Table Of ContentEcological Studies
Analysis and Synthesis
Edited by
W. D. Billings, Durham (USA) F. Golley, Athens (USA)
O. L. Lange, Wiirzburg (FRG) I. S. Olson, Oak Ridge (USA)
H. Remmert, Marburg (FRG)
Volume 54
Karsten Reise
Tidal Flat Ecology
An Experimental Approach
to Species Interactions
With 69 Figures
Springer-Verlag
Berlin Heidelberg New York Tokyo
KARSTEN REISE
Litoralstation
D-2282 List/Sylt, FRO
ISBN -13: 978-3-642-70497-0 e-ISBN-13: 978-3-642-70495-6
DOl: 10.1007/978-3-642-70495-6
Library of Congress Cataloging in Publication Data. Reise, Karsten. Tidal flat ecology. (Ecological studies; v.54).
Bibliography: p. Includes index. I. Tidal flat ecology. I. Title. II. Series. QH541.5.S35R45. 1985.574.5'2636.85-2859.
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© by Springer-Verlag Berlin Heidelberg 1985
Softcover reprint of the hardcover I st edition 1985
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2131/3130-543210
Preface
The tidal coastline presents a fascinating ecological world. Rocky
shores with their recurrent zonation of algae and sessile invertebrates
demonstrate the orderliness of nature, apparently obeying general explan
atory principles. The niche theory could just as well have hatched out of
the tight species-packing on the coral reef flats. Fluxes of carbon and
nitrogen are best studied in mangroves and salt marshes with their
outstanding primary productivity; the bare mud and sands of the tidal
flats are different. Their ecological treasures are well concealed, and
perhaps not to everybody's taste. Pick up a piece of tidal sediment and see
how it resembles a large, rotten cheese! It smells, is slimy and sticky, is
punched with holes and crowded with various worms.
Tidal flats receive detritus from both the land and the sea. They sup
port a rich benthic community which attracts birds from far distant
breeding grounds, and serves as a nursery for crabs, shrimp and fish. Tidal
flats are a busy ecological turntable. They import low valued organic
matter, and they export well-fed birds to the land and grown-up fish to the
sea. They offer ideal opportunities for aquaculture but are also used as
dumping grounds for industrial wastes. All this may call for a marine
ecologist to investigate the basic processes involved. Yet there is still
another reason. The tidal sediments are inhabited by a marine fauna
which elsewhere can only be studied from a ship with remote sampling
gear or by diving. Particularly when it comes to field experiments, the
ready accessibility to tidal flats is a major advantage. The main topic of
this book is field experiments on the role of species interactions in shaping
the tidal flat communities. I believe that many of the phenomena revealed
by these experiments also occur in the sediments covered permanently by
the sea. Thus, marine ecologists who lack the funds for the sophisticated
technology needed out on the sea are invited to accept the tidal flats as a
convenient substitute for carrying out their next experiments.
This book is based on 10 years of experimental experience with mud,
sand and worms in the European Wadden Sea. In these experiments out
on the flats, some community components are added or removed, and the
response of the others is compared to natural control conditions. Such
field experiments have the potential to reveal the kind and strength of
VI Preface
interactions between the various parts of a community, they may uncover
hidden relationships, and eventually offer predictions on future composi
tions of the species assemblage. They are primarily a tool for the analysis
of the qualitative properties of ecological systems, and thus provide a
necessary complement to the quantifications of energy flow, nutrient
cycling and production. These experiments in the field are always an
adventure. The natural course of events all too often tilts even the best
experimental design. Instead of straight answers to the experimental
interventions, the complexity of the interactions surprises us with riddles.
Detailed knowledge of the biology of all the species involved is required to
extract the most parsimonous interpretation, and usually auxiliary
experiments are needed.
The interactions between the constituent species on the tidal flats are
not chaotic but they undoubtedly lack perfection. As a consequence, it is
inherently impossible to arrive at clearcut conclusions about their pattern.
What can be said is simply that certain sequences of events are more likely
to occur than others, but it is never possible to reject some other sequence
once and for all. A hesitating and pedantic personality might easily get lost
in this ecological realm. In the following text I do not hesitate to express
my opinion in the face of uncertainty, and it thus goes without saying that
none of the pages should be read uncritically. The book is not a definitive
summary of facts but rather a starting point for more comprehensive
research on the tidal flat ecotone.
Although the tidal zone is physically a harsh environment for the
marine organisms, these nevertheless interact strongly with each other,
albeit in an unrefined manner. Predation is identified as the prevailing
process, keeping infaunal densities below carrying capacity. On the other
hand, amelioration of the sediment brought about by members of the
large burrowing infauna affects the small organisms positively. Compe
tition seeins to have little effect on the shape of the tidal flat community.
The first three chapters are an attempt to provide a general introduc
tion to tidal flat ecology. This is followed by a description of the
experimental area and its biota in the northern part of the Wadden Sea.
The main part ofthe book is about field experiments designed to reveal the
most important interactions. I begin with methodological considerations,
followed by chapters on the role of various groups of predators and how
prey populations get along with them. As a balance to these negative
effects on the benthic fauna, I present other experiments where positive
effects of irrigation and fertilization of the sediment by some organisms is
beneficial to the others. In two final chapters, I propose a synthesis of all
the known interactions between tidal flat organisms.
Preface VII
Acknowledgements
I wish to thank Hermann Remmert who suggested that I write this
volume. To Peter Ax I am deeply grateful for his vital encouragements and
for clearing my mind when I could not decide between alternate concepts
for the book. Wieland Riesen helped enormously with the drawings,
spotted various errors in the manuscript and brought order into chaotic
sentences. Ragnhild and Harald Asmus provided several substantive
comments on the manuscript and I am thankful to their never-expiring
readiness to discuss several topics of the book. The students associated
with my laboratory during the experimental work and the writing of
the book often served as a critical sounding board when I bothered them
with my premature ideas. They contributed in many ways to the
development of the text and I want to express my thanks to Werner
Armonies, Christine Buchholz, Elke Debus, Sabine Dittmann, Monika
Hellwig, Markus Hiittel, Klaus Kossmagk-Stephan, Uwe Noldt, Libia
Pardo M., Petra Potel, Roberto Quinones D., Silke Riebensahm, Bernd
Schade, Bernd Scherer, Andreas Schubert, Christian Wehrenberg, Willi
Xylander and Marianne Zocher. I am grateful to them all. None of
the work synthesized in this volume would have been possible without
the generous support of the German Research Federation (DFG), and
the Biologische Anstalt Helgoland (BAH) povided superb laboratory
facilities. The cooperation with Springer-Verlag was a pleasure.
Finally, I wish to dedicate this volume to a permanent resident of
the coastal waters at the island of Sylt, for his benevolence as well as for
his pranks he played on my experiments, to the cheerful merman Ekke
Nekkepenn.
Island of Sylt, North Sea KARSTEN REISE
February 1985
Contents
1. Introduction. . . . . . . . . . . . . . . . . . . 1
1.1 The Beginnings of Research in Tidal Flat Ecology 1
1.2 Field Experiments on Tidal Flats . . . . . . . 3
The Tidal Flat Ecotone
2. Tides, Sediments, and the Distribution of Organisms 9
2.1 Tides and Sediments . 9
2.2 The Distribution of Organisms 11
3. Biogeochemistry of Tidal Sediments. 17
3.1 The Vertical Chemocline 17
3.2 Burrows and Pellets 21
4. Living in Tidal Sediments . 25
4.1 Low Tide Endurance, A voidance, and Peference 25
4.2 Production and Consumption of Biomass 29
5. The Tidal Flats of K6nigshafen 35
5.1 The Environment 35
5.2 The Biotic Community 38
Experiments on Tidal Flats
6. Some Problems of Methodology 57
6.1 General Considerations. . 57
6.2 The Methodology of Caging 59
7. Exclusion of Large Fish and Birds 63
7.1 Effects on Macrofauna . . . 63
7.2 Effects of Grazing . . . . . 69
7.3 Moderate Effects on the Benthos 70
8. Predation by Crabs, Shrimp, and Small Fish. 75
8.1 Predator Additions. . . . . . . . . . 75
x
Contents
8.2 Associated Predators. . . . 79
8.3 Predator Removals. . . . . 83
8.4 Predation in the Tidal Nurseries 96
9. Endobenthic Predation . . . . . . 101
9.1 Carnivores Within the Tidal Sediments 101
9.2 Predator Additions and Removals 103
9.3 Multiple Predation on Tidal Flats 106
10. Prey Dynamics and Predator Impact 108
10.1 Cockles . . . . . . . . . 108
10.2 Lugworms . . . . . . . . 114
11. Macrofauna Promotes Meiofauna 119
11.1 Promotive Bivalves. . . . . 120
11.2 Meiofauna at Lugworm Burrows 126
11.3 Removal of Lugworms . . . . . 136
12. Interactions in the Biotic Assemblage . 146
12.1 A Conceptual Hierarchy of Ecological Processes 146
12.2 Promotor Effects 148
12.3 Consumer Effects . . . . . . 151
12.4 Competition . . . . . . . . 153
13. The Open Community on Tidal Flats 158
13.1 An Ecological Turntable . . . 158
13.2 Low Connection Between Species 160
13.3 The Prevalence of Predation. 162
References 167
SUbject Index 183
1. Introduction
Tidal flats are marine sediments regularly exposed and submerged by
the tides, and which gently slope towards the sea. Occasionally they oc
cupy up to 20 km between the tidemarks, as in the European Wadden Sea,
but more often tidal flats are restricted to a narrow fringe between the
landward marsh grasses or mangroves and the permanent realm of the
sea. Tidal flats constitute a transition zone - an ecotone - between the
land and the sea, where the biotic elements of the sea clearly dominate.
In estuaries, the flats are subject to strong salinity fluctuations. At high
latitudes ice cover may last several months, and in regions with an arid
climate the daily change in temperature is difficult to endure by the ma
rine inhabitants.
In spite of this, harshness and environmental variability are not the
only characteristics of this ecotone. Compared to the land, the biomass
of invertebrate life is very high and this attracts flocks of birds to the tidal
flats. Compared to the sea, benthic microalgae are more important than
the plankton as food for the sediment-dwelling animals. On the shallow
flats, young fish, little crabs, and small shrimp find ample food, and here
they are safe from their marine predators. Thus, tidal flats are important
nurseries for populations in which the adults live out in the sea. Besides
these characteristics, tidal flats have many species and ecological pro
cesses in common with the adjacent subtidal sedimentary habitats.
1.1 The Beginnings of Research in Tidal Flat Ecology
Historically, tidal flats remained for long the muddy backwaters of
marine ecological research. Compared to the vastness of the open sea,
tidal flats seemed to be a negligible fringe, full of aberrant phenomena un
worthy of attention to a science concerned with the world's largest ecosys
tem. Being neither sea nor land, with most of the organisms hidden inside
the sediment and tedious to extract, with no inviting place to sit down and
reflect for a while, the sediments between the tidemarks and the turbid
tidal waters attracted few scientists. Indeed, by all standards, tidal flat
2 Introduction
ecologists appear somewhat backward: they have neither ship nor diving
gear at their disposal, but walk out in rubber boots with a spade in one
hand and a bucket in the other as if to collect potatoes; and when they
come back from their field work, they are besmeared all over with the
sticky mud and yet confess they love it. This does not resemble exact sci
entific endeavor seeking the unifying laws of nature.
Natural histories of prominent species dwelling on the tidal flats were
already written in the preceding century, but ecological research con
cerned with the entire biota of tidal flats started only about 50 years ago.
A British school of investigators emphasized the zoned pattern of the
fauna from high tide line towards low tide line (i.e., Bean1and 1940, Brady
1943, Stephen 1929, 1930, Watkin 1942, summarized in Eltringham 1971).
These studies paralleled earlier work on the rocky shore.
In the Wadden Sea, where many of the tidal flats extend several kilo
meters out into the sea, Wohlenberg (1937) and Linke (1939) made at
tempts to identify species associations on the tidal flats, and to link these
with subtle environmental differences or with postulated competitive re
lations. This line of research was inspired by phytosocio10gica1 studies on
terrestrial vegetation. Remane (1940) summarized this work with addi
tional notes on the distribution of the small interstitial fauna.
Apparently the first to recognize the significance of tidal flats as the
nurseries for many commercially important fish was Biickmann (1934).
Thamdrup (1935) pointed out that while there are relatively few species
on tidal flats, numbers of individuals and biomasses are very high. Where
conditions are harsh and variable, small-sized individuals dominate, and
where the flats are more benign, the larger individuals prevail. Thamdrup
also determined the oxygen consumption per unit area as a measure of
community metabolism. In the same part of the Danish Wadden Sea,
Smidt (1951) studied comprehensively the amount of food produced for
bottom-feeding fish. He recognized the importance of the very small-sized
fauna, the meiofauna and juvenile macrofauna, for the consumption of
the young fish. He explained the seasonal decline of benthic populations
with fish predation.
The decisive role of bacteria for the properties of tidal flat sediments
and as food to benthic animals was first outlined by Zobell and Feltham
(1942). Very high values of primary production by benthic diatoms were
measured by Gmntved (1962). This initial measurement was an overesti
mate, but brought to attention that tidal flats differ fundamentally from
most permanently submerged sea bottoms by having a substantial au
tochthonous source of easily digestible unicellular algae.
Only gradually did it come to be comprehended that also birds affect
the benthic fauna of the tidal flats (i.e., Hancock and Urquhart 1965,
Drinnan 1957, Goss-Custard 1969). Since about the 1970's, almost all ma-
