Table Of ContentAnimal Energetics
VOLUME 2
Bivalvia through Reptilia
Edited by
T. J. PANDIAN
Department of Animal Sciences
School of Biological Sciences
Madurai Kamaraj University
Madurai, Tamilnadu, India
F. JOHN VERNBERG
Belle W. Baruch Institute for Marine Biology
and Coastal Research
University of South Carolina
Columbia, South Carolina
ACADEMIC PRESS, INC.
Harcourt Brace Jovanovich, Publishers
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COPYRIGHT © 1987 BY ACADEMIC PRESS. INC.
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United Kingdom Edition published by
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Library of Congress Cataloging in Publication Data
Animal energetics.
Includes index.
Contents: v. 1. Protozoa through insecta — v. 2.
Bivalvia through reptilia.
1. Energy metabolism. 2. Bioenergetics.
I. Pandian,T. J. II. Vernberg, F. John, Date
QP171.A67 1987 591.19Ί21 87-1170
ISBN 0-12-544792-2 (v. 2: alk. paper)
PRINTED IN THE UNITED STATES OF AMERICA
87 88 89 90 9 8 7 6 5 4 3 2 1
Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
Thomas H. Carefoot (89), Department of Zoology, University of British
Columbia, Vancouver, Canada V6T 2A9
Alan G. Clark (173), Department of Biochemistry, Victoria University of
Wellington, Wellington, New Zealand
Aline Fiala-Medioni (323), Universite P. et M. Curie (Paris VI), Laboratoire
Arago, 66650 Banyuls-sur-Mer, France
Dennis P. Gordon (173), New Zealand Oceanographic Institute, Division of
Marine and Freshwater Science, DSIR, Wellington, New Zealand
C. L. Griffiths (1), Zoology Department, University of Cape Town, Ron-
debosch 7700, South Africa
R. J. Griffiths (1), Zoology Department, University of Cape Town, Ron-
debosch 7700, South Africa
John F. Harper (173), Department of Mathematics, Victoria University of
Wellington, Wellington, New Zealand
Steven M. Jones1 (553), Department of Zoology, University of Wisconsin,
Madison, Wisconsin 53706
John M. Lawrence (229), Department of Biology, University of South Flor
ida, Tampa, Florida 33620
T. J. Pandian (357), Department of Animal Sciences, School of Biological
Sciences, Madurai Kamaraj University, Madurai 625 021, Tamilnadu,
India
Warren P. Porter (553), Department of Zoology, University of Wisconsin,
Madison, Wisconsin 53706
Present address: BCM Eastern Inc., One Plymouth Meeting, Plymouth Meeting, Pennsylva
nia 19462.
IX
X Contributors
Dianne B. Seale (467), Center for Great Lakes Studies, Department of Bio
logical Sciences, University of Wisconsin-Milwaukee, Milwaukee,
Wisconsin 53201
A. J. Southward (201), Marine Biological Association, The Laboratory, Cit
adel Hill, Plymouth PL1 2PB, England
Eve C. Southward (201), Marine Biological Association, The Laboratory,
Citadel Hill, Plymouth PL1 2PB, England
Steven R. Waldschmidt2 (553), Department of Zoology, University of
Wisconsin, Madison, Wisconsin 53706
2Present address: Department of Biology, Leidy Labs, University of Pennsylvania, Phila
delphia, Pennsylvania 19104-6018.
Preface
An ever-increasing number of papers are appearing in the scientific liter
ature that deal with the diverse facets of animal energetics. We felt there was
a decided demand for a treatise about this field of science that would not
only review and synthesize the existing literature but also stimulate the
future course of research by pinpointing gaps in our existing knowledge and
suggesting new topics for investigation.
Bioenergetics is the study of energy transformation in living systems, and
can be studied at various levels of biological organization: (1) molecular and
cellular; (2) organismic; and (3) population (ecosystem). This two-volume
treatise focuses primarily on the integrated picture of the energy transforma
tion process at the organismic level. As biologists readily recognize, howev
er, it is almost impossible (and not particularly desirable) to restrict mean
ingful discussions to only one level of organization. Hence, some reference
is made to population energetics as well as to the suborganismic level.
Bioenergetics of both vertebrate and invertebrate groups are discussed;
however, the warm-blooded vertebrates (birds and mammals) are omitted
because they have received more attention in the literature during recent
years.
The study of bioenergetics has implication for both basic science and
applied fields such as aquaculture. Brody (1945) in his classic book, "Bio
energetics and Growth," presented an integration of research on the ener
getic efficiencies of agricultural processes such as production of meat, milk,
and eggs, and muscular work in domestic mammals and birds. In develop
ing countries where undernutrition and malnutrition are chronic problems,
a pressing demand for low-cost, protein-rich food has clearly shown the
need for the rapid establishment of aquaculture. Although the principles
involved in the production processes of the shellfishes and fishes are almost
the same as in animal husbandry, the "domestication" of these animals
poses a different set of problems and requires a different management tech-
XI
xii Preface
nique. Indeed, the maintenance energy cost of these animals must the
oretically be lower, and hence the production efficiency is likely to be
higher. These thermoconformers incur almost no energy expenditure for the
maintenance of their body temperature; they inhabit a denser medium and
thus use less energy to support their body in comparison to their terrestrial
counterparts.
The application of the principles of thermodynamics to cells, organisms,
and communities is a recent concern, but one much entertained by nutri
tionists, biologists, physiologists, and ecologists. Understanding the efficient
and fast transformation of biological energy has become an important issue
in world affairs; studies on energetics and growth of thermoconformers can
therefore be expected to expand greatly in the future. We hope this book
will provide many keys to a broader understanding of biology and will open
untrodden avenues to biologists with the quest for newer energy sources and
efficient methods of energy utilization. Animal energetics is too important a
field to be ignored.
During the preparation of this book, we have received much assistance
and advice from several colleagues: B. J. Finlay, D. Schlichter, J. B. Jen
nings, J. J. Gilbert, R. Marchant, K. Fauchald, R. J. Conover, L. Schroeder,
B. L. Bayne, P. L. Calow, C. S. Hammen, G. Stephens, K. H. Mann, C. B.
Jorgensen, and A. Adeladie. Their criticisms and suggestions have done
much to improve this book, and we gratefully acknowledge them. In partic
ular, we want to thank Miss Anne B. Miller (Columbia) and Miss D. Bharathi
(Madurai) for their valuable assistance.
T. ). Pandian
F. lohn Vernberg
1
Bivalvia
C. L. GRIFFITHS and R. J. GRIFFITHS
I. Introduction
II. Feeding
A. Modes of Feeding
B. Measuring Feeding Rate
C. Efficiency of Particle Retention
D. Particle Selection and Pseudofeces Production
E. Relation to Body Size
F. Particle Concentration
G. Temperature
H. Tidal Exposure and Starvation
III. Absorption and Egestion
A. Methods of Measurement
B. Food Concentration
C. Body Size
D. Temperature
E. Nature of Diet
F. Feeding Periodicity
IV. Respiration
A. Measurement
B. Effects of Body Size
C. Activity Level
D. Temperature
E. Oxygen Availability
F. Aerial Exposure
G. Season
H. Salinity
V. Excretion
A. Nature of Excretory Products
B. Rates of Excretion
C. Temperature
D. Salinity
1
ANIMAL ENERGETICS, VOL. 2
Copyright © 1987 by Academic Press, Inc.
All rights of reproduction in any form reserved.
2 C. L. Griffiths and R. J. Griffiths
E. Tidal Exposure
F. Overall Excretory Output
VI. Production
A. Scope for Growth in Relation to Size and Ration
B. Scope for Growth and Temperature
C. Other Factors
VII. Somatic Growth
A. Methods of Measurement
B. Environmental Influences
VIII. Reproductive Output
A. Methods of Assessment
B. Reproductive Effort in Different Species
C. Relation to Size and Age
D. Environmental Influences
IX. Population Energy Budgets
References
I. INTRODUCTION
Bivalves dominate the macrofauna of many estuarine and coastal marine
systems and an understanding of their ecological role is crucial to analyses
of productivity and energy flow in such areas. Many species, notably
oysters, mussels, and clams, are also economically important and are fre
quently cultured, so that there is considerable interest in maximizing growth
and optimizing conversion efficiencies in these forms. Because of their dom
inance, ease of collection and maintenance, sessile mode of life, and filter-
feeding habits, bivalves are also popular experimental animals, particularly
for pollution studies. For these and other reasons much research has been
conducted into the physiology and ecological energetics of bivalves—prob
ably more than on any other invertebrate group outside the Arthropoda.
We have not in this chapter attempted to comprehensively review the
literature on bivalve energetics. A full listing would occupy virtually all the
space available and additional bibliographies are provided in recent pub
lications by Bayne (1976a) and Bayne and Newell (1983). Instead we have
attempted to illustrate processes with selected examples. The text is sub
divided according to the parameters of the standard energy budget equation
(see page 199 of Volume I). The first section thus considers methods and
rates of food consumption (C), following which we discuss the energetic
losses resulting from egestion (F), respiration (R), and excretion (U). The
product of these measurements gives an index of metabolic energy balance
[C - (F + R + U)] or scope for growth. Direct measurements may also be
made of growth rate (Pg) and reproductive output (Pr) and these are consid
ered separately. A final section examines population energy budgets.
1. Bivalvia 3
II. FEEDING
A. Modes of Feeding
A variety of feeding techniques are found within the bivalves, although
the vast majority utilize cilia to gather fine particulate material from the
water column (suspension feeding) or from the substratum (deposit feeding)
(Owen, 1974).
In the primitive Protobrachia, elongate palp proboscides are extruded
from the shell and moved over the bottom sediment. Ciliary currents gener
ated in the grooved ventral surface of each proboscis transport particles to
the palps for sorting and ingestion. Suspended material inhaled through the
siphons with the respiratory water current may also impinge directly on the
palps, or adhere to the gills and be transferred to the palps, but the small size
of the gills relative to the palps suggests that the former play a minor role as
feeding organs.
In lamellibranch bivalves the greatly enlarged gills perform the entire
food-gathering function (j0rgensen, 1966; Dral, 1967). The gills divide the
mantle cavity into two chambers and cilia arranged along the filaments
propel water and suspended particles in through an inhalent aperture, sieve
out the particles, and expel the water through an exhalent aperture. In
epifaunal species the inhalent aperture often occupies most of the mantle
margin, while in burrowing forms the mantle edge may be extended into
elongate siphons that protrude into the overlying water. The exhalent aper
ture or siphon is usually relatively narrow and directs filtered water away
from the inhalent one to prevent recirculation, and the siphon or mantle
apertures frequently possess tentacles that exclude large particles from the
mantle cavity.
While suspension- or deposit-feeding techniques are typical of most
bivalves, a few groups have developed supplementary or alternate mecha
nisms. Septibranchia, for example, have adopted a variety of carnivorous
habits. Representatives of the family Cuspidariidae have raptorial inhalent
siphons that detect vibrations produced by small invertebrate prey (Reid and
Reid, 1974). In Poromya granulata the inhalent siphon can be enormously
enlarged and everted and has a distal overarching cowl that is thought to
clamp over living prey (Morton, 1981).
The giant clam Tridacna retains its filter-feeding capacity but also main
tains autotrophic algal symbionts within its body and utilizes these as a
secondary source of nutrition (Falkboner, 1971).
Shipworms retain their filter-feeding capacity but have also developed the
ability to digest wood. Genera such as Teredo and Bankia have elongate
cylindrical bodies that fill a tubelike burrow cut into the wood by the shell,
4 C. L. Griffiths and R. J. Griffiths
which is a modified rasping tool. It is currently thought that cellulose diges
tion is initiated by gram-negative bacteria housed in the organ of Deshayes,
which opens into the esophagus and is analogous to a salivary gland. Fur
ther breakdown is accomplished by phagocytic cells in large digestive diver-
ticula that have developed independently of those used for the digestion of
filtered food (Morton, 1978). A few bivalves are also parasitic, for example,
Entovalva, an endoparasite of Holothuria. Little is known of feeding in such
species, although their simple guts indicate that they may absorb pre-
digested food through the body wall.
Since research has been concentrated on economically important suspen
sion- and deposit-feeding species, the following account is confined largely
to these groups.
B. Measuring Feeding Rate
Rates of filter-feeding are usually determined by measuring the rate of
removal of particles from suspension (clearance rate), although the volume
of water passing through the mantle cavity (ventilation or pumping rate) can
also be used. The two readings have the same numerical value if all particles
entering the mantle cavity are retained. This is normally the case if the
particles are sufficiently large, but if retention efficiency is below 100%,
ventilation rate will exceed clearance rate and the latter will provide a better
estimate of the amount of material removed from suspension. This will
equate with ingestion ration only if no pseudofeces is being produced by the
animal.
Numerous methods have been devised to measure filtration rates in
bivalves and are reviewed by Ali (1970), Bayne (1976a), Winter (1978), and
others. Ventilation rate is normally estimated by physically separating inha-
lent and exhalent apertures and monitoring the flow of water from the latter
(see, e.g., Davids, 1964; Drinnan, 1964). Great care needs to be taken with
this method to balance water levels so that neither is water siphoned through
the mantle cavity nor is the animal forced to pump against a back pressure.
The tubes or baffles used to isolate the exhalent aperture also tend to restrict
pumping activity. Alternative methods that overcome these objections in
clude the introduction of dyes or other particles into the exhalent current to
make the flow visible (see, e.g., Coughlan and Ansell, 1964). Although
measurements of ventilation rate can be used to monitor short-term fluctua
tions in pumping activity and may be made in particle-free water, feeding is
probably better estimated from clearance rate. In its simplest form clearance
rate can be obtained by confining animals in a fixed volume of water con
taining suitably sized particles and monitoring the exponential decline in
