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Bryozoans and microbial communities of cool-temperate to subtropical latitudes—paleoecological implications

II. Diversity of microbial fouling on laminar shallow marine bryozoans of Japan and New Zealand

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Abstract

Laminar bryozoans of shallow marine sites from cool-temperate to subtropical climate in Japan and New Zealand tolerated mainly agglutinated biofilms composed of diatoms, fungi, cyanobacteria and other bacteria as well as debris trapped in slimes. Also monobacterial films were relatively frequent on living bryozoans, while rigid, tangled mats of filamentous cyanobacteria mainly occupied surrounding substrates or dead bryozoan colonies. Three levels of microbial fouling low, medium and high were defined. Low-level fouling was more frequent on bryozoan colonies collected at warm-water settings, while medium levels became more frequent in cooler water. The decrease of microbial fouling towards lower latitudes parallels findings in part one of this study (Kaselowsky et al. 2004, this volume) in which bryozoan lamina types comparatively strong in overgrowth competition increased towards lower latitudes. Such morphological signals of competitive interaction of bryozoans and associated epizoic biofilms are potentially of paleoecologic value. Our collections from two different sampling periods revealed only small changes between seasons which may account for the predominance of oceanographic factors controlling shallow marine sampling sites around Japan and New Zealand coasts.

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Acknowledgements

We are grateful to D. P. Gordon (Wellington, New Zealand), K. P. Probert (Dunedin, New Zealand), S. F. Mawatari (Sapporo, Hokkaido, Japan), A. Gorbushina and K. Palinska (Oldenburg, Germany), R. Crawford and F. Hinz (Bremerhaven, Germany), for their help in species determinations and constructive discussions. In addition, we gratefully acknowledge the possibilities for carrying out some SEM microphotographs using a field emission scanning electron microscope kindly provided by the NASA JSC Astrobiology Institute, Houston (photograph courtesy of Prof. Dr. Penny Morris-Smith and Mrs. Teresa G. Langazo). The critical reviews of the manuscript by two anonymous reviewers were kindly appreciated. This study was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft) project GE 64/8-1, 64/8-2, cooperation projects no 446 JAP-113/216/0, 447 NSL-113/4/9, and by the Research Agencies of Japan (JSPS), and New Zealand (MREST).

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Authors and Affiliations

  1. Marine Laboratory, Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University of Oldenburg, Schleusenstr. 1, 26382, Wilhelmshaven, Germany

    Gisela Gerdes & Nicole Kadagies

  2. Department of Biology, James Madison University, Burruss Hall, MSC7801, Harrisonburg, VA, 22807, USA

    Antje Lauer

  3. Sektion Marine Evertebraten III, Forschungsinstitut und Naturmuseum Senckenberg, Senckenberganlage 25, 60325, Frankfurt, Germany

    Jürgen Kaselowsky & Joachim Scholz

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  1. Gisela Gerdes
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  5. Joachim Scholz
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Correspondence to Gisela Gerdes.

Appendices

Appendix A1: Glossary of terms used

Agglutinated biofilm

The main type of microbial build-ups in this study containing significant amounts of detrital components bound together by extracellular polymeric substances; see also EPS.

Biofilm

Aggregates of microbial cells developing at interfaces and embedded in a matrix of EPS. The biofilm organization provides advantages in terms of protection, synergisms, exchange of nutrients, signals and genes.

Common

Ecological term to characterize the estimated abundance of species within an association or assemblage of organisms: species relatively abundant but not dominant; see also rare.

Dominant

Ecological term to characterize the estimated abundance of species within an association or assemblage of organisms: a species or species group that is particularly abundant; see also common, rare.

Epizoic

Organisms living attached to the surface of metazoans.

EPS

Organic polymers of microbial origin which in biofilm systems are frequently responsible for binding cells and other particulate materials together and to the substratum (Characklis and Wilderer .1989)

Frequency

Estimations of the number of observations of a structure, species or taxon group in relation to the whole number of samples.

Microbial fouling

The attachment and growth of biofilms on submersed surfaces (modified after Glossary of Geology, Bates and Jackson 1987).

Microbial mat

Tangled, carpet-like cover of sedimentary surfaces produced by microbial communities in which species forming filamentous cell chains are dominant (e.g., cyanobacteria). Microbial communities in mat-like systems coexist in self-organizing patterns. Their metabolic interactions influence and imprint deeply the substrate on which they grow (Krumbein 1983).

Morphotype

The visible character of organismic structures that reflects the interaction of genotype and environment (bryozoans and biofilms in the study presented here).

Rare

Ecologic term used to characterize the estimated abundance of species within an association or assemblage of organisms; here: species that occur only in small numbers in relation to other members.

Stromatolite

Biolaminated rock. Lamina are built of tissue-like microbial mats (stroma).

Trapping

The ability of biofilms and microbial mats to trap sediments from near bottom fluids.

Appendix A2: Criteria used for the distinction of low, medium and high levels of bryozoan-associated microbial fouling, based on microscopic, microbiological and molecular data obtained in this study:

Low level fouling (Figs. 3a–b, d)):

  • proportion of zooid space covered by biofilms <50%

  • biofilm composition: mainly diffuse water-enriched slimes which agglutinate diatom debris, mineral particles and floccose organic matter (this type we term “agglutinated biofilm”); some few individual organisms are visible which are dispersed rather than colonially organized. Filamentous forms are rare.

  • biofilm consistency: low degree of cohesion

  • biofilm distribution on the zooids: patchy, inhomogenous

Medium level fouling (Fig. 3c):

  • proportion of zooid space covered by biofilms 50–75%

  • biofilm composition: while the category “agglutinated biofilm” (see above) is still dominant, colonial aggregates of organisms (both coccoid and filamentous) become increasingly abundant (Fig. 2b)

  • biofilm consistency: increasingly coherent

  • biofilm distribution on the zooids: increasingly homogenous, colonial aggregates of individuals of the same species occupy larger areas

High level fouling (Figs. 3f–g)):

  • proportion of zooid space covered by biofilms > 75%

  • biofilm composition: morphological heterogeneity due to filamentous and coccoid organisms

  • biofilm consistency: highly tangled and cohesive due to EPS enrichment including slimes, capsules and sheathes (Fig. 3g)

  • biofilm distribution: larger areas homogeneously covered

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Gerdes, G., Kadagies, N., Kaselowsky, J. et al. Bryozoans and microbial communities of cool-temperate to subtropical latitudes—paleoecological implications. Facies 50, 363–389 (2005). https://doi.org/10.1007/s10347-004-0037-2

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