Table Of ContentAnimal Energetics
VOLUME 1
Protozoa through Insecta
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 591.19*121 87-1170
ISBN 0-12-544791-4 (v. 1: aik. 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.
P. Calow (121), Department of Zoology, The University of Sheffield,
Sheffield S10 2TN, Scotland
Leon M. Cammen (217), Bigelow Laboratory for Ocean Sciences, West
Boothbay Harbor, Maine 04575
Madhab C. Dash (261), School of Life Science, Sambalpur University, Jyoti
Vihar, Sambalpur, Orissa 768 019, India
Thomas M. Frost (27), Center of Limnology, University of Wisconsin,
Madison, Wisconsin 53706
Johanna Laybourn-Parry (1), Department of Biological Sciences, University
of Lancaster, Lancaster, England
J. Muthukrishnan (373), Department of Zoology, A.P.A. College, Palni 624
602, India
T. J. Pandian (373), Department of Animal Sciences, School of Biological
Sciences, Madurai Kamaraj University, Madurai 625 021, Tamilnadu,
India
Fritz Schiemer (185), Institut fur Zoologie, Universitat Wien, A-1090 Wien,
Austria
Kenneth P. Sebens (55), Marine Science and Maritime Studies Center,
Northeastern University, East Point, Nahant, Massachusetts 01908
Peter L. Starkweather (159), Department of Biological Sciences, University
of Nevada, Las Vegas, Nevada 89154
F. John Vernberg (301), Belle W. Baruch Institute for Marine Biology and
Coastal Research, University of South Carolina, Columbia, South Car
olina 29208
ix
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. John Vernberg
1
Protozoa
JOHANNA LAYBOURN-PARRY
I. Introduction
II. Ingestion
A. Modes of Feeding and Food Selection
B. Factors Influencing Energy Intake
C. Trophic Relations
III. Egestion and Excretion
IV. Growth
A. Mean Cell Volume Variation
B. Factors Influencing Growth and Division
C. Encystment
V. Respiration
A. Aerobic Respiration
B. Anaerobic Respiration
VI. Budgets and Efficiencies
VII. Conclusion
References
I. INTRODUCTION
Within the free-living Protozoa a wide spectrum of trophic types is found.
Although the majority are bacterivores exploiting the decomposer bacteria
as an energy source, some are herbivores feeding on unicellular or filamen
tous algae and others are predators of elements of the micro- and meio-
fauna, including Protozoa. Much of the energetic functioning of Protozoa is
involved in the complex decomposer food web, which is responsible for the
recycling of essential nutrients in nature. The obvious ecological role of the
bacterivore Protozoa is the transfer of bacterial production through their
own tissues as potential energy to successive trophic levels. However, it is
1
ANIMAL ENERGETICS, VOL. 1
Copyright © 1987 by Academic Press, Inc.
All rights of reproduction in any form reserved.
2 Johanna Laybourn-Parry
now becoming increasingly clear from studies on nutrient recycling and
bacterial growth dynamics, particularly in the soil, that the contribution
made by Protozoa may be greater and more complex than we had pre
viously assumed. There is growing evidence that Protozoa stimulate bacte
rial growth and hence the rate of decomposition and recycling of nutrients.
Energetics studies on Protozoa are fairly recent and few compared to the
information on the ecological energetics of other invertebrates. The first
energy budget produced for a protozoan was for Acanthamoeba sp. (Heal,
1967). This energy budget, valuable though it was in paving the way for
subsequent energetics studies, had some limitations in that it applied to one
temperature only and suffered from a lack of calorimetry data. Later investi
gations integrated temperature, food concentration, and sometimes field-
determined parameters of the energy budget in an attempt to relate pro
tozoan energetics to natural environmental conditions and food resources.
There is still a relative paucity of information on Protozoa and there are
several reasons why this is so. Until fairly recently the micro- and meiofauna
in ecosystems were mentioned only in passing, if at all, and were dismissed
as probably contributing little to the overall functioning and energy flow in
aquatic and terrestrial communities. Thus there was little impetus to devote
time to their study. Those who embarked on investigations of protozoan
energetics had to contend with an array of technical difficulties imposed by
the small size of these organisms and the complex, highly diverse commu
nities in which they live.
The pattern of production in Protozoa differs fundamentally from most
Metazoa. In most animals production appears as growth in body mass dur
ing the immature developmental stages and as reproductive products (eggs,
embryos) in the adult stage, whereas in the Protozoa reproducing by binary
or multiple fission the cell or body is the reproductive product passed on as
two, or numerous, cells to the succeeding generation. Under normal cir
cumstances, therefore, growth and reproduction are essentially one and the
same as far as production is concerned. It should be noted that a few groups
with complex life cycles, such as the foraminiferans, do not conform to this
pattern. Metazoans die after reproducing once or repeatedly during their life
cycles and the corpse is lost from the biomass of a species population.
Although in the Protozoa asexual reproduction strictly speaking results in
the death of an animal as an individual entity, the biomass is not lost to the
population but is bequeathed to the next generation. In theory the biomass
of a population could increase indefinitely, but physical, chemical, and
biological factors mediate against this possibility.
The life cycles of protozoans are short compared to those of other ani
mals. Under ideal conditions a generation may span a few hours in the
smallest species up to days in the largest species. Generation times, or the
3
1. Protozoa
period between divisions, vary as a function of prevalent environmental
conditions, the most important of which are temperature and food availabil
ity. In addition, the mean cell volume of a population may vary in response
to the same factors. Variability in generation time and mean cell volume
present a complication that must be taken into account in energetic investi
gations.
Although we can broadly categorize Protozoa into trophic groups, the
exact nutritional requirements of the majority of species are poorly re
searched. We do not know to any real extent what feeding preferences are
in the wild, or how the elements of competition for food on an intra- and
interspecific basis affect energy consumption or other aspects of the phys
iology. As Lee (1980) points out, our understanding of energy transforma
tions involving Protozoa requires that two fundamental components related
to food quality be elucidated, first, information on the molecular constitu
tion of the prey and, second, the ability of Protozoa to recognize and utilize
it. Although we are able to demonstrate how food quality and quantity affect
growth and reproduction in some species, we can only place this informa
tion into the context of the natural community to a limited extent.
II. INGESTION
A. Modes of Feeding and Food Selection
The modes of feeding displayed by the various groups of Protozoa are
very diverse and differ in relation to the presence or absence of a cytostome,
the type of feeding and locomotor organelles present, and the trophic status
of the organism. The majority of ciliates feeding on bacteria are filter
feeders, producing feeding currents with cilia and ciliary structures to cap
ture and direct material onto the cell mouth or cytostome. The more primi
tive species, the gymnostomes, are essentially raptorial macrophages taking
in algae and other organisms that make contact with the mouth (Fenchel,
1968a). Some very specialized carnivores, notably the sedentary suctorians,
have developed tentacles, each of which is essentially a mouth designed to
capture and extract the cell contents of other ciliates. Many flagellates create
feeding currents with the flagellum and direct food items onto the cytostome
or, where this structure is absent, onto particular areas of the cell for inges
tion. In collared flagellates, for example, particles are driven against the
collar, which periodically contracts or rolls up to bring the food into contact
with the cell surface, where food vacuoles are formed at the collar base
(Fjerdingstad, 1961).
Sarcodine Protozoa capture bacteria, micro-, and meiofauna by means of
4 Johanna Laybourn-Parry
various types of pseudopodia. There is a diverse array of pseudopodial
structures within the group. Most sarcodines are macrophages that consume
particles with which they make contact. In some species the pseudopodia
flow around and engulf particles, or particles enter a pseudopod on contact,
while in others, such as the radiolarians, the rhizopodia transport captured
food down toward the main body of the cell for ingestion.
There is evidence that some protozoans may practice osmotrophic nutri
tion. Enzymes have been isolated from axenic cultures of amoebae and
ciliates, indicating the possibility of extracellular digestion (Pandian, 1975).
The filter-feeding mechanism and capabilities of a range of bacterivore cili
ates have recently been investigated by Fenchel (1980a,b,c,d). Bacterivore
ciliates appear to discriminate what they ingest on the basis of particle size
and shape only and this is related to the mouth morphology (Fenchel,
1980a). In other words, they apparently ingest all particles in the size range
within the retention capacity of the oral ciliary organelles, irrespective of the
energy value of the particles. Thus there is no selection practiced in feeding
other than on purely mechanical grounds. This differs from some filter-
feeding metazoans, in which particle density and type may determine the
filtering rate and ingestion (Lehman, 1976). Each ciliate species has its own
size range of particle, there being a correlation between minimum particle
size retained and the free surface between adjoining cilia of the ciliary filter
(Fenchel, 1980b,c,d). Most holotrichs feeding on bacteria are able to retain
particles down to 0.2 |xm in diameter, retaining particles between 0.3 and
1.0 p-m most efficiently, while spirotrichs do not retain particles smaller than
1-2 |xm. It appears that the filtering rate is constant irrespective of particle
concentration. The uptake of particles is a linear function of particle density
increasing, experimentally, as a linear function of time. The maximum up
take rate is determined by the rate at which particles can be phagocytosed.
As particle density increases, the filtering apparatus becomes clogged by
particles, because the rate at which ingestion can be achieved is limited, so
that some of the collected food will be lost from the ciliary filter (Fenchel,
1980a,c). The feeding capability of ciliates is one of the factors determining
their ecological distribution. Those adapted to feeding on bacterial-sized
particles have a low capacity for water processing and are restricted to
bacterial-rich environments, while those populating open waters with low
bacterial densities possess porous filters optimized to retain phytoplankton-
sized particles (j0rgensen, 1983).
These simple animals do not appear to maximize energy return from their
filter-feeding activities. It could be argued that any organism that apparently
filters at a constant rate irrespective of the density of particles in the medium
is not operating efficiently. To be efficient an organism should modulate the
filtering rate so that in any given food density the quantity of material passing
1. Protozoa 5
over the filtering apparatus and into the mouth is the maximum that can be
adequately coped with. A protozoan filtering at a constant rate will in high
food densities receive too much material to phagocytose and blocking of the
filter will occur. Temperature, however, will impose an effect on the rate of
filtering since ciliary activity varies in response to temperature (Sleigh, 1956;
Jahn and Bovee, 1967). The lack of selectivity in the particles ingested is
also seemingly inefficient. Although most of the particles retained are likely
to be bacteria, it has been demonstrated that bacterial species vary in their
value for supporting protozoan growth and reproduction, and some are
toxic to Protozoa (Curds and Vandyke, 1966).
In general Protozoa have high growth rates and rapid reproduction and
there is probably no real advantage to unicellular organisms normally inhab
iting food-rich environments in evolving or pursuing a strategy designed to
maximize energy return from feeding. Such strategies may have evolved in
the ecological interactions of higher organisms in response to longer life
cycles and greater physiological complexity imposing pressure to "con
serve" energy.
Food selection does occur in the large omnivorous ciliate species Stentor
(Schaeffer, 1910). The selection is achieved by changes in the ciliary beat of
the cilia of the pouch and funnel of the oral region. Of any group of particles
reaching the pouch, some will be carried to the mouth and ingested and
others are rejected by localized reversal of the ciliary beat. Stentor can
discriminate among different food organisms and between animate and in
animate material. The degree of selectivity is more refined when the animal
is almost satiated than when starved (Schaeffer, 1910). Other investigations
have shown a preference for ciliate prey over algal or flagellate prey (Rap
port et ai, 1972). Chemoreception has been shown to be the main mecha
nism responsible for prey recognition by carnivorous ciliates, amoebae, and
flagellates (Seravin and Orlovskaja, 1977).
The suctorian ciliates prey almost entirely on holotrichous and spirotri-
chous ciliates. The ciliated "young" of the suctorians are never captured nor
are hypotrich ciliates, flagellates, or amoebae. Food selection appears to be
chemically mediated, there being a chemical reaction between compounds
on the prey surface and the tentacle tip. Hull (1954, 1961a) has demon
strated that acetylcholine is essential to successful prey adhesion. The pres
2+ 2 +
ence of SH groups appears to be necessary and the adherence of prey will
not take place in the absence of Ca and Mg . Protozoa that are not
taken as prey presumably lack the appropriate chemical makeup on their
surface, so that when they make contact with a tentacle capture and adhe
sion do not occur.
After capturing a ciliate the suctorian then proceeds to extract the cell
contents of the prey, which are transported by the tentacles into the preda-
