstofftransfer und einer Modulation von Futterqualitätseffekten auf detrivore, bentische Invertebraten.
Zu diesem Zweck etablierte ich standardisierte Laborwachstumsexperimente mit C.
fluminea. Dort konnte ich mit eukaryotischen und prokaryotischen Nahrungsquellen für die Muscheln einen Zusammenhang zwischen Muschelwachstumsraten und der Lipidzusammensetzung der Nahrungsquellen aufzeigen. Somatische Wachstumsraten waren signifikant höher, wenn Jungtiere mit eukaryotischen Algen gefüttert wurden, im Vergleich
fluminea. Dort konnte ich mit eukaryotischen und prokaryotischen Nahrungsquellen für die Muscheln einen Zusammenhang zwischen Muschelwachstumsraten und der Lipidzusammensetzung der Nahrungsquellen aufzeigen. Somatische Wachstumsraten waren signifikant höher, wenn Jungtiere mit eukaryotischen Algen gefüttert wurden, im Vergleich