Direct and indirect effects of fungi and oomycetes on leaf litter degradation by freshwater macroinvertebrates

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Direkte und indirekte Effekte von Pilzen und Oomyceten auf die Laub Zersetzung durch aquatische Makroinvertebraten
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The decomposition processes in lakes are documented in few reports only, and it is therefore important to improve our understanding of the process of leaf conditioning and its effects on the benthic community in lakes. In the present thesis I investigated how the identity of microbial colonisers affects the consumption by macroinvertebrates organisms were examined. For the studies presented here the shredder Gammarus roeselii and small-particle-feeder Limnomysis benedeni, a recent invader of Lake Constance were chosen because of their numerical importance in the littoral benthic community of Lake Constance. Here two experiments were performed, in which alder leaves were exposed in the littoral of Lake Constance. Regular leaf subsamples were analysed for chemical and physical leaf parameters, and the consumption rates of G. roeselii were determined in laboratory food choice assays with autoclaved and leached alder leaves as additional food items. In addition to leaf toughness the bulk leaf parameters N-, C-, P-, protein- and polyphenol content were measured and the ergosterol content was determined by HPLC. Consumption rates of littoral exposed leaves were statistically analysed for effects of leaf parameters using permutation based tests and a linear model approach. In both experiments leaf parameters changed and consumption by G. roeselii increased significantly with conditioning in the littoral. The negative correlation of polyphenols with shredder feeding corroborated the known repellence by polyphenols. Notwithstanding studies by others the N- and the protein content decreased over the first time of exposure in the littoral, which suggested that leaf colonising micro-organisms (fungi and oomycetes) could not compensate for leaching of N-containing constituents. In both exposition experiments increasing ergosterol content over exposition time pointed at increasing metabolically active eumycotic fungal biomass on the littoral-exposed leaves, and therefore aquatic fungi and oomycetes were isolated from leaves.The fungal and oomycete isolates were cultured and identified based on the sequence of internal transcribed spacer (ITS) regions of rDNA, and the sequences obtained during these studies were deposits into GenBank®. In freshwaters, fungi are regarded as the most important microbial component on decaying leaves, and here 9 ascomycete and 4 oomycete strains were isolated from conditioned leaf litter. Here, for the first time, oomycetes were demonstrated to affect leaf parameters to a similar extent as other fungal strains and to positively affect consumption by Gammarus, which suggest that oomycetes have a greater impact on leaf litter decomposition in freshwaters than hitherto assumed. In order to experimentally separate effects of leaching and colonisation by fungi or oomycetes, experiments with single isolates growing on autoclaved leaves were performed, in which effects of single strains on leaf parameters and on consumption by G. roeselii were assessed. The majority of the different fungi and oomycete isolates on leaves were significantly preferred over controls, and consumption rates by G. roeselii proved to be strain-specific. The leaf parameters N, C, P, protein and polyphenol were affected by colonisation with single isolates, and the magnitude of the effects was strongly strain-specific. Statistical analysis with a linear model revealed that polyphenol and protein levels were major determinants of the consumption rate of Gammarus, suggesting that fungi and oomycetes might indirectly steer consumption by altering the leaf litter content of protein and polyphenols, in particular during later stages of conditioning in the field. Shredders discriminate between leaves colonised by different fungal and oomycete species, but mechanistically, the mediation of preference by fungi on leaves is not well understood. In order to test the hypothesis, that the strain-specific preference of G. roeselii is mediated by attractants or repellents that are constituents of fungi or oomycetes, selected fungal and oomycete strains were grown either in synthetic or leaf extract medium. Mycelia were extracted with solvents methanol or methylene chloride:methanol (2:1, v:v). Leaves covered with these extracts were subjected to choice feeding assays with G. roeselii. Methanol extracts proved to be repellent, and lipid extracts had no effect on the preference of G. roeselii. These results were contrary to the effects of the single isolates on leaves and suggested that compounds others than lipids or those extracted by methanol mediated the preference of G. roeselii. The repellent effect of the extracts of fungi or oomycetes was strongly affected by the C-source in the growth medium. The benthic mysid L. benedeni has recently invaded Lake Constance. Controlled laboratory experiments revealed that this mysid fed as well on shortly as well as on extensively leached leaf litter of several tree species. The interaction of the measured leaf parameters C- and polyphenol content explained 74% of the attractiveness of the leaf litter for the mysid, which suggested that feeding of L. benedeni is hindered by the waxes and cutin of the cuticula and by the lignocellulose structure of the leaf. 3 fungi growing on leaves elicited an intermediate feeding activity by L. benedeni, compared to that of littoral-exposed and autoclaved leaf litter. This suggests that L. benedeni feeds unselectively on the different microbial colonisers on decaying leaves. For the first time it was demonstrated that L. benedeni is a benthic leaf consumer that might potentially facilitate leaf degradation in Lake Constance.

Zusammenfassung in einer weiteren Sprache

Detritus kann einen wesentlichen Anteil des organischen Eintrags in Seen ausmachen, und litorale Gemeinschaften erhalten relativ hohe Einträge an Laub entlang der Uferlinie, wo dieses zersetzt und in die Sekundärproduktion eingebracht wird. In der vorliegenden Arbeit habe ich untersucht, wie die Identität von mikrobiellen Besiedlern die Konsumption konditionierten Laubs durch Makroinvertebraten beeinflusst. Für die hier gezeigte Untersuchung wurde der Shredder Gammarus roeselii und der Klein-Partikel-Fresser Limnomysis benedeni, der erst in jüngster Zeit in den Bodensee eingewandert ist, wegen ihrer zahlenmäßigen Bedeutung in der benthischen Gemeinschaft des Litorals des Bodensees ausgesucht. Hier wurden zwei Experimente durchgeführt, in denen Erlenlaub im Litoral des Bodensees ausgebracht wurde. Regelmäßig wurden von Laubunterproben die chem. und physik. Blattparameter untersucht und in standardisierten Wahlexperimenten die Konsumptionsraten von G. roeselii mit den zusätzlichen Futterarten autoklaviertes und ausgewaschenes Erlenlaub bestimmt. Zusätzlich zur Blatthärte wurden die Blattparameter wie der N-, C-, P-, Protein- und Polyphenolgehalt bestimmt und der Ergosterolgehalt mit der HPLC gemessen. Die Effekte der Blattparameter auf die Fraßraten der im Litoral ausgebrachten Blätter wurden mit permutations-basierten Tests und mit einem linearen Modell statistisch ausgewertet. Mit der Konditionierung im Litoral veränderten sich in beiden Experimenten die Blattparameter, und der Fraß von G. roeselii stieg signifikant an. Die negative Korrelation zwischen den Polyphenolen und dem Fraß der Shredder bestätigte die schon bekannte abschreckende Wirkung der Polyphenole. Hier nahm der N- und Proteingehalt während der ersten Zeit der Exposition im Litoral ab, was darauf hindeutet, dass die Besiedlung mit Mikroorganismen das Auswaschen der stickstoffhaltigen Inhaltsstoffe nicht kompensieren konnte. In beiden Expositionsexperimenten deutete der über die Expositionszeit ansteigende Ergosterolgehalt auf eine ansteigende metabolisch aktive eumycotische Pilzbiomasse auf den im Litoral ausgebrachten Blättern hin. Deshalb wurden von Laub, aquatische Pilze und Oomyceten isoliert, in Kultur gebracht und, basierend auf der Sequenz der Internal-Transcribed-Spacer (ITS) Regionen der rDNA, identifiziert. Die in den Studien erhaltenen Sequenzen wurden in GenBank® hinterlegt. In Süßwasser werden Pilze als wichtigste mikrobielle Komponente auf sich zersetzendem Laub angesehen, hier wurden 9 Ascomyceten und 4 Oomyceten gefunden. Zum ersten Mal wurde hier nachgewiesen, dass Oomyceten, ebenso wie andere Pilzarten, die Parameter der Blätter beeinflussten und sich positiv auf den Fraß von Gammarus auswirkten. Das deutet darauf hin, dass Oomyceten einen größeren Einfluss auf die Laubdekomposition in Süßgewässern haben als bisher angenommen. Um die Effekte der Auswaschung die der Besiedlung durch Pilze und Oomyceten experimentell zu trennen, wurden Versuche durchgeführt, in denen die einzelnen Isolate auf autoklaviertem Laub wuchsen und die Effekte der einzelnen Pilze und Oomyceten auf die Blattparameter und den Fraß durch G. roeselii untersucht wurden. Im Vergleich zu den Kontrollen, führte der Großteil der unterschiedlichen Pilze und Oomyceten auf Laub zu erhöhten Fraßraten von G. roeselii. Die Blattparameter N, C, P, Protein und Polyphenol wurden spezifisch durch die einzelnen Isolate beeinflusst. Die statistische Auswertung mit einem linearen Modell machte deutlich, dass die Gehalte an Polyphenol und Protein die bestimmenden Faktoren für die Fraßrate von Gammarus waren. Dies deutet darauf hin, dass Pilze und Oomyceten die Konsumption indirekt steuern können, indem sie den Protein- und Polyphenolgehalt des Laubes ändern. Um die Hypothese zu untersuchen, dass die isolat- spezifische Präferenz von G. roeselii durch Attraktantien und Repellentien der Pilze oder Oomyceten hervorgerufen wird, wurden ausgesuchte Pilz und Oomyceten Isolate entweder in synthetischem oder in Blattextraktmedium herangezogen. Die Mycelien wurden mit den Lösungsmitteln Methanol oder Dichlormethan:Methanol (2:1, v:v) extrahiert. In Futterwahlversuchen mit G. roeselii und Laub, das mit diesen Extrakten behandelt wurde, erwiesen sich die Methanolextrakte als abschreckend, und die Lipid Extrakte hatten keinen Effekt auf die Präferenz von G. roeselii. Diese Ergebnisse stehen im Gegensatz zu den Effekten der einzelnen Isolate auf Laub und deuten darauf hin, dass andere Inhaltstoffe als Lipide oder die durch Methanol extrahierten die Präferenz von G. roeselii vermitteln. Der abschreckende Effekt der Extrakte aus Pilzen und Oomyceten wurde stark durch die Art der Kohlenstoffquelle im Wachstumsmedium beeinflusst. Die benthische Myside L. benedeni ist erst kürzlich in den Bodensee eingewandert. Hier konnte in kontrollierten Laborexperimenten gezeigt werden, dass diese Myside sowohl kurz als auch intensiv ausgewaschenes Laub von unterschiedlichen Baumarten frisst. Die Interaktion der gemessenen Blattparameter Kohlenstoff- und Polyphenol-Gehalt erklärte 74% der Attraktivität des Laubes für die Myside, was darauf hinweist, dass der Fraß von L. benedeni durch Wachse und das Cutin der Cuticula und durch die Lignocellulosestruktur des Blattes behindert wird. Im Vergleich zu Litoral exponiertem und autoklaviertem Laub, lösten 3 Pilze, die auf dem Laub wuchsen, eine intermediäre Fraßaktivität bei L. benedeni aus. Dies lässt vermuten, dass L. benedeni die unterschiedlichen mikrobiellen Besiedler des Laubes unselektiv frisst. Hier wurde zum ersten Mal gezeigt, dass L. benedeni ein benthischer Laubkonsument ist, der die Laubzersetzung im Bodensee potentiell fördern könnte.

Fachgebiet (DDC)
500 Naturwissenschaften
Schlagwörter
Pilze, Oomyceten, Laubzerkleinerer, Futterwahl, Dekomposition, Gammarus, Gammarus roeselii, Amphipode, invasive Art, Limnomysis benedeni, Fungi, oomycetes, leaf shredder, food selection, decomposition, Gammarus, Gammarus roeselii, amphipod, invasive species, Limnomysis benedeni
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ISO 690ASSMANN, Christine, 2010. Direct and indirect effects of fungi and oomycetes on leaf litter degradation by freshwater macroinvertebrates [Dissertation]. Konstanz: University of Konstanz
BibTex
@phdthesis{Amann2010Direc-6705,
  year={2010},
  title={Direct and indirect effects of fungi and oomycetes on leaf litter degradation by freshwater macroinvertebrates},
  author={Aßmann, Christine},
  address={Konstanz},
  school={Universität Konstanz}
}
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In addition to leaf toughness the bulk leaf parameters N-, C-, P-, protein- and polyphenol content were measured and the ergosterol content was determined by HPLC. Consumption rates of littoral exposed leaves were statistically analysed for effects of leaf parameters using permutation based tests and a linear model approach. In both experiments leaf parameters changed and consumption by G. roeselii increased significantly with conditioning in the littoral. The negative correlation of polyphenols with shredder feeding corroborated the known repellence by polyphenols. Notwithstanding studies by others the N- and the protein content decreased over the first time of exposure in the littoral, which suggested that leaf colonising micro-organisms (fungi and oomycetes) could not compensate for leaching of N-containing constituents. In both exposition experiments increasing ergosterol content over exposition time pointed at increasing metabolically active eumycotic fungal biomass on the littoral-exposed leaves, and therefore aquatic fungi and oomycetes were isolated from leaves.The fungal and oomycete isolates were cultured and identified based on the sequence of internal transcribed spacer (ITS) regions of rDNA, and the sequences obtained during these studies were deposits into GenBank®. In freshwaters, fungi are regarded as the most important microbial component on decaying leaves, and here 9 ascomycete and 4 oomycete strains were isolated from conditioned leaf litter. Here, for the first time, oomycetes were demonstrated to affect leaf parameters to a similar extent as other fungal strains and to positively affect consumption by Gammarus, which suggest that oomycetes have a greater impact on leaf litter decomposition in freshwaters than hitherto assumed. In order to experimentally separate effects of leaching and colonisation by fungi or oomycetes, experiments with single isolates growing on autoclaved leaves were performed, in which effects of single strains on leaf parameters and on consumption by G. roeselii were assessed. The majority of the different fungi and oomycete isolates on leaves were significantly preferred over controls, and consumption rates by G. roeselii proved to be strain-specific. The leaf parameters N, C, P, protein and polyphenol were affected by colonisation with single isolates, and the magnitude of the effects was strongly strain-specific. Statistical analysis with a linear model revealed that polyphenol and protein levels were major determinants of the consumption rate of Gammarus, suggesting that fungi and oomycetes might indirectly steer consumption by altering the leaf litter content of protein and polyphenols, in particular during later stages of conditioning in the field. Shredders discriminate between leaves colonised by different fungal and oomycete species, but mechanistically, the mediation of preference by fungi on leaves is not well understood. In order to test the hypothesis, that the strain-specific preference of G. roeselii is mediated by attractants or repellents that are constituents of fungi or oomycetes, selected fungal and oomycete strains were grown either in synthetic or leaf extract medium. Mycelia were extracted with solvents methanol or methylene chloride:methanol (2:1, v:v). Leaves covered with these extracts were subjected to choice feeding assays with G. roeselii. Methanol extracts proved to be repellent, and lipid extracts had no effect on the preference of G. roeselii. These results were contrary to the effects of the single isolates on leaves and suggested that compounds others than lipids or those extracted by methanol mediated the preference of G. roeselii. The repellent effect of the extracts of fungi or oomycetes was strongly affected by the C-source in the growth medium. The benthic mysid L. benedeni has recently invaded Lake Constance. Controlled laboratory experiments revealed that this mysid fed as well on shortly as well as on extensively leached leaf litter of several tree species. The interaction of the measured leaf parameters C- and polyphenol content explained 74% of the attractiveness of the leaf litter for the mysid, which suggested that feeding of L. benedeni is hindered by the waxes and cutin of the cuticula and by the lignocellulose structure of the leaf. 3 fungi growing on leaves elicited an intermediate feeding activity by L. benedeni, compared to that of littoral-exposed and autoclaved leaf litter. This suggests that L. benedeni feeds unselectively on the different microbial colonisers on decaying leaves. 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