P LANKTOTHRIX RUBESCENS
P. RUBESCENS - INDUCED ENVIRONMENTAL CHANGES : INDIRECT EFFECTS
darkness and reduced food resources below the metalimnic layer result in an unavoidable reduction of metabolism (see chapter 4.1). Hence it appears inevitable, that Lake Ammersee coregonids suffer sustained nutritional constraints when migrating from the metalimnic layers in order to escape elevated P. rubescens densities, which, depending on the duration of the P. rubescens stratification, could result in a deficient nutrition of the fish.
In conclusion, both avoidance of P. rubescens (either as a consequence of reduced food intake or migration from typical habitats) and exposure to toxic P. rubescens can be expected to cause detrimental effects on coregonid metabolism and thus to result in sustained impairment of their nutrition. This suggests that the occurrence of toxic P. rubescens per se causes a deficient nutrition of feral coregonids in Lake Ammersee.
P.
RUBESCENS-
INDUCED ENVIRONMENTAL CHANGES:
INDIRECT EFFECTSCyanobacteria have been shown to affect various biotic and abiotic factors in lakes, hence suggesting indirect effects on coregonids living in the pelagic zone of lakes. This particularly concerns possible impacts on coregonid food organisms (such as cladoceran plankton) and effects on exogenous factors (e.g. effects on oxygen conditions, pH values, ammonium content etc.), which may result in an insufficient sometimes even hostile environment for fish (Wiegand &
Pflugmacher, 2005 and references therein).
Fig. 5.3: Snapshots from Lake Ammersee during summer 2001: Acoustic recordings (background) demonstrated a continuously migration of coregonids (grey sickles) beneath the metalimnion which is characterised by the temperature (green), oxygen conditions (red) and P. rubescens layers (purple).
Acoustic campaigns were conducted with a Lowrance X-16/192 kHz-echo sounder (Lowrance, USA) immediately after sun down. The surface bubble layer in the range of 0-6 m depth has to be excluded. Temperature, oxygen profiles and P.
rubescens cell densities were determined as carried out in chapter 4.1 and 2.1, respectively.
P. rubescens [103 cells/ml]
Depth [m]
Impacts on Coregonids following P. rubescens-induced Changes in Oxygen Regime
One of the most critical exogenous parameters, which can be affected by cyanobacteria are oxygen conditions, as the decomposition of senescent cyanobacterial bloom material often causes substantial oxygen depletion and consequentially extensive mortalities of feral fish (Jewel et al., 2003; Nascimento & Azevedo, 1999; Pollux & Pollux, 2004; Toranzo et al., 1990).
The oxygen regime in Lake Ammersee is characterised by the regular occurrence of a pronounced metalimnic oxygen depletion (Kucklentz et al., 2001; Lenhart, 2000), which, as demonstrated in this study (see chapter 4.1), appears to be causally related to recurring high P. rubescens abundance16. As these metalimnic oxygen depletions regularly cause levels to fall below coregonid tolerance (see chapter 4.1), they may provide, in addition to stratified microcystin-containing P. rubescens, for an additional stress factor in the metalimnic layer. This suggests that metalimnic stratified P. rubescens could force the coregonids in Lake Ammersee to withdraw from their typical habitat not only directly, in order to avoid contact with filaments but also indirectly, due to enhanced oxygen depletion. As discussed above, such migration out of the metalimnic layer would result in a reduction of coregonid nutrition (see above) and thus coregonid starvation.
Impacts on Coregonids via P. rubescens-induced Effects on Zooplankton
Toxic cyanobacteria have been demonstrated to influence the zooplankton composition of waterbodies, as there is remarkable variation in the response of diverse zooplankton species to toxic and even to non-toxic cyanobacteria (summarised in Sivonen & Jones, 1999). Small and selective foraging species (e.g. Bosmina sp., various copepods) seemed to be less affected, while larger, filter feeding cladoceran species (mostly Daphnia sp.) are negatively selected as they cannot avoid cyanobacterial uptake except by stopping grazing. Since pelagic coregonids are planktivorous, feeding preferentially on large non-evasive cladoceran species (e.g. Daphnia sp., Bythotrephes sp.; see Mayr, 2001; Mookerji et al., 1998 and Skurdal et al., 1985), cyanobacteria thus in principle appear able to change the zooplankton composition in a manner disadvantageous for coregonids.
In comparison with other pre-alpine lakes, the feeding habits of Lake Ammersee coregonids are unusually often based on Bosmina and copepod species (Mayr, 2001). It therefore appears possible, that the occurrence of toxic P. rubescens may shift the balance of zooplankton from Daphnia sp. toward Bosmina and copepods. As a consequence a qualitative and, when the regular appearance of empty coregonid guts during the growth season are considered, even a general loss of coregonid food organisms is possible. Such insufficient food supply can be assumed to substantially impair coregonid nutritional status.
In addition, several organisms serving as fish food have themselves been shown to accumulate considerable amounts of cyanobacterial toxins and for this reason represent potential vectors for the ingestion of cyanobacterial toxins by fish (Engström-Öst et al., 2002; Kankaanpää et al.,
16 Resulting from oxygen-dependent decomposition of senescent metalimnic P. rubescens cells or from a shift of the stratified P.
2005b; Karjalainen et al., 2005; Smith & Haney, 2006). Observations of this study demonstrate copepods in Lake Ammersee to accumulate P. rubescens components within their digestive tract and furthermore show copepods to play an important role in the diet of Lake Ammersee coregonids (chapter 4.2). It therefore appears plausible, that coregonids in Lake Ammersee may be exposed to P. rubescens toxins via feeding on copepods which have accumulated toxic P. rubescens components. This in principle might cause toxicological damage and effects on the coregonid nutrition comparable to that arising subsequent to ingestion of toxin-containing P. rubescens filaments.
C
ONSEQUENCESIn reviewing the various routes by which microcystin-containing P. rubescens may impact feral coregonids in the pelagic zone of Lake Ammersee, it is obvious that in addition to influences causing direct adverse effects (e.g. effects on embryonal development and organ damage) to the fish, all conceivable factors of P. rubescens exposure finally culminate in a deficient nutrition for the coregonids. Prolonged P. rubescens abundances, as observable in Lake Ammersee, thus appear to result in substantial deficiencies in the coregonids nutrition. This can be expected to result in significant growth reduction hence providing a possible explanation for anomalous annuli arising on the scales of Lake Ammersee coregonids during the growing season and the associated growth retardation.
Furthermore, when considering that in pre-alpine lakes the coregonids growing season normally has a duration of just five months (Enz et al., 2001, Mookerji et al., 1998), it appears clear that prolonged nutritional deficiencies severely restrict the ability of coregonids to stockpile the energy reserves that are crucial for spawning and overwintering. Accordingly, prolonged P. rubescens abundances as observable in Lake Ammersee can be expected to result in incomplete and even exhaustion of energy reserves, most likely additionally reducing coregonid fitness and increasing their susceptibility to other detrimental effects.
In 1993 and 1994, subsequent to the elevated P. rubescens abundances which occurred in 1992 and 1993 (Lenhart, 2000), Lake Ammersee coregonids were indeed demonstrated to lack sufficient fat and glycogen reserves (Negele et al., 2000). These observations corroborate the expected causality of prolonged P. rubescens abundance and deficient energy reserves. As coregonids have been shown to counterbalance their energy deficiencies with progressive degradation of muscle protein, it moreover appears likely, that inadequate nutrition ensuing from prolonged occurrence of toxic P. rubescens might not only result in reduced growth but also in significant weight reduction.
It can be assumed, that the regular lack of energy most likely causes problems for coregonids during late winter and early spring, when after overwintering, depletion of energy stores is maximal, sufficient food supply is still lacking and furthermore, increasing water temperatures
stimulate coregonid metabolism thus increasing energy demands (Negele et al., 2000;
Reshetnikov et al., 1970; Valtonen, 1974). Hence it is not surprising, that coregonid age groups in Lake Ammersee repeatedly disappear during the months of April and May. This is supported by the fact that the disappearance of coregonids predominantly involves mature age groups (Wißmath, 2004), which need an energy surplus for spawning. It is thus plausible that the loss of coregonid age groups in Lake Ammersee results from energy deficiencies caused by insufficient coregonid nutrition in the summer prior to spawning linking the disappearance of coregonid age groups to detrimental impacts of prolonged occurrence of toxic P. rubescens.
C
ONCLUDING ASSESSMENTThe intentional re-depletion of phosphorous loads (re-oligotrophication) of Lake Ammersee provoked a renaissance of the microcystin-producing cyanobacterium P. rubescens. The prolonged occurrence of this toxic P. rubescens can be expected to affect feral coregonids in the pelagic zone in a variety of ways including immediate detrimental effects but also indirectly, primarily resulting in an insufficient nutrition of the coregonids causing reduced growth and deficient energy reserves. These energy deficiencies appear to cause the increased mortalities of Lake Ammersee coregonids, primarily observed after spawning and overwintering, when energy reserves are required. As a result of this, whole age groups of Lake Ammersee coregonids disappear subsequent to first spawning, i.e. in the first month of their third year. Regular disappearance of three-year-old coregonids represents a sustained detrimental effect on the population dynamics of coregonids, since this restricts the continuity of the pelagic Lake Ammersee population to spawning of a single age group.
Furthermore, as sustainable fishery aims to catch only fish which have spawned at least once in their lifetime, coregonids dying after first spawning thus disappear before being suitable for sustainable fishery. This represents a huge loss of the fishing base for the coregonid fishery and dramatic slumps in fishery yields, which correspond, due to the importance of coregonids for the local fishery, to an existential threat to professional Lake Ammersee fishermen.
In conclusion, the current investigations reveal a significant impact of toxic P. rubescens on coregonids unambiguously confirming the supposed link between the occurrence of toxic P. rubescens and the observed irregulatories in growth and population dynamics of coregonids in Lake Ammersee.