Antarctic Fish Biology. Evolution in a Unique Environment

321 Pages·1993·11.93 MB·English

by  Joseph T. Eastman (Auth.)

Antarctic
Fish Biology
Evolution in a Unique Environment
Joseph T. Eastman
Department of Biological Sciences
Ohio University
Athens, Ohio
Illustrations and graphics by Danette Pratt
Photography by William Winn
Academic Press, Inc.
Harcourt Brace & Company
San Diego New York Boston London Sydney Tokyo Toronto
Front cover photograph: Ultrastructure of the liver of Dissostichus mawsoni showing lipid
droplets in darkly stained perisinusoidal cell and in hepatocytes. For details see Chapter 10,
Figure 8.
Front cover illustrations (top to bottom):
Cottoperca gobio. For details see Chapter 6, Figure 1, part B. From Regan (1913), reproduced
by permission of the Royal Society of Edinburgh from Trans. R. Soc. Edin., Vol. 49, plate IV,
Figure 3.
Deep-dwelling bathydraconid Bathydraco scotiae. For details see Chapter 6, Figure 9, part D.
From Regan (1913), plate IX, Figure 4, see above reference.
Benthic Trematomus bernacchii. For details see Chapter 6, Figure 5, part C. From Boulenger
(1902). Pisces. In "Report on the Collections of Natural History Made in the Antarctic Regions
During the Voyage of the 'Southern Cross,"' pp. 174-189. British Museun (Natural History),
London.
Pelagic Cryodraco antarcticus. For details see Chapter 6, Figure 11, part B. From Regan
(1914). Fishes. Br. Antarct. ("Terra Nova") Exped. 1910, Nat. Hist. Rep., Zool., 1: 1-54.
This book is printed on acid-free paper. @)
Copyright © 1993 by ACADEMIC PRESS, INC.
All Rights Reserved.
No part of this publication may be reproduced or transmitted in any form or by any means,
electronic or mechanical, including photocopy, recording, or any information storage and
retrieval system, without permission in writing from the publisher.
Academic Press, Inc.
1250 Sixth Avenue, San Diego, California 92101-4311
United Kingdom Edition published by
Academic Press Limited
24-28 Oval Road, London NW1 7DX
Library of Congress Cataloging-in-Publication Data
Eastman, Joseph T.
Antarctic fish biology : evolution in a unique environment / by
Joseph T. Eastman.
p. cm.
Includes bibliographical references (p. ) and index.
ISBN 0-12-228140-3
1. Fishes— Antarctic regions. 2. Fishes—Antarctic regions-
-Evolution. 3. Fishes—Antarctic regions—Physiology. 4. Fishes-
-Antarctic regions—Adaptation. I. Title.
QL637.2.E2 1993
597.092'4—dc20 92-43103
CIP
PRINTED IN THE UNITED STATES OF AMERICA
93 94 95 96 97 98 E B 9 8 7 6 5 4 3 2 1
Preface
Antarctica and its fauna command increasing attention in a world aware of
global climatic change, destruction of natural habitat, and loss of biological
diversity. The Southern Ocean surrounding Antarctica is an enormous ma­
rine habitat, about one-tenth of the world's ocean. Fishes are an integral
component of this ecosystem, which includes subzero coastal waters that, as
recently as 100 years ago, were thought to be devoid of this vertebrate group.
The fauna is dominated by the notothenioids, an endemic perciform sub­
order that has undergone considerable phyletic, ecological, and physiological
diversification. They occupy a noteworthy extreme in the spectrum of habi­
tats where we find fishes.
My goal is to give the reader an appreciation for the biology of Antarctic
fishes and why they hold the interest of those of us who study them. To do
this we must know something about the past and present environments of
Antarctica, why notothenioids prevail in the modern fauna, and what evolu­
tionary modifications are characteristic of life under Antarctic conditions.
The focus of this book is sufficiently broad to relate to some of the major
areas of inquiry in modern comparative biology. Although our knowledge is
far from complete, I have used notothenioids as subjects in evaluating paleo-
climatic influences on faunal change, the utility of cladistic methodology in
the analysis of relationships, the roles of vicariance and dispersal in the origin
of the fauna, and physiological adaptations to an unusual environment.
This book, consisting of three parts, addresses aspects of the biology of
Antarctic fishes with emphasis on the organismal biology of notothenioids
and especially on the speciose family Nototheniidae. The first part (Chapters
1-3) contains a general introduction to Antarctica and the Southern Ocean,
a summary of the geologic and climatic history of Antarctica, and a review of
the fossil fish faunas of Antarctica. The second part (Chapters 4-8) deals with
the modern fish fauna especially notothenioids. Topics include distribution,
taxonomic composition, systematic relationships, and Zoogeographie origins.
This part also includes Chapter 6 on what we might call the general biology
of notothenioids emphasizing ecological diversification, and including the
non-Antarctic members of the suborder. The third part, encompassing Chapters
9-14, focuses on organismal and organ system adaptation in notothenioids.
XI
xii Preface
As the term is used here, adaptation means evolutionary adjustment of the
morphology, physiology, and ecology to the environment. We have good
examples of adaptation in notothenioids, with antifreeze glycopeptides prob­
ably the most striking. I have tried, however, to avoid an overtly adaptationist
slant because some derived conditions ("adaptations") do not have a func­
tional explanation and may simply reflect phyletic inertia or chance muta­
tion. There is no evidence, for example, that a persistent Root effect is adap­
tive in the absence of a rete mirabile or that the hemoglobinless condition in
channichthyids is adaptive in light of the array of cardiovascular alterations
necessary to compensate for the absence of respiratory pigments. I have
concentrated on the evaluation of physiological characters as related to their
phyletic distribution. I have done this by mapping some physiological characters
on cladograms constructed from other data.
Chapters 12-14 cover the muscular, cardiovascular, and nervous systems
of notothenioids. Some chapters begin with an anatomical description of the
system. Rather than emphasizing physiological mechanisms, I have at­
tempted to interpret notothenioid physiology in a phyletic and ecological
context. The two published proceedings of the quadrennial Antarctic Fish
Biology Conferences at Ravello, Italy, have provided an excellent forum for
specialists to periodically review notothenioid physiology and biochemistry.
It is hoped that these meetings and this tradition will continue.
Publication of Fishes of the Southern Ocean (Gon and Heemstra, 1990) has
eased my task, and I have relied heavily on the material in this comprehensive
and useful book. In the interest of nomenclatural stability and because I favor
a relatively conservative taxonomic approach, I have followed Fishes of the
Southern Ocean in all matters of taxonomy and systematics. Since plans call for
revising Fishes of the Southern Ocean at 10-year intervals, we will have stability
as well as a vehicle for change.
There are areas that will not be covered in this book; some are treated in
Karl-Hermann Kock's Antarctic Fish and Fisheries (Cambridge University Press,
1992). I have not dealt with these topics: age and rate of growth, larval fish
biology, reproduction and fecundity, fishery statistics, many dietary studies, and
most taxonomic controversies.
This book is intended for ichthyologists wishing to become familiar with
notothenioids and their life in a biologically unique environment. Many
scientists working in the Antarctic have a general interest in Antarctic biolo­
gy that extends beyond their specialty. I hope this book will satisfy their need
for an overview of the fishes. It may also appeal to a broader audience of
marine biologists and general biologists wishing to learn about the ichthyo-
fauna, its history, and its adaptation to the Antarctic environment.
My own research on notothenioids has been focused primarily on species
available in McMurdo Sound. I am most grateful to colleagues and museum
Preface xiii
curators for the gift or loan of specimens from other locations around Ant­
arctica and elsewhere in the Southern Hemisphere. I extend my thanks to
Louise Barber, McMaster University, Hamilton, Ontario; Arthur DeVries,
University of Illinois, Urbana; Hugh DeWitt, University of Maine, Orono;
Martin F. Gomon, Museum of Victoria, Melbourne; Gerd Hubold, Institut
fur Polarökologie, Universität Kiel; T. Iwamoto, California Academy of Sci­
ences, San Francisco; Susan L. Jewett, Smithsonian Institution, Washington,
DC; Karl-Hermann Kock, Institut für Seefischerei, Hamburg; F. Patricio
Ojeda, Pontifica Universidad Católica de Chile, Santiago; German Pequeno,
Universidad Austral de Chile, Valdivia; Jeffrey A. Seigel, Natural History
Museum of Los Angeles County; M. Stehmann, Zoologisches Museum, Uni­
versität Hamburg; Andrew Stewart, National Museum of New Zealand, Well­
ington; Martin White, British Antarctic Survey, Cambridge; and Richard
Williams, Australian Antarctic Division, Kingston, Tasmania.
I am fortunate to have had expert help in the preparation of the figures.
Danette Pratt produced some original artwork and modified many existing
figures for use in this book. Most photographs are the work of William
Winn. Tim Creamer, Robert Hikida, John Sattler, and Hans Ramlov also
contributed photographs. James Eastman of Weston Engraving in Min­
neapolis was especially helpful in converting some color figures to black and
white. This book would not have been possible without the contributions of
these people and I am most grateful to them.
For their advice and criticism on various chapters I thank Mary Cham-
berlin, Robert Hikida, Michael Lannoo, Hans Ramlov, and Michael Rowe.
Scott Moody was a source of advice on cladistic matters.
Finally, it is a pleasure to thank Mary Kay, Erik, and Erin for their encour­
agement and support.
1
Physical and Biological
Characteristics of the Antarctic
Marine Environment
^f JfcM^i^; -,, > I· The Antarctic Continent
wHM J The Antarctic landmass covers 14 million km 2, about twice
^F the size of Australia, and is isolated by large expanses of cold ocean
from all other land except the southern tip of South America (Fig. 1.1). The
Transantarctic Mountains divide the continent into a larger East Antarctica
and a smaller West Antarctica, the latter located entirely within the Western
Hemisphere (Fig. 1.2). Partially detached from the rest of the continent by
the embayments of the Weddell and Ross Seas, West Antarctica is a moun­
tainous area that includes the Antarctic Peninsula. For Zoogeographie pur­
poses the Weddell and Ross Seas are considered to be allied with East Antarc­
tica (Nybelin, 1947, 1952; DeWitt, 1971).
A. Climate
Continental temperatures are usually below 0°C throughout the year in most
interior as well as in some coastal regions. The world's record low tempera­
ture of -89.6°C was recorded at the U.S.S.R. Vostok Station in 1983 (Phill-
pot, 1985). The South Pole receives only trace amounts of snowfall; coastal
regions have 40-100 cm yr_1.
Antarctica has a few small, ice-covered lakes with simple ecosystems that
do not include fishes. There were freshwater fishes living on the continent
180 million years (m.y.) ago, but the modern fauna is exclusively marine. The
cold, windy, and arid climate precludes the existence of fishes on the conti­
nent today.
B. The ice sheet
Over millennia accumulated snow has become transformed into a massive
continental ice sheet. This sheet averages 2160 m in thickness and covers all
3

I. The Antarctic Continent 5
Figure 1.2 Antarctica with major geographic features mentioned in the text. Scientific sta­
tions are also indicated. The Antarctic Circle is located at 66.5°S. From Weller et al. (1987) with
permission of the author and the American Association for the Advancement of Science, copy­
right 1987 by the AAAS.
but 2.4% of Antarctica (Drewry, 1983). The weight of the ice has depressed
both the continent and continental shelf by several hundred meters. There­
fore a considerable portion of the Antarctic landmass lies below sea level.
Some high mountain ranges project over 2000 m above the surface of the ice.
The ice sheet contains glaciers in mountainous areas and is continuous with
large ice shelves in the Weddell and Ross Seas. Ice shelves comprise about
44% of the Antarctic coastline (Drewry, 1983) and receive drainage from
about 62% of the surface area of the ice sheet (Anderson, 1991).
<
Figure 1.1 Antarctica and the Southern Ocean in relation to other continents and the world's
ocean. This view centered on the South Pole emphasizes the isolation of Antarctica, the continu­
ity of the oceans, and the differences between the Antarctic and Arctic Regions in the disposition
of land and water. Redrawn from Spilhaus (1976) with permission of H.S. Borst/Marsh Commu­
nications, Inc., Mount Kisco, NY.
6 1 The Antarctic Marine Environment
Antarctica has a polar glacial regime, meaning ice is lost as bergs from the
periphery of ice shelves rather than by the melting characteristic of a temper­
ate glacial marine setting such as the Gulf of Alaska (Anderson, 1991). Ice
shelves move seaward at about 1 m day-1 (Foster, 1984) to eventually calve
tabular icebergs at their margins. About 1450 km3 (Kennett, 1982) or, more
impressively, a trillion (1012) tons (Radok, 1985) of ice is discharged annually
from the Antarctic continent. In 1987 a 5000-km2 iceberg, slightly smaller
than the state of Delaware, separated from the Ross Ice Shelf (Maslanik and
Barry, 1990). Most ice is transported from the interior of the continent by ice
streams—fast moving, 30- to 80-km-wide regions of ice within the ice sheet
(Weller et al, 1987). Measurements made through boreholes in a rapidly
moving (1.2 m day-1) ice stream in West Antarctica indicate that the base
is close to the melting point of ice and that basal water pressure is near the
ice overburden pressure. Therefore the stream probably moves by basal slid­
ing and by deformation of water-saturated subglacial till (Engelhardt et al,
1990).
Under reasonably constant climatic conditions over centuries, the mass of
the ice sheet is balanced by gain through addition of snow at the interior of
the continent and by loss through ablation (evaporation) and discharge of ice
at the periphery of the continent. There is negligible melting of ice on the
continent; however, the ocean plays an important role in melting ice on the
underside of ice shelves (Gordon, 1988). A scenario involving global warming
predicts increased seaward movement and loss of mass from the ice sheet
with a subsequent rise in sea level. The East Antarctic ice sheet is largely
terrestrial and probably developed prior to the West Antarctic ice sheet.
Since the West Antarctic ice sheet is mostly marine and below sea level, it
might be more sensitive to climatic warming than the East Antarctic ice
sheet. If the West Antarctic ice sheet thinned and retreated, more ice would
be discharged into the ocean (Weller et al, 1987). There is no evidence that
the Antarctic ice sheet, as a whole, is shrinking. However, many researchers
believe that some parts of the West Antarctic ice sheet exhibit changes indic­
ative of possible collapse, and that the situation should be closely monitored
(Bindschadler, 1990).
Katabatic winds are another characteristic feature of Antarctica. The
continent has an average elevation of over 2000 m (Phillpot, 1985). Dense
cold air from the elevated continental plateau spills down slope, under the
influence of gravity, to the continental margin. When channeled through
narrow valleys, these winds reach gale force at the coastline, sometimes
exceeding 50 m s-1 (Drewry, 1987). In some areas pack ice is blown away
from the coast creating areas of open water 50 to 100 km wide known as
coastal polynyas.
II. The Marine Environment 7
II. The Marine Environment
A. The Southern Ocean
An enormous expanse of cold seawater surrounds the continent as the South­
ern Ocean (Figs. 1.1, 1.3, and 4.1). This is the habitat of modern Antarctic
fishes, an exclusively marine fauna. The Southern Ocean may be thought of
Figure 1.3 Antarctica and the surrounding Southern Ocean. Limited shallow water habitat is
indicated by the dashed line of the 1000-m isobath. A heavy line indicates the position of the
Antarctic Convergence (Antarctic Polar Front), an important océanographie and Zoogeographie
boundary. Base map from DeWitt (1971) and location of the Convergence from Hedgpeth
(1969). Modified from Eastman and DeVries (1986a), copyright © 1986 by Scientific American,
Inc. All rights reserved.