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PRIMARY PRODUCTIVITY IN
AQUATIC ENVIRONMENTS
Primary Productivity in
Aquatic Environments

Proceedings of an I.B.P. PF Symposium

Pallanza, Italy, April 26-May 1,1965
Edited by C. R. Goldman

UNIVERSITY OF CALIFORNIA PRESS

Berkeley and Los Angeles 1966
 University of California Press
Berkeley and Los Angeles, California

Cambridge University Press

London, England

Library of Congress Catalog Card Number : 66-23180

Printed in thè United States of America

 FOREWORD

Welcome to Pallanza and to the Istituto Italiano di Idrobiologia.

I do not want to take the valuable time of this audience to
recall the scope and the philosophy of the International Biological
Programme. I am quite sure that all of you know that its principal
purpose is the basic study of productivity and that we are all
therefore perfectly on the crest of this wave.
It would perhaps be interesting to inform you that this Sym-
posium is the first one to be held in the I.B.P., and it is of some
significance that is concerned with primary productivity in water,
«mater vitae ». I sincerely believe that your experience and bril-
liant talents will produce a first class first I.B.P. symposium on
the first link of the aquatic food-chain, which will stimulate the future
I.B.P. symposia dealing with successive steps.
As you know, a triad, Dr. C. R. Goldman, Dr. R. A. Yollenweider
and myself, is responsible for the organization of this meeting, but
I must acknowledge that the first two took on their shoulders most
of the work for the realization of the scientific scheme. The privilege
of having more white hair is the only reason I am speaking to
you first.
We organizers are convinced that this convention of marine
and fresh water specialists will not produce a meromictic state
of affairs, because the eddy diffusion of ideas and the desirable
turbulence of discussion will produce a mixed water, flavoured
« cum sale sapientiae ».
The first three days will be spent in listening to and discussing
individual contributions, which, as you have agreed, should be
printed as proceedings in a Supplement volume of the « Memorie »
of this Institute. The sessions will be directed by chairmen, who
will carefully control the time allotted for each paper.
The last three days, as it has already been announced, will be
devoted to discussions, through which decisions will be reached
8 Foreword

for the preparation of a methodological manual on primary pro-

ductivity in water. This will greatly help the future work of many
scientists in the choice of the most suitable methods of measure-
ment, offering them, whenever possible, intercalibration procedures.
Working groups have been selected for this second half of the
week. Outlines of what form the manual may take have already been
distributed. This second part of our work requires our deepest
attention, because of the large distribution which the Central
Office of I.B.P. intends to give to these methodological manuals,
and because the financial support we have received for the organ-
ization of this Symposium, namely from I.B.P. itself and from
the Italian National Research Council, was intended primarily for
this purpose.
And now, « buon lavoro »!
Vittorio Tonolli

Verbania Pallanza, 26 April 1965

 PREFACE

The International Biological Programme has aptly chosen « The

Biological Basis of Productivity and Human Welfare » as the inte-
grating theme for aquatic and terrestrial environments. The section
of this program on productivity of freshwater logically selected
primary productivity as the subject for the first symposium, leaving
higher levels of the food pyramid for subsequent symposia.
In the last decade there have been many meetings on problems
of primary productivity in aquatic food chains {e.g., East Lansing
1955; Bergen 1957; Honolulu 1961; Princeton 1961, 1962; Edinburgh
1964). The great research effort that has been and will continue to
be expended on investigations of primary productivity in both
marine and freshwaters is good reason for repeated re-evaluation of
both methods and principles. The symposium here reported consti-
tutes a conscious effort to extend rather than duplicate its prede-
cessors at a time when both theory and methods of measurement
deserve particular re-evaluation.
To prevent a « meromixis of ideas » as Professor Tonolli so aptly
describes it, the organizers assembled an international group with
both marine and freshwater experience in the general areas of
Limnology, Oceanography, Plant Physiology, and Biochemistry. The
charge to these specialists from twelve countries was to review the
achievements in primary productivity research, as well as to discuss
and formulate ideas for further exploration of the most promising
areas of research.
A subject as broad as primary productivity in aquatic environ-
ments does not lend itself to rigid organization in this volume. The
general categories under which the papers are listed have been
selected with full recognition of their not inconsiderable inter-
relationship ; they are intended only as a general guide to the reader.
Although the often exciting and sometimes heated discussions that
followed each paper have not been reported per se, they have in a
10 Preface

real sense been incorporated, in many cases, as useful modification

of the papers presented here.
A particular effort has been made for rapid publication of this
symposium which regrettably may result in some errors. I am
particularly indebted to Professor Vittorio Tonolli, Convener of
the Productivity of Freshwater section of the IBP, for arranging for
expeditious publication and for maintaining the flow of manuscripts
among the editor, contributors, and printer. I should also like to
particularly acknowledge the conscientious and imaginative assist-
ance of Mrs. Kathleen C. Green in the task of editing. The editor
was a John Simon Guggenheim Fellow during the preparation of
these proceedings.

Charles R. Goldman
Davis, California
November 1965

CITATION OF PAPERS PROM

THIS VOLUME
For consistency and to prevent confusion, workers
citing papers from this volume are urged to adopt
the following form:
Author. 1965. Title of paper, p. 000-000. In C. R.
Goldman [ed.], Primary Productivity in Aquatic
Environments. Mem. 1st. Ital. Idrobiol., 18 Suppl.,
University of California Press, Berkeley.
 LIST OF PARTICIPANTS

Laboratory of Radiation Ecology, Building 772-6

ROBERT J . B E Y E R S .
SRP, Aiken, South Carolina (U.S.A.)
E . K . DUURSMA. I.A.E.A. - Musée Océanographique, Monaco (Monaco
Principauté)
HANS-JOACHIM ELSTER. Limnologisches Institut der Universität Frei-
burg, Falkau (Schwarzwald) (Germany)
INGO FINDENEGG. Biologische Station Lunz, Lunz-am-See (Nieder-
österreich, Austria)
G . E . FOGG.Westfield College, Botany Department, Hampstead, Lon-
don N.W.3 (Great Britain)
Laboratorio di Fisiologia Vegetale, Istituto di Scienze
GIORGIO F O R T I .
Botaniche dell'Università, Milano (Italy)
MARCO GEHLETTI. Istituto Italiano di Idrobiologia, Pallanza (No-
vara) (Itaìly)
CHARLES R . GOLDMAN. Department of Zoology, University of Cali-
fornia, Davis, California (U.S.A.)
HANS E. GOLTERMAN. Hydrobiological Institute, Nieuwersluis (Ne-
therland)
J O H N E . HOBBIE. Department of Zoology, North Carolina State Uni-
versity, Raleigh, N.C. (U.S.A.)
RAMON MARGALEP. Instituto de Investigaciones Pesqueras, Paseo
Nacional, Barcelona 3 (Spain)
W. O H L E . Hydrobiologische Anstalt der Max-Planck-Gesellschaft,
232 Plön, Holstein (Germany)
M. O W E N S . Water Pollution Research Laboratory, Elder Way, Ste-
venage, Herts (Great Britain)
T . V . R . PILLAY. F.A.O. Biology Branch, Roma (Italy)
D O M E N I C O POVOLEDO. Istituto Italiano di Idrobiologia, Pallanza (No-
vara) (Italy)
12 List 0/ participants

WILHELM RODHE. Limnologiska Institutionen, Uppsala Universitet,

Uppsala (SwedenJ
C. S. SOEDER. Limnologisches Institut der Universität Freiburg,
Falkau (Schwarzwald) (Germany)
Iu. I. S O R O K I N . Institute of Freshwater Biology, USSR Academy of
Sciences, Borok, Jaroslav, Nekouz (U.R.S.S.)
JOHN H. STEELE. Marine Laboratory, P.O. Box 101, Victoria Road,
Aberdeen, Scotland (Great Britain)
E. STEEMANN NIELSEN. Royal Danish School of Pharmacy, Copen-
hagen (Denmark)
MIROSLAV S T E P A N E K . Rosy Luxetnburkove 20, Praha-Smichov (Czecho-
slovakia)
J. F. TALLING. Freshwater Biological Association, The F&rry House,
Ambleside, Westmorland (Great Britain)
VITTORIO TONOLLI. Istituto Italiano di Idrobiologia, Pallanza (No-
vara) (Italy)
JOHN R. VALLENTYNE. Department of Zoology, Cornell University,
Ithaca, New York (U.S.A.)
RICHARD A. VOLLENWEIDER. Istituto Italiano di Idrobiologia, Pal-
lanza (Novara) (Italy)
D. F. WESTLAKE. Freshwater BiologicaU Association, The River La-
boratory, East Stoke, Wareham (Dorset, Great Britain)
ROBERT G . W E T Z E L . Department of Botany and Plant Pathology,
Kellogg Gull Lake Biological Station, Michigan State University,
Hickory Comers, Michigan (U.S.A.)
CHARLES S . YENTSCH. Woods Hole Oceanographic Institution, Woods
Hole, Massachusetts (U.S.A.)
 TABLE OF CONTENTS

Foreword 7
Preface 9
List of participants 11

I. - The photosynthesis and adaptation of algae

G. FORTI - Light Energy Utilization in Photosynthesis 17
E . G . JORGENSEN and E . S T E E M A N N - N I E L S E N - Adaptation in Plankton Algae 37
C. J. SOEDER - Some Aspects of Phytoplankton Growth and Activity . . . 47
R. J. B E Y E R S - The Pattern of Photosynthesis and Respiration in Laboratory
Microecosystems 61

II. - Factors limiting the productivity of natural phytoplankton popula-

tions
H. J. E L S T E R - Absolute and Relative Assimilation Rates in Relation to
Phytoplankton Populations 77
I . FINDENEGG - Factors Controlling Primary Productivity, Especially with
Regard to Water Replenishment, Stratification, and Mixing 105
C . R. GOLDMAN - Micronutrient Limiting Factors and their Detection in Natural
Phytoplankton Populations 121
R . G. W E T Z E L - Nutritional Aspects of Algal Productivity in Marl Lakes with
Particular Reference to Enrichment Bioassays and their Interpretation . 137

III. - Production and utilization of organic 'solutes by bacteria and

phytoplankton
E. K. DUURSMA - (Abstract) Dissolved Organic Matter in Surface Water as a
Parameter for Primary Production 161
G . E. FOGG and W . D . W A T T - The Kinetics of Release of Extracellular Pro-
ducts of Photosynthesis by Phytoplankton 165
J . E. H O B B I E and R . T . W R I G H T - Competition between Planktonic Bacteria
and Algae for Organic Solutes 175
Jtr. I . SOROKIN - On the Trophic Role of Chemosynthesis and Bacterial Bio-
synthesis in Water Bodies 187

IV. - Productivity of higher aquatic plants and periphyton

M. OWENS - Some Factors involved in the Use of Dissolved-Oxygen Distribu-
tions in Streams to Determine Productivity 209
J. H. S T E E L E - (Abstract) Sublittoral Benthic Production on a Sandy Beach . 225
14 Table of contents

D. F. W E S T L A K E - Some Basic Data for Investigations of the Productivity of

Aquatic Macrophytes 229
R. G . W E T Z E L - Techniques and Problems of Primary Productivity Measure-
ments in Higher Aquatic Plants and Periphyton 249

V. - Primary productivity and standing crop

I . FINDENEOG - Relationship between Standing Crop and Primary Product-
ivity 271
M. STEPANEK - Numerical Aspects of Nannoplankton Production in Reservoirs 2 9 1
J . R. VALLENTYNE - (Abstract) Net Primary Productivity and Photosynthetic
Efficiency in the Biosphere 309
D . F . W E S T L A K E - Theoretical Aspects of the Comparability of Productivity
Data 313
C. S . Y E N T S C H - The Relationship between Chlorophyll and Photosynthetic
Carbon Production with Reference to the Measurement of Decomposition
Products of Chloroplastic Pigments 323

VI. - Theoretical problems of primary productivity, light, and com-

munity structure
E. K. DUURSMA - Note on Diffusion Uptake in Cells: Some Mathematical
Formulae 349
R. MARGALEF - Ecological Correlations and the Relationship between Primary
Productivity and Community Structure 355
W . R O D H E - Standard Correlations between Pelagic Photosynthesis and Light 365
J. H. S T E E L E - Notes on Some Theoretical Problems in Production Ecology . 383
J . F. TALLING - Comparative Problems of Phytoplankton Production and Photo-
synthetic Productivity in a Tropical and a Temperate Lake 399
R. A . VOLLENWEIDER - Calculation Models of Photosynthesis-Depth Curves
and some Implications Regarding Day Rate Estimates in Primary Pro-
duction Measurements 425
 LIGHT ENERGY UTILIZATION
IN PHOTOSYNTHESIS

GIORGIO FOKTI
Laboratorio di Fisiologia Vegetale
Istituto di Scienze Botaniche dell'Università, Milano

For bibliographic citation of this paper, see page 10.

 Abstract

The current views and experimental approaches to the mechanism of

photosynthesis are discussed with regard to the biochemical processes involved
in the metabolic utilization of light energy. Light energy absorbed by the
molecules of photosynthetic pigments is utilized to generate ATP and TPNH,
which are then utilized for the reduction of C02 to the carbohydrate level.
Other metabolic utilizations of photosynthetically-generated ATP and TPNH
are also discussed, as are the possible regulatory mechanisms by which photo-
synthesis and other metabolic processes might influence each other.

Primary productivity of aquatic environments is basically de-

pendent on the photosynthetic activity of the autotrophic organisms,
namely the photosynthetic organisms capable of transforming CO2
into organic matter. For this reason, the estimation of the primary
productivity of natural waters is based upon the measure of their
photosynthetic activity, which is due primarily to algae, but possibly
also to photosynthetic bacteria.
Photosynthesis was discovered by Priestley as a process by which
green plants « purify » air. Soon after, Ingenhousz recognized that
the photosynthetic process is of fundamental physiological impor-
tance for plant nutrition, and that green plants can « feed on light».
In more recent times, it was recognized that light energy is utilized
in photosynthesis to move electrons against the thermochemical
gradient. The most general equation that can be written for photo-
synthesis of green plants
light
6 CO2 + 6 H 2 0 • C6H1206 + 6 C0 2 (1)
shows clearly that the overall process is a redox reaction: CO2 is
reduced, and water is oxidized. Van Niel (1941) first emphasized
this concept, and extended it to interpret also bacterial photosyn-
thesis, where no oxygen is evolved. Equation (1) can thus be written
more generally as
hv
2 AH2 + C0 2 • (HCOH) + 2 A + H 2 0 (2)
where AH2 stands for a reductant, which may be water, H2S, Na2S203,
or an organic carbon compound.
20 G. Forti

The fact that, experimentally, the same amount of light energy

is required per mole of C0 2 assimilated regardless of the nature and
redox potential of the reductant utilized, suggested to Van Niel the
idea that the primary reaction is the same in all organisms, and that
it consists of the splitting of a molecule of H 2 0 to yield a reducing
agent (H) and an oxidant (OH).

hv
H20 v (H) + (OH) (3)
(H) and (OH) here indicate in very general terms a reductant and
an oxidant).
Such a general presentation of photosynthesis as a light-driven
redox reaction involving H 2 0 proved to be extremely productive and
was the basis of the recent most successful experimental work.
According to Van Niel's hypothesis, the oxidant (OH) can be
employed in green plants to oxidize water with production of 0 2 ,
or, for instance in sulfur bacteria, to form sulfur:

green plants: 2 H 2 0 + 4 (OH) • 02 + 4 H20 (4)

purple bacteria: 2 H2S + 4 (OH) • 2 S + 4 H20 (5)
An interesting implication of these reactions is that the 0 2 evolved
in photosynthesis of green plants must be derived from water and
not from the C02. This was indeed experimentally demonstrated by
Ruben et al. (1941) in a classical experiment utilizing O" labelled
H 2 0. These experiments were questioned by Warburg (1958), who
pointed out that the exchange of the oxygen atoms of C0 2 with those
of water accounts for these observations.
More recently Brown (1953) confirmed Ruben and Kamen's re-
sults, under conditions where Warburg's objections cannot be re-
levant.

THE OVERALL REACTION OF PHOTOSYNTHESIS:

ENERGETIC ASPECTS

In the reaction
118,000 cal
C0 2 + H 2 0 • (HCOH) + 0 2 (6)
the free energy gain is of 118 K cal/mole. Quite obviously, this
energy has to be provided by light. In order to be effective in the
biochemical transformations involved in photosynthesis, light has to
be absorbed by the molecules of pigments, raising the energetic level
of these molecules well above the ground state. A pigment molecule
in an excited state is then responsible for the reduction of a redox
 Light Energy Utilization in Photosynthesis 21

substance, X, which must be present in the oxidized state in .order to

be able to accept it. As a result, the pigment will be left with a
positive charge, and the oxidant generated in this way is responsible
for the oxidation of an intermediate, and ultimately of AH2. The
reductant generated in the light reaction, XH, will be used eventually
for the reduction of C0 2 . This sequence of events can be represented
as follows:
hv

C0 2
V
XH ^ C h l « - « - « - + - Y H 2 0 (7)
Co2

where the arrows point out the direction of electron flow. Each arrow
indicates one step; however, it should be clearly understood that the
number of steps is far from being ascertained at our days. The
scheme, as presented, indicates only that one (or more than one, as
we shall see later) light reaction provides the reagents for a series
of « dark » enzymatic reactions. It follows from this that the dark
reactions should be limiting the rate at low light intensities. This
is indeed the case: the rate versus light-intensity curve, shortly called
the intensity curve, starts with a constant slope, and then bends and
becomes parallel to the abscissa. At high light intensities, the
maximal rate attainable is called the «light saturation » rate. The
saturation rate can be lowered by lowering the concentration of
C0 2 or the temperature. These treatments do not change the slopes
of the light intensity curves at low light intensity. These observ-
ations are taken as a demonstration that photosynthesis involves
temperature-dependent dark reactions and temperature-independent
light reactions (photochemical reactions). As stated above, C0 2 can
be made a limiting factor for photosynthesis, and this can certainly
occur under natural conditions. Photosynthesis of green plants is
probably seldom limited by the concentration of H 2 0 and certainly
not in aquatic organisms. However, it might be pertinent to point
out that the hydrogen donor concentration might well be a limiting
factor, for instance, in purple bacteria photosynthesis utilizing H 2 S
(or other reducing substances from the environment) for the re-
duction of C0 2 . This fact should be taken into account in all in-
stances where bacterial photosynthesis contributes appreciably to the
productivity of an aquatic environment.
The evidence for the occurrence of light and dark reactions in
photosynthesis was obtained also with a different approach. Emerson
and Arnold (1932) measured photosynthesis (as oxygen evolution)
of green algae with very short flashes of saturating light, separated
by short dark periods. Using flashes of 10"5 seconds (of saturating
intensity) they observed that the amount of oxygen produced per
flash (flash yield) increased with the length of the dark period sep-
22 G. Forti

arating two successive flashes up to dark periods of a few hundreths

of a seeond. For longer dark periods, there was no further increase
in rate even if more intense flashes were used. It was also found that
the maximum yield was of one 0 2 molecule per 2000 - 2500 chloro-
phyll molecules. The presence of inhibitors of the dark reactions,
such as or phenylurethanes, did not change the maximum flash
yield, but caused the dark periods needed to be of longer duration.
These experiments led to the hypothesis, proposed by Gaffron and
Wohl (1936), of the « photosynthetic unit ». The history of the photo-
synthetic unit concept is beyond the scope of this work, and we refer
to Rabinowitch (1956) for a more complete discussion. Only the most
fundamental observations and theoretical discussions will be briefly
summarized here, freely borrowing from Duysens (1952, 1964). The
model proposed by Duysens for the photosynthetic unit implies that
light energy absorbed by a large number of pigment molecules is
transferred by the physical mechanisms of induced resonance to
pigment molecules, called the reaction centers, present in a small
concentration as compared to the bulk of photosynthetic pigments.
In algae, each reaction center receives energy from about 200 chloro-
phyll molecules. The assembly of these molecules with the reaction
center is the «photosynthetic unit». The molecule at the reaction
center initiates the chemical reactions (consisting of redox re-
actions) of photosynthesis. The transfer of the energy of a quantum
by induced resonance from the pigment molecules of the unit to the
reaction center occurs within 1(T8 second after the absorption of the
quantum. Upon excitation, the reaction center molecule reacts photo-
chemically with a molecule, X, bound to it, and this reaction produces
a reductant, XH; the « oxydized » reaction center molecule is rapidly
restored into the initial state by another molecule, YH, which donates
an electron to it. The time required for this dark reaction (the re-
generation of the reaction center in its initial state) is at least 10"5
second. A quantum absorbed by the unit cannot be utilized unless
the reaction center molecule is ready to accept it, i.e. in its initial
state. Tamiya and Chiba (1949) and Tamiva (1949) used flashes of
the duration of 10~2 seconds, and under these conditions found a
maximum flash yield higher than Emerson's (on a chlorophyll basis),
but requiring much longer dark intervals to be attained. The dark
period needed between the flashes was longer at lower temperatures.
During the flash of 10 milliseconds the dark reaction evidently could
restore the reaction center several times while a longer dark interval
was needed for the subsequent enzymatic reactions to utilize the
larger amounts of XH and of Y generated.
The results of Emerson and of Tamiya suggested that the primary
dark reaction which regenerates the reaction center takes place in
a time of 10 -3 second or shorter, but longer that 10"5 second. We shall
see later that the concept of a « photosynthetic unit» has received
a larger body of evidence by the recent studies on the sequence of the
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