Biology of Oysters, Volume 41 1st

Edition Bayne
Visit to download the full and correct content document:
https://ebookmass.com/product/biology-of-oysters-volume-41-1st-edition-bayne/
More products digital (pdf, epub, mobi) instant
download maybe you interests ...

Principles of Cancer Biology 1st Edition

https://ebookmass.com/product/principles-of-cancer-biology-1st-
edition/

Principles of Bone Biology (2 Volume Set) 4th Edition

Edition John P. Bilezikian

https://ebookmass.com/product/principles-of-bone-
biology-2-volume-set-4th-edition-edition-john-p-bilezikian/

The Blitz 1940–41: The Luftwaffe's Biggest Strategic

Bombing Campaign 1st Edition Julian Hale

https://ebookmass.com/product/the-blitz-1940-41-the-luftwaffes-
biggest-strategic-bombing-campaign-1st-edition-julian-hale/

The Biology of Parasites 1st Edition – Ebook PDF

Version

https://ebookmass.com/product/the-biology-of-parasites-1st-
edition-ebook-pdf-version/
Biology of Domestic Animals 1st Edition Colin G. Scanes

https://ebookmass.com/product/biology-of-domestic-animals-1st-
edition-colin-g-scanes/

Cell biology : translational impact in cancer biology

and bioinformatics 1st Edition Mitchell

https://ebookmass.com/product/cell-biology-translational-impact-
in-cancer-biology-and-bioinformatics-1st-edition-mitchell/

Biology of Cardiovascular and Metabolic Diseases 1st

Edition Chaya Gopalan

https://ebookmass.com/product/biology-of-cardiovascular-and-
metabolic-diseases-1st-edition-chaya-gopalan/

Zika Virus Biology, Transmission, and Pathways Volume

1: The Neuroscience of Zika Colin R. Martin

https://ebookmass.com/product/zika-virus-biology-transmission-
and-pathways-volume-1-the-neuroscience-of-zika-colin-r-martin/

The Palgrave Handbook of Biology and Society 1st

Edition Maurizio Meloni

https://ebookmass.com/product/the-palgrave-handbook-of-biology-
and-society-1st-edition-maurizio-meloni/
Developments in Aquaculture
and Fisheries Science
Volume 41
Biology of Oysters
DEVELOPMENTS IN AQUACULTURE AND
FISHERIES SCIENCE

The following volumes are still available:

22. FRONTIERS OF SHRIMP RESEARCH
Edited by P. F. DeLoach, W. J. Dougherty and M. A. Davidson 1991 xv+412 pages
24. MODERN METHODS OF AQUACULTURE IN JAPAN
Edited by H. Ikenoue and T. Kafuku 1992 xvi+274 pages
26. PROTOZOAN PARASITES OF FISHES
Edited by J. Lom and I. Dykova´ 1992 xii+316 pages
28. FRESHWATER FISH CULTURE IN CHINA: PRINCIPLES AND PRACTICE
Edited by J. Mathias and S. Li 1994 xvi+446 pages
29. PRINCIPLES OF SALMONID CULTURE
Edited by W. Pennell and B. A. Barton 1996 xxx+1040 pages
30. STRIPED BASS AND OTHER MORONE CULTURE
Edited by R. M. Harrell 1997 xx+366 pages
31. BIOLOGY OF THE HARD CLAM
Edited by J. N. Kraeuter and M. Castagna 2001 xix+751 pages
32. EDIBLE SEA URCHINS: BIOLOGY AND ECOLOGY
Edited by J. M. Lawrence 2001 xv+419 pages
33. GLOBAL SEAGRASS RESEARCH METHODS
Edited by F. T. Short and R. G. Coles 2001 viii+482 pages
34. BIOLOGY AND CULTURE OF CHANNEL CATFISH
Edited by C. S. Tucker and J. A. Hargreaves 2004 x+676 pages
36. THE KNOWLEDGE BASE FOR FISHERIES MANAGEMENT
Edited by L. Motos and D. Wilson 2006 xxi+476 pages
38. SEA URCHINS
Edited by J. M. Lawrence 2013 xviii+532 pages
39. THE SEA CUCUMBER APOSTICHOPUS JAPONICUS
Edited by H. Yang, J. F. Hamel, and A. Mercier 2015 xxiv+454 pages
40. SCALLOPS: BIOLOGY, ECOLOGY, AQUACULTURE, AND FISHERIES, THIRD EDITION
Edited by S. E. Shumway and G. J. Parsons 2016 xviii+1196 pages
Developments in Aquaculture
and Fisheries Science
Volume 41
Biology of Oysters

Brian Bayne
Academic Press is an imprint of Elsevier
125 London Wall, London EC2Y 5AS, United Kingdom
525 B Street, Suite 1800, San Diego, CA 92101-4495, United States
50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States
The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom

© 2017 Elsevier 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
photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on
how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as
the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions.

This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted
herein).

Notices
Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in
research methods, professional practices, or medical treatment may become necessary.

Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods,
compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the
safety of others, including parties for whom they have a professional responsibility.

To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or
damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods,
products, instructions, or ideas contained in the material herein.

Library of Congress Cataloging-in-Publication Data

A catalog record for this book is available from the Library of Congress

British Library Cataloguing-in-Publication Data

A catalogue record for this book is available from the British Library

ISBN 978-0-12-803472-9
ISSN 0167-9309

For information on all Academic Press publications

visit our website at https://www.elsevier.com/books-and-journals

Publisher: Nikki Levy

Acquisition Editor: Patricia Osborn
Editorial Project Manager: Jaclyn A. Truesdell
Production Project Manager: Punithavathy Govindaradjane
Cover Designer: Matthew Limbert

Typeset by SPi Global, India

Contents

Preface ix 3.3. Invasions by Oysters and Other Bivalves 95

Acknowledgments xv 3.3.1. The Pacific Oyster Crassostrea
gigas as an Invasive Species 96
3.3.2. Predicting Invasion Outcomes:
The Mussel Mytilus galloprovincialis
1. Phylogeny 1 in South Africa and the Oyster
Crassostrea ariakensis in the
1.1. Introduction 1 United States 102
1.2. Origins and Classification 2 3.4. Range Boundaries and Dispersal 106
1.3. Phylogenetic Systematics 7 3.4.1. Larval Dispersion 107
1.3.1. Some Oyster Phylogenies: Fossils 11 3.5. Temperature and Species Range 117
1.3.2. Some Oyster Phylogenies: 3.5.1. Correlations Between Species’
Recent Taxa 14 Distributions and Tolerance 117
1.3.3. Some Oyster Phylogenies: Species 3.5.2. Temperatures and Intertidal
Identities 16 Bivalves 120
1.4. Phylogeography 22 3.5.3. Thermal Stress and Heat-Shock
1.4.1. Population Structure 22 Proteins in Oysters 121
1.4.2. Isolation by Distance 27 3.6. Decline and Extirpation of Populations 123
1.4.3. Sweepstakes Reproduction, 3.7. Modeling Species’ Distributions 124
Selection, and Hybridization 29 Bibliography 130
1.4.4. Physiological Differences Among
Populations 35 4. Ecology II: Distribution at Local
Bibliography 38
Scales 139
2. Evolution 47 4.1. Introduction 139
4.2. Oysters and Estuaries 141
2.1. Introduction 47 4.2.1. Salinity Tolerance 143
2.2. Patterns in the Rates and Trajectories 4.3. The Food of Oysters 161
of Bivalve Evolution 49 4.3.1. Retention Efficiency 162
2.2.1. Diversifications in Time 51 4.3.2. The Seston: Quantity
2.2.2. Diversifications in Space 55 and Quality of Suspended
2.3. Some Drivers of Evolution in Oysters 56 Particles 166
2.3.1. Heterochrony and Larval Life 56 4.3.3. Hydrodynamics and the
2.3.2. Size and Shape 63 Food Supply 184
2.3.3. The Ecology of Some Fossil Oysters 71 Bibliography 198
2.3.4. Predation as a Driver of
Evolutionary Change 73
5. Feeding 209
2.3.5. Adaptation 77
Bibliography 82 5.1. Introduction 209
5.2. Particle Uptake 210
3. Ecology I: Distribution at Regional and 5.2.1. Particle Transport and Sorting
Global Scales 89 Within the Pallial Cavity 212
5.2.2. Morphological Variability
3.1. Introduction 89 of the Pallial Organs 217
3.2. The Biogeography of Oysters 90 5.2.3. Selection and Selection Efficiency 219

v
vi Contents

5.3. Ventilation, Particle Capture, and 7.4.4. Gametogenesis and Spawning 450
Clearance 235 7.4.5. Energy Allocations 451
5.3.1. Particle Filtration and Ambient 7.4.6. The Testing of Bioenergetics
Water Flow 235 Models 454
5.3.2. Measuring Feeding Behavior 7.5. Stoichiometry and Growth 457
in the Field 243 7.6. Dynamic Energy Budget Models 469
5.3.3. Particle Capture and Clearance 250 7.6.1. The Standard DEB Model,
5.4. The Functional Morphology of Digestion With an Emphasis on Bivalves 469
and Absorption 275 7.6.2. Environmental Forcing
5.4.1. The Stomach and Digestive Gland 277 by Temperature and Food 483
5.4.2. Intestinal and Glandular Feces 280 7.6.3. Parameter Estimation and the
5.4.3. Absorption and Absorption General Model for Oyster Growth 483
Efficiency 282 7.6.4. The Validation and Application
5.4.4. Metabolic Fecal Loss 291 of DEB Models of Bivalves 485
5.5. Modeling Feeding Behavior 292 7.7. Comparing DEB and Scope
5.5.1. Optimal Feeding Models 292 for Growth (SFG) Models 491
5.5.2. Guts as Chemical Reactors 295 Bibliography 494
5.5.3. Stoichiometry Models 298
5.5.4. A Mechanistic Model 8. Temperature Effects and Other
of Absorption and Gut Transit Time 305 Manifestations of Stress 505
5.5.5. The Geometric Framework 306
5.5.6. The Inducible Response 8.1. Introduction 505
to Predators as a Cost of Feeding 311 8.2. Temperature Effects 506
Bibliography 314 8.2.1. Oxygen- and Capacity-Limitation
of Thermal Tolerance 509
8.2.2. The Heat-Shock Response 511
6. Metabolic Expenditure 331
8.2.3. Methodology 513
6.1. Introduction 331 8.2.4. Two Examples: An Antarctic
6.2. Respiration and the Regulation of Oxygen Bivalve and the European Flat
Uptake 332 Oyster 514
6.3. Levels of Metabolic Rate 336 8.2.5. Mitochondria and Thermal
6.3.1. Components of Standard Tolerance 520
(and Substandard) Metabolic Rate 338 8.2.6. Temperature and the Transcriptome 525
6.3.2. Maintenance Metabolic Rate 355 8.2.7. Ecological Limits 538
6.3.3. Routine Metabolic Rate: 8.3. The Effects of Multiple Environmental
The Effects of Body Size and Genetic Factors on Growth 541
and Feeding 358 Bibliography 554
6.4. Nitrogen Excretion 395
Bibliography 403 9. Reproduction 565
9.1. Introduction 565
7. Growth 417
9.2. Gamete Production 565
7.1. Introduction 417 9.2.1. Hermaphroditism, Sex-Change,
7.2. Measuring Shell Growth 418 and Sex-Ratios 565
7.2.1. Shell-Marking Techniques 418 9.2.2. The Reproductive Cycle 576
7.3. The Description of Growth 427 9.2.3. Spawning and Fertilization 591
7.3.1. The von Bertalanffy Growth 9.2.4. Nutrition, Storage Cycles, and
Model 427 Gametogenesis 600
7.3.2. Growth Models, Aspects 9.2.5. Fecundity and Reproduction
of Life History, and Some Costs, Effort, and Value 610
Bioenergetics 432 9.3. The Oyster Larva 617
7.4. Bioenergetics Models 436 9.3.1. Larval Development and Nutrition 617
7.4.1. Food Consumption 440 9.3.2. Swimming, Settlement, and
7.4.2. Respiration 447 Metamorphosis 655
7.4.3. Excretion 448 Bibliography 683
 Contents vii

10. Oysters and the Ecosystem 703 10.6.2. Biodeposition and Nutrient
Cycles 761
10.1. Introduction 703 10.6.3. Biodiversity 774
10.2. Oysters as Keystone Species 10.6.4. Valuing Ecological Services 792
and Ecological Engineers 704 10.7. Carrying Capacity 793
10.3. The Decline of Oysters 709 10.7.1. Statistical Models 794
10.3.1. Baselines, Shifting 10.7.2. Biomass/Production
and Otherwise 709 Relationships and Self-Thinning 795
10.3.2. Population Changes 711 10.7.3. Biofiltration and the
10.3.3. Global Declines in Oyster Food Supply 797
Numbers 721 10.7.4. Box Models 798
10.3.4. Local Declines 723 10.7.5. Fully Spatial Models 803
10.4. Oysters and Ecosystem Trophic 10.7.6. Other Models 808
Networks 729 Bibliography 818
10.5. The “Structured Habitats”
of Oysters 739
10.6. Ecosystem Functions and Services 745
10.6.1. Biofiltration 747 Index 835
This page intentionally left blank
Preface

The time seems right to try to condense into one place an account of research on oysters, as a contribution to current
advances and new opportunities for understanding how they “make a living.” The advances are in two areas, function
at the molecular level and the part played by bivalves in the ecology of coastal seas. Knowledge at the organismal level
provides the bridge between these two areas of research. However, the information is in danger of being lost to working
scientists because of its shear mass and the variety of outlets in which it is published. Edible oysters (the family Ostreidae)
are my focus of attention because they are significant in aquaculture and in the ecology of the coastal benthos, and because
they serve increasingly as experimental models for functional analysis. In a recent bibliometric survey, Guo, Xu, Feng, and
Zhang (2016) used the Science Citation Index to identify 11,493 publications on these oysters between 1991 and 2014
(9604 research articles, 694 meeting abstracts, and 400 reviews). The articles were in 1463 journals, 1259 of which
had published <10 relevant papers. And 10 countries were noted as publishing more than 250 of these papers, including
3960 in the United States, 1456 in France, 888 in China, 566 in Japan, and 274 in Brazil.
Aquaculture currently contributes approximately half of the fish (finfish þ shellfish) consumed worldwide and has been
described as the most vibrant sector of the global food system (Troell et al., 2014). Reports by the Food and Agriculture
Organisation of the United Nations (FAO) attest to an increasingly important role for oysters in aquaculture. For example,
the Pacific oyster, Crassostrea gigas (Thunberg, 1793), due to its potential for rapid growth and tolerance of a wide range of
environmental conditions, has become the species of choice for cultivation in many regions of the world. From its origins in
Japan and following widespread introductions elsewhere (Guo, 2009) its worldwide aquaculture production continues to
expand, from 156,000 tonnes in 1950 to 437,000 per annum by 1970, 1.2 million tonnes in 1990 and reaching nearly 4.5
million tonnes 13 years later (FAO Fisheries and Aquaculture Department: Cultured Aquatic Species Information Pro-
gramme). A related species, the Eastern oyster Crassostrea virginica (Gmelin, 1791), has been harvested for many years
in the United States but now, following the introduction of C. gigas, accounts for less than 35% of the total oyster landings
in that country. Other species of Crassostrea, such as C. angulata and C. sikamea (successfully cultured in China and
Japan), the mangrove oysters of the tropics (C. gasar, C. rhizophorae), and oysters in the genera Ostrea and Saccostrea,
also contribute to total oyster landings worldwide that are now in excess of 5.5 million tonnes per annum, or  38% of total
molluscan aquaculture.
The importance of oysters to the coastal ecosystems of the world (especially estuaries) is expressed in a variety of ways.
The three genera that are the subject of this book (Crassostrea, Ostrea, and Saccostrea) are, for different reasons, com-
monly described as ecosystem engineers and/or functional dominants. The topic is discussed in Chapter 10, but the general
features are well known: as filter feeders, oysters facilitate benthic/pelagic exchanges that influence the balance between
production cycles in the water column and in the sediments; their propensity for creating reefs and other surficial hard
substrate (oyster shell) contributes significantly to increased habitat diversity and biodiversity in otherwise soft-sediment
habitats. They are therefore key species in the functioning of coastal ecosystems, the net outcome of which is the provision
of various ecological services that have societal value, in addition to their value as a food.
A knowledge of oysters therefore contributes to two of the most pressing problems facing ecology as a predictive
science—how will climate change affect the security of global food provision, and how will the anticipated changes in
environment influence the biodiversity of coastal systems? Environmental change elicits three overlapping categories
of response in organisms: their inherent phenotypic plasticity may be expressed without involving changes in the genotype;
they may alter their distribution in space to escape unfavorable changes in habitat—and even though oysters are attached
and sessile as adults, the existence of a dispersive larval stage allows for population migration; and, if forced beyond the
limits of effective phenotypic response alone, the genetic structure of the population may alter over time (genetic diver-
sification leading to speciation). Oysters have provided a rewarding research focus in all three topics—phenotypic plas-
ticity, the connectivity between populations, and genetic pattern in spatially distinct populations. Although strictly
aquacultural aspects of oyster biology are not discussed in this book, relevant features of their physiology, reproduction,
and ecology are.

ix
x Preface

Researchers considering oysters as subjects for investigation are immediately struck by the immense volume of
available literature. This book has been written by drawing on many of the publications available in the refereed journals,
but only a small fraction of the whole are discussed in detail. In selecting papers for discussion my aim has been to provide a
convincing sample of the scholarship involved, without any pretence of complete coverage. I have benefited from previous
efforts to do the same, including C.M. Yonge’s “Oysters” (1960: The New Naturalist series, Collins, London), Paul
Galtsoff’s peerless “The American Oyster Crassostrea virginica Gmelin” (1964: US Fish and Wildlife Service Fishery
Bulletin 64), and many of the chapters in “The Eastern Oyster Crassostrea virginica” edited by Victor Kennedy, Roger
Newell, and Albert Eble (1996: Maryland Sea Grant).
On reading this literature, one issue cannot be ignored. This is a tendency in many published investigations to miss or to
disregard the wider context provided by both theoretical and empirical studies, the latter including other taxa. These missed
opportunities have compromised the ability of the research to meet two challenges: the gain in insight that is possible when
well-judged hypotheses on the interactions between “whole organism” and “molecular” approaches can be formulated; and
the growing demand for computer models that formalize and can be used to predict these effects. Models are essential in
capturing the complexities of ecological systems as they adapt to, or are degraded by, climate change, and they require that
the physiology and behavior of individual organisms be represented. However, the effective inclusion of data on physio-
logical traits to bridge between organismic and molecular approaches, or in making ecological models, depends on a legit-
imacy that is only afforded by appropriate theory. Without this there is a danger of what Levins (writing in 1968) called “an
indigestion of facts” (the problem works both ways: Levins also observed that theoretical work may diverge too far from life
and “become exercises in mathematics inspired by biology rather than an analysis of living systems”). Various examples
are briefly touched upon in this book. Though often understated (due to limits on space), the potential for expressing
soundly based physiological understanding in concepts such as macrophysiology, for example (Chown, Gaston, &
Robinson, 2004; Osovitz & Hofmann, 2007), or individual-based models (Judson, 1994), will be evident to the reader.
But two examples of the drive for legitimacy are worth discussing here (they are covered more fully in relevant chapters).
They both concern the growth of individuals, the first in terms of computer modeling of growth from a knowledge of phys-
iological rates, and the second in terms of the integration between growth and the molecular biology of these traits.
Identifying growth as the difference between rates of energy gain from the food and of metabolic expenditure to ensure
survival has been researched for many years. In Chapter 6 a starting point for discussion is suggested in the application
of von Bertalanffy’s concept of growth as the difference between mass-dependent rates of anabolism and catabolism. From
this simple insight there has grown a large and effective body of theory applied to predicting growth, including the rates
of energy gain and loss by individual organisms, the increase and decline of populations, and the relationships between
these processes and evolutionary fitness. However, doubts concerning the fundamental nature of energy transfers within
organisms, uncertainties arising from empirical representations of the rates of these processes in different species, and
difficulties in describing the dynamics of growth when simulated in this way stimulated the derivation of a more dynamic
description of energy budgeting (Bas Kooijman, 1993, 2010: “Dynamic Energy Budget Theory for Metabolic Organi-
sation,” Cambridge University Press).1 DEB theory now provides the platform of choice for including maintenance,
growth, and reproduction of organisms in ecological models. The narrative of the development of these ideas over the
last 100 years is an instructive example of scientific method and progress. It hinges on the need for a general theory
that predicts the dynamic behavior of species and in circumstances that extend beyond a limited empirical base. Physio-
logical ecologists now possess the means to set their analyses, with confidence, within an appropriate theoretical construct.
The functional biology of oysters and other bivalves has played a key part in the development of these ideas (Chapter 7)
and continues to do so.
A description of the genome of the oyster Crassostrea gigas was published in 2012 by Guofan Zhang and his many
coauthors, a watershed for research on the biology of oysters. From the outset, an emphasis was placed on what the genome
reveals about this oyster’s capacity to resist the stresses imposed by estuaries and the intertidal (the paper was titled “The
oyster genome reveals stress adaptation and complexity of shell formation”). In a subsequent review, Zhang et al. (2016)
described in more detail the genomic response to environmental factors such as temperature, salinity, hypoxia, air exposure,
and exposure to pathogens, and they “. . .used genome analysis to highlight the strong cellular homeostasis system, a unique
adaptive characteristic of oysters.” The authors of these and related studies have been impressed by the large number of
genes or “gene sets” that contribute to defense against physical stressors and potential pathogens. For example, apoptosis
(the physiological process by which organisms maintain an equilibrium between cell proliferation and cell death) is viewed

1. A generalization of mass- and temperature-dependent metabolic relationships to provide a basis for a unified theory of ecology (“Toward a metabolic
theory of ecology”; Brown, Gillooly, Allen, Savage, & West, 2004) is also pertinent here but a discussion is beyond the reach of this book (see Sibly,
Brown, & Kodric-Brown, 2012; Humphries & McCann, 2014).
 Preface xi

as a focal process in the oyster’s cellular stress response. The oyster genome revealed 48 genes coding for apoptosis inhib-
itors (Cg—for C. gigas—IAPs), compared with 7 in sea urchins, 5 in Drosophila, and 8 in humans. This finding implied the
presence of an especially complex system to delay cell death and allow time for the repair of cellular damage (in apoptosis,
unlike cell lysis, cell death is regulated or “programmed”): Importantly, “. . .at the molecular level, the expansion, func-
tional diversity and high expression of key gene families [including heat shock protein 70 and the IAPs] are probably central
to the oyster’s adaptation to sessile life in the intertidal zone” (Zhang et al., 2016).
Zhang and colleagues (2016) then ask the following questions: (a) Why are so many defense-related genes found in
oysters? (b) Are these genes all functional, and if so, are they indicative of plasticity in the cell’s stress responses and
involved in acclimation to stress? (c) What roles do these genes play in adaptive differentiation? These questions cannot
be answered by a description of the genome alone; they demand a collaborative effort between molecular geneticists and
physiologists. The techniques available to the molecular biologist include screening the transcription of the genes, silencing
specific genes, and mapping the proteins that are expressed (the proteome) when the organism is exposed to a change in
environment. In a review of proteomics in the study of adaptations to environmental stress Tomanek (2014) describes the
proteome as “. . .a dynamic and complex network that can respond quickly to environmental change and, in many ways,
does so independent of the genome, eg without requiring transcriptional activation.” Responses that do not require mod-
ification of the genomics include a host of posttranslational processes and protein-protein interactions, and these will not be
predicted simply by mapping the transcriptome. Noble (2006: “The Music of Life: Biology beyond the Genome,” Oxford
University Press) makes the wider point elegantly. To paraphrase using his words: “A gene will do one thing in one set of
circumstances and another if circumstances change. . .they operate under control. Genes are controlled by proteins. Those
proteins are in turn coded for by other genes. The genes cannot do what they do without the proteins. And the proteins are
not free agents either. They respond to influences from across the rest of the organism and ultimately from the environment,
too.” This is “downward causation” (see Fig. 1, which is a modification redrawn from Noble, 2006). “So even if we speak of
gene-protein networks, we must be careful. These are not networks that operate independently of higher-level processes.”
Comparisons of the proteome among populations that are experiencing different levels of environmental stress (and
resulting, for example, in differences in the proportional expressions between functional gene families that signal quali-
tatively different impacts on the organism) help to formulate hypotheses for causal relationships between the gene and the
animal’s response. These hypotheses must then be tested by direct investigation of the functional link between genotypic
and phenotypic variation, including individual genes. Oysters have proved to be an effective model in this endeavor. Not
only is there a considerable knowledge base supporting both genomic and physiological investigations, but the resources
of oyster hatcheries can also be employed to produce genetically defined families. Hedgecock, Manahan, and colleagues
(e.g., Hedgecock, McGoldrick, & Bayne, 1995, Hedgecock et al., 2007; Applebaum, Pan, Hedgecock, & Manahan, 2014;
Frieder, Applebaum, Pan, Hedgecock, & Manahan, 2016) demonstrate the power of linked genetic-genomic-physiological
approaches to understanding growth and adaptations to environmental change, using the Pacific oyster. For example,
they warn that experiments with wild-caught individuals subjected to different environmental conditions cannot adequately
control for genotype (G) and genotype  environment (E) interactions: “Experiments that manipulate G and, most impor-
tantly, G  E, as well as E, to produce phenotypic contrasts that integrate genomic, transcriptomic, proteomic and

FIG. 1 Emphasis is given to downward-acting inter- Downward causation

actions. Noble writes: “Loops of interacting downward
Organism
and upward causation can be built between all levels of
biological organisation.” (Redrawn from Noble, 2006).
Higher-level
triggers of cell Tissues/organs
signaling

Cells Higher-level
controls of gene
expression
Biochemicals pathways

Protein Proteins
machinary
reads genes
Genes
xii Preface

metabolomic with classical biochemical and physiological approaches are required to understand and to predict the
Darwinian responses of organisms to global change.”
The approach described by Noble to understand the functioning organism is not a retreat from reductionism. Rather, it is
a recommendation to concentrate investigations on the points of contact, the interactions and feedbacks, between precisely
defined entities, such as the cell and the matrix of gene-protein interactions. This provides direction to research, and is the
subject of Richard Lewontin’s influential book (2000: “The Triple Helix: Gene, Organism and Environment,” Harvard
University Press). Lewontin argues that every biologist knows that the information in DNA sequences is insufficient to
specify even a folded protein, never mind an entire organism (“. . .if we want to understand which protein is produced
from a gene, we must investigate the complete chain of production in its spatial and temporal detail”); and that organisms
and their environments are in a constant state of flux in which both act as cause and effect in the evolutionary process. There
are many insights in this short book to guide the physiological ecologist who works in collaboration with molecular genet-
icists. For example, Lewontin argues that, as a result of its structural and functional heterogeneity, an organism may be
thought of as a “nexus of a large number of interacting forces that are individually weak.” Experimental science normally
consists of trying to hold most of these forces constant while strongly perturbing one of them to measure its influence. But
it may be misleading then to extrapolate this effect, given a background of many other causal processes acting contem-
poraneously. “Many of the problems of understanding in biology appear when experimental perturbations, chosen because
they can be studied conveniently, are extrapolated to normal circumstances” (Lewontin). The organism in its natural setting
is the appropriate subject of study.
This problem of extrapolation is a serious constraint when applying the results of laboratory experiments to scale phys-
iological responses in the natural environment, and to incorporate physiological traits into ecological models. The point is
illustrated by Angilletta and Sears (2011) in a discussion of the concept of the niche (Lewontin describes the niche as a
flawed metaphor), and in discriminating between the fundamental and the realized thermal niche when attempting to
predict the effects of climate change. The idea that the environment of an organism is causally independent of the organisms
and that “. . .changes in the environment are autonomous and independent of changes in the species itself, is clearly wrong”
(Lewontin). Two aspects can be highlighted (see the review of The Triple Helix by Lloyd, 2004), and both are important in
the biology of oysters. The first is that organisms change their environments by living in them. The gregarious nature of
oysters ensures significant engineering of both their macro- and microenvironments (Chapters 5 and 10). The second is
related but more nuanced. The organism defines its own environment by its phenotypic poise, determining what features
are important for its own survival and performance. It follows that the concept of the niche as a collection of physical and
biological features that may or may not be inhabitable by the organism is unhelpful. Angilletta and Sears (2011) concluded
that “perhaps the best way to circumvent this problem would be to model the niche as an emergent property of a phenotype
interacting with its environment.” The current generation of “mechanistic niche models” does this by using the empirical
knowledge base, formalized in dynamic (and stoichiometrically balanced) submodels, to suggest hypothetical relationships
between environmental factors and physiological performance (Kearney & Porter, 2009). The testing of these models
requires measurements of performance (growth, reproduction, and survival) and their monitoring in the natural envi-
ronment. This is familiar territory for the physiological ecologist whose research can now be enriched by matching the
results to changes in the expression of specific genes.
This book is intended as an account of some of what we know (and some of what we do not know but may infer from
studies of other species) of the biology of oysters, including their phylogeny, evolution, ecology, and physiology, and of the
mechanistic models that are proposed for encapsulating this knowledge in a format useful for prediction. There are gaps in
the coverage, four in particular. The book offers no advice on how to prepare oysters for the table (of the many texts
available, try “Consider the Oyster” by MFK Fisher, 1988: North Point Press, New York; and for a wider historical
treatment see “Oyster: A World History” by Drew Smith, 2010: The History Press, Stroud). The aquaculture of oysters
is not considered because this is covered in detail elsewhere (e.g., “Bivalve Molluscs: Biology, Ecology and Culture”
by Elizabeth Gosling, 2003: Fishing News Books, Oxford). However, this gap extends to research on the restoration of
degraded or lost oyster habitat, which is a timely and popular topic and a test bed of ideas on how oysters affect and
are affected by their environment and the ecosystem (e.g., “Shellfish Aquaculture and the Environment,” edited by Sandra
Shumway, 2011: Wiley and Sons, Chichester). Regretfully, neither space nor time allowed me to include a discussion
of this important subject (but see the journal “Restoration Ecology,” published for The Society for Ecological Restoration).
I also regret not being able to include disease, for the same reasons (“Infectious Disease in Aquaculture: Prevention and
Control,” edited by Brian Austin, 2012: Woodhead Publishing, Oxford). I am aware that an account of the ecology of
oysters that does not include disease does not do full justice to the subject, since disease-mediated mortality has been
(and still is) a significant cause in the decline of oyster stocks worldwide, and a constraint on efforts to cultivate oysters
given the ubiquitous existence of pathogens.
 Preface xiii

The fourth area that I do not include is the genomics and molecular biology of oysters. The book was specifically
planned as an account of the biology of oysters, primarily at the organismal level, in the hope that this would contribute
to future developments by providing some context, along the lines discussed above, for the very rapid growth in molecular
research. I know of other researchers who will in time extend the present narrative into these new and exciting areas.

REFERENCES
Angilletta, M. J., & Sears, M. (2011). Coordinating theoretical and empirical efforts to understand the linkages between organisms and environments.
Integrative and Comparative Biology, 51, 653–661.
Applebaum, S., Pan, T. -C., Hedgecock, D., & Manahan, D. T. (2014). Separating the nature and nurture of the allocation of energy in response to global
change. Integrative and Comparative Biology, 54, 284–295.
Brown, J., Gillooly, J., Allen, A., Savage, V., & West, G. (2004). Toward a metabolic theory of ecology. Ecology, 85, 1771–1789.
Chown, S., Gaston, K., & Robinson, D. (2004). Macrophysiology: Large-scale patterns in physiological traits and their ecological implications. Functional
Ecology, 18, 159–167.
Frieder, C., Applebaum, S., Pan, T. -C., Hedgecock, D., & Manahan, D. T. (2016). Metabolic cost of calcification in bivalve larvae under experimental
ocean acidification. ICES Journal of Marine Science. http://dx.doi.org/10.1093/icesjms/fsw213.
Guo, X. (2009). Use and exchange of genetic resources in molluscan aquaculture. Reviews in Aquaculture, 1, 251–259.
Guo, X., Xu, F., Feng, Z., & Zhang, G. (2016). A bibliometric analysis of oyster research from 1991 to 2014. Aquaculture International, 24, 327–344.
Hedgecock, D., Lin, J. -Z., DeCola, S., Haudenschild, C., Meyer, E., Manahan, D. T., et al. (2007). Transcriptomic analysis of growth heterosis in larval
Pacific oysters (Crassostrea gigas). Proceedings of the National Academy of Sciences of the United States of America, 104, 2313–2318.
Hedgecock, D., McGoldrick, D., & Bayne, B. L. (1995). Hybrid vigour in Pacific oysters: An experimental approach using crosses among inbred lines.
Aquaculture, 137, 285–298.
Humphries, M., & McCann, K. (2014). Metabolic ecology. Journal of Animal Ecology, 83, 7–19.
Judson, O. (1994). The rise of the individual-based model in ecology. Trends in Ecology & Evolution, 9, 9–14.
Kearney, M., & Porter, W. (2009). Mechanistic niche modelling: Combining physiological and spatial data to predict species’ ranges. Ecology Letters, 12,
334–350.
Levins, R. (1968). Evolution in changing environments: Some theoretical explorations. Princeton, NJ: Princeton University Press.
Lloyd, E. A. (2004). Book review: Richard C Lewontin, 2000. The triple helix: Gene, organism and environment. Harvard University Press, Cambridge,
MA. Journal of Bioeconomics, 6, 97–104.
Noble, D. (2006). The music of life: biology beyond the genome. Oxford: Oxford University Press.
Osovitz, C., & Hofmann, G. (2007). Marine macrophysiology: Studying physiological variation across large spatial scales in marine systems. Comparative
Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 147, 821–827.
Sibly, R., Brown, J. H., & Kodric-Brown, A. (2012). Metabolic ecology: A scaling approach. Oxford: Wiley-Blackwell.
Tomanek, L. (2014). Proteomics to study adaptations in marine organisms to environmental stress. Journal of Proteomics, 105, 92–106.
Troell, M., et al. (2014). Does aquaculture add resilience to the global food system? Proceedings of the National Academy of Sciences of the United States
of America, 111, 13257–13263.
Zhang, G., Li, L., Meng, J., Qi, H., Qu, T., Xu, F., et al. (2016). Molecular basis for adaptation of oysters to stressful marine intertidal environments. Annual
Review of Animal Biosciences, 4, 357–381.
Zhang, G., et al. (2012). The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490, 49–54.
This page intentionally left blank
Acknowledgments

My first and most sincere appreciation is to my family, especially my wife Marianne, who have tolerated my seclusions
with patience and grace. Many friends read various sections, not to correct my mistakes but to advise me on the form the
book was taking and the direction of travel. I acknowledge Dennis Hedgecock, Jerry Hilbish, Richard Koehn, Donal
Manahan, Enrique Navarro, and Tony Underwood. Sandy Shumway helped in the interface with the publishers, and Ellie
Kramer-Taylor helped with getting permissions to reproduce illustrations, and Eric Heuple for the cover design. My thanks
to all the Journals and the Publishers that gave their permission to use their illustrations in the Figures for this book. Tony
Underwood and Gee Chapman provided encouragement from the start. I could not have progressed beyond the first page
without access to the amazing resources of the Library of the University of Sydney and the National Library of Scotland in
Edinburgh. Finally, I dedicate the book to my grandchildren Eren and Ula, as evidence that I did at last complete Chapter 9.

xv
This page intentionally left blank
Chapter 1

Phylogeny

Within certain limits, defined by the fact that the shell consists of two hinged valves, oysters are among the most plastic
organisms known

Gunter (1954)

The oysters are probably the most difficult single group of macrofossils to classify
Cleevely and Morris (1987)

1.1 INTRODUCTION
The view expressed by Cleevely and Morris (1987) and quoted above is widely shared by others who would welcome a
coherent and enduring system of classification that includes both fossil and living oysters. Stenzel (1971) wrote of a
“. . .protean diversity of form in the family Ostreidae, displayed even within well-defined, geographically and genetically
isolated, living oyster species [and which] is not amenable to easy classification.” It is now commonplace for research
papers to start with a similar remark. For example, the taxonomy of oysters “. . . is difficult and often inaccurately deter-
mined because of the high level of phenotypic plasticity of the shell morphology” (Xia, Wu, Xiao, & Yu, 2014); this is often
followed by a proposal for a new or modified phylogeny based on molecular characters. The use of molecular sequences
has expanded rapidly as more potential markers of genealogical relationships have been identified, and the technology that
can recognize and analyse their distribution amongst taxa has developed in parallel. Attempts to discern the phylogeny of
groups of organisms can be traced from the use of allozymes (enzymes encoded by different alleles of the same locus),
thence of targeted genes in the mitochondrial and nuclear genomes, and the current phase of phylogenomics in which mul-
tiple gene loci and even entire genomes can be searched for their application in phylogenetic reconstruction (Dunn et al.,
2008; Boore & Fuerstenberg, 2008). At each step in this progress there has been the challenge of incongruence between
different markers in the phylogenetic patterns that are resolved statistically, between morphological and molecular char-
acters, and between genetic loci.
In this chapter I discuss aspects of the search for clarity in the phylogeny of oysters, in which morphological and
molecular characters have been employed both separately and together. The heuristic power of molecular phylogenetics
is impressive; the morphological and ecological contexts in which phylogenetic resolution is set are rich and complex; and
the search for the relevant evolutionary processes involves knowledge across a wide range of research endeavor—the fossil
record, speciation, life history, larval dispersal, population structure, and the geography of oyster distributions. Multilocus
genomic analysis is bringing new clarity to phylogenetic relationships within the Mollusca in general (Smith et al., 2011)
and the Bivalvia in particular (Bieler et al., 2014; Plazzi, Ceregato, Taviani, & Passamonti, 2011; González et al., 2015) and
with the promise of doing so for families of oysters. Phylogenetic analysis at any taxonomic level (among populations,
species and/or higher taxa) is an exercise in hypothesis setting. Testing predictions for genealogical relations inevitably
involves the underlying ecological and evolutionary processes that determine the proposed phylogenetic pattern. And
resolving these relationships will continue to challenge an understanding of the biology of oysters, in all its aspects.
The likely benefits include the conservation of stocks and maintenance of biodiversity, and in understanding the evolu-
tionary trends in this important group of animals.

Biology of Oysters, Vol. 41. http://dx.doi.org/10.1016/B978-0-12-803472-9.00001-7

© 2017 Elsevier Inc. All rights reserved. 1
2 Biology of Oysters

1.2 ORIGINS AND CLASSIFICATION

Identifying the earliest oysters has proved to be difficult and controversial. This is not surprising, given the paucity of fossils
of the appropriate age and the limited number of definitive morphological characteristics that can be deduced from them.
The most relevant geological period, the early Triassic some 250 million years ago, has been described by Fortey (1997) as
a dark age of geological time when fossils are hard to come by and well-preserved oysters or their putative ancestors are rare
(Hautmann, 2006). By the Jurassic 40 my later the fossil record for oysters is better. Considerable plasticity of shell shape is
a common feature of oysters and their close relatives, however, and taxonomic analyses based only upon shell shape are
unreliable. To quote Stenzel (1971) again: “The first prerequisite in oyster classification is the availability of ample
material.” There are relatively few characters other than shape to work with when trying to interpret a fossil’s taxonomic
position. Of the features considered diagnostic (listed in Panel 1.1) only those associated with shell mineralogy, shell orna-
mentation, the form of the hinge and ligament, impressions left on the inside of the shell by muscle insertions, and evidence
of whether attachment to the substrate was by the left or the right valve, are normally available. And even these few features
are made difficult to categorize a priori as either ancestral or derived due to the common occurrence within the Bivalvia of
homomorphy (similar morphologies in unrelated groups), convergence between unrelated taxa, and secondary loss of ana-
tomical features.
There are also pitfalls in relating diagnostic morphological features in living individuals to the phylogenetic interpre-
tation of fossils. For example, shells comprising foliated calcite evolved in at least two other orders of bivalves. The shell of
present-day adult oysters is primarily calcitic, but this may not have been so in the early lineage. (The shells of oyster larvae
are aragonitic.) Historically, shell mineralogy varied with changes in water chemistry and temperature (Harper, Palmer, &
Alphey, 1997; Carter, Barrera, & Tevesz, 1998; Hautmann, 2006) such that the earliest oysters may have ranged in com-
position between predominantly aragonitic and predominantly calcitic shells (Malchus, 2008). An early ostreid, Umbostrea
was described by Hautmann (2001) as having an aragonitic inner shell layer, and this was not uncommon in oysters of that
age: Hautmann writes “. . .the loss of aragonitic shell layers in the Ostreidae seems to coincide with the change from an
‘aragonite sea’ to a ‘calcite sea’ (Sandberg, 1983) at the Triassic/Jurassic boundary.”1 Another example concerns cemen-
tation by the left valve, which is considered a defining character of oysters but may have been variable in some ancestral
species (Márquez-Aliaga, Jimènez-Jimènez, Checa, & Hagdorn, 2005). Newell and Boyd (1970) suggest that the ratio of
left-valve to right-valve attachment in the earliest species may have been low, increasing gradually through the Triassic but
“. . .the historical facts remain obscure.” However, Hautmann and Hagdorn (2012) reexamined the relevant fossils and con-
firmed that attachment by the left valve, together with a characteristic (alivincular-arcuate) ligament, are indeed definitive
features of the true oysters. Fossils in two genera from the late Triassic (Umbostrea and Nacrolopha; Carter et al., 2011) are
probably close to the ancestral taxon.
Adult oysters are cemented to the substrate, but cementation evolved independently in many bivalve clades (Harper and
Kelley, 2012) and was accompanied by various mechanisms to strengthen the articulation between the two valves. In the
ostreids this took the form of a mirror imaging of the ligament between the right and left valves. “The resilifer of the right
valve is elevated and fits into the resilifer of the left valve, while the bourrelets of the left valve engage into the receding
bourrelets of the right valve” (Hautmann, 2004; see Panel 1.1); this type of ligament is an important morphological char-
acteristic of oysters. Checa and Jiménez-Jiménez (2003) describe the ribbed shell of oysters as “antimarginal,” that is the
ribs diverge from the center of the shell to remain approximately perpendicular to the shell margin throughout their growth.
This feature is present in both fossil and extant oysters and the authors make a case for including antimarginal shell ribs as a
characteristic feature of the Ostreidae (the shells of the Gryphaeidae are usually smooth). Some aspects of shell morphology
make a clear taxonomic statement, therefore, but uncertainties persist in establishing an evolutionary link between oysters
and other taxa, in part because of the specialized habit of oysters (sessile, cemented, and epibenthic), which tends to mask
characters shared with possible ancestral groups. To gain an idea of the differences of emphasis over the evolutionary origin
of oysters see the debate between Márquez-Aliaga et al. (2005), Hautmann (2006), Checa, Pablo Jiménez-Jiménez,
Márquez-Aliaga, and Hagdorn (2006), Malchus (2008), and Hautmann and Hagdorn (2012).
Molecular phylogeny of extant taxa provides some clarity. Ayala (2003) wrote: “The virtually unlimited evolutionary
information encoded in the DNA of living organisms allows evolutionists to reconstruct any evolutionary relationships that
have led to present-day organisms. . .with as much detail as wanted.” Molecular criteria are now the method of choice to

1. The change from an aragonitic to a predominantly calcitic shell coincident with a change in water chemistry may have been linked to adaptive changes
in life habit or due to the increased metabolic costs of secreting a calcite shell when the medium was aragonitic, and vice versa (Hautmann, 2006). In
comparative experiments the mineralogical composition of the shell had consequences for the shells’ mechanical properties (fracture strength); the calcitic
shells of oysters were considerably weaker than those of species with aragonitic shells. However, Hautmann (2006) found no association between shell
mineralogy and either a change in morphology or in the mode of life.
 Phylogeny Chapter 1 3

PANEL 1.1 A Diagnosis and Classification of Oysters (Based on Hautmann, 2001; Littlewood, 1994)

Diagnosis. (The terms in italics are defined in the table).

Oysters are monomyarian bivalves which are cemented by their left valve to the substrate in the postlarval stage (i.e., they are
“pleurothetic”). Settling from a planktonic to a benthic habit, and the accompanying metamorphosis, mark the end of the larval stage,
soon after which the foot and byssus are lost and subsequent attachment is by cementation which is mediated by the mantle. A pallial
line is missing except in Recent Saccostrea in which a disjunct line of pallial muscle insertions is present. The ligament is alivincular-
arcuate; the resilium is completely fibrous and continuous between valves; the ligament area has a broad resilifer, which is elevated on
the right valve. Bourrelets are narrow, hinge teeth lacking. Postlarval shells of modern forms comprise an outer layer of simple prismatic
calcite and a middle and inner layer of foliated calcite which may develop structural chambers. Aragonite is restricted to the myos-
tracum and ligostracum in post-Triassic forms, but occurred as an inner shell layer in Triassic species. Gills are pseudolamellibranch.
Classification (Littlewood, 1994; Carter et al., 2011)
Phylum Mollusca
Class Bivalvia
Subclass Pteriomorphia
Order Ostreida
Superfamily Ostreoidea
Family Ostreidae
Subfamily Ostreinaea
Tribe Ostreini [Ostrea3]
Family Flemingostreidae
Subfamily Crassostreinaea
Tribe Striostreini [Saccostrea1]
Tribe Crassostreini [Crassostrea2]
a
These are the “true” oysters and the main subject of this book.
Common names used here are: 1, rock oysters; 2, cupped oysters; 3, flat oysters.

To distinguish the subfamilies Ostreinae from Crassostreinae:

1. Right valve not plicate (Ostreinae) or plicate (Crassostreinae).
2. Muscle scar not colored (Ost) or pigmented (Crass).
3. Promyal chamber (connection on the right (upper) side between inhalant and exhalant chambers) absent (Ost) or present (Crass).
4. Larvae are incubated by the adult (Ost) or eggs and sperm are discharged into the sea for fertilization (Crass).
To distinguish the tribes Striostrini from Crassostreini:
5. Hyote spines absent (Crassostreini), present (Striostreini).
6. Chomata present (Strios), absent (Crass).
7. Labial palps fused (Strios), not fused (Crass).

Some morphological terms

Term Description
Monomyarian Having one adductor muscle, the ancestral anterior adductor having been lost
Bourrelets The attachment surface for the lateral ligament on the valves at the apex (hinge) of the shell, raised on the
left valve, recessed on the right valve
Byssus Threads attaching the larva to the substrate at metamorphosis; retained in some bivalves (e.g., mussels)
into the adult stage, but lost in oysters and functionally replaced by an adhesive produced by the mantle
lobes
Chomata Ridges on the right valve with corresponding pits on the left valve
Gill: Ascending and descending folds (lamellae) of the gills are linked by tissue connections between gill fil-
Pseudolamellibranch aments (Chapter 5). Oysters are pseudo-lamellibranch because these tissue connections are not as
extensive as in other eulamellibranch species. In filibranch bivalves (e.g., mussels, scallops) gill lamellae
are linked by interlocking cilia, not by tissue connections
Hinge teeth Projections of the shell at the hinge; present in the larva but lost in the adult and functionally replaced by
the folded (tongue-and-groove) nature of the ligament

Continued
Another random document with
no related content on Scribd:
 It must be noted that Salamanca’s name was not in the list of
Ministers suggested by Narvaez. The Queen wished it to be added,
but Narvaez declined to follow suit, as he knew that this statesman
was supported by Bulwer, whose dislike of the King was well known;
and the way he had spoken of Francisco before his wedding
naturally made the King averse to seeing him.
Bulwer worked with Bermejo against Isabella during the
premiership of Salamanca, and the publication in The Times of a
demand for the royal divorce was due to him.
At last Francisco and Isabella were reconciled. It was on October
13 that the King returned to the capital. He entered the gate of the
palace in a carriage drawn by six horses, with a mounted escort of
the Guardia Civil. He was dressed quietly in black, and Brunelli, the
Pope’s Legate, was seated on his left. Narvaez, Count Alcoy, Count
Vistahermosa, rode by the coach, and two carriages followed with
the high dignitaries of the palace.
The King looked pleased. General Serrano, whom he hated so
cordially, had left Madrid, and the Queen was waiting for him at the
window. Brunelli was about to follow the royal couple as they walked
away after their first meeting, but Narvaez said: “Whither away, Your
Eminence? Let them be alone with their tears and kisses. These
things are done better without witnesses.”
The Queen arrived that day at her dwelling in the Calle de las
Rejas. There was a family dinner-party in the evening at the palace,
and, in a private interview with her daughter, Maria Cristina begged
her to be more discreet in future; and she reminded her that although
she had, as a widow, allowed herself to be captivated by a
commoner, whilst she was the wife of the King she had never
allowed her thoughts to wander beyond the circle of her rank and her
duty.
 The reckless extravagance of the Queen excited much remark.
Courtiers are still living who recollect seeing Isabella give her
bracelets to the beggars who sometimes infest the courtyard of the
palace.
When Miraflores, who was considered the soul of truth, received
a reckless order from the Queen to dispense a certain amount of
money on some petitioner, he had the sum put in pieces on a table,
and it was only the sight of the large sum which was thus laid before
the Queen which showed her the extravagance of her command.
A great influence was soon found to be at work in the palace in
the person of Sister Patrocinio, whose brother, Quiroga, was one of
the gentlemen-in-waiting.
 CHAPTER XI
ATTEMPT ON THE LIFE OF QUEEN ISABELLA—THE OVERTHROW OF THE
QUEEN-MOTHER, MARIA CRISTINA

1850–1854

There was much variety of feeling when it was known that an heir to
the throne was expected. On the day of the birth, July 12, 1850, the
clerics, Ministers, diplomats, officers, and other important
personages of the realm, assembled at the palace to pay their
respects to the expected infant. But the bells and cannon had hardly
announced to the nation the birth of the girl-child when it expired. So
the dead form of the infant, which had only drawn breath in this world
for five minutes, was brought into the assembly of dignitaries, and
after this sad display the gathering dispersed in silence. The kind-
heartedness of the Queen was shown in her thoughtful generosity to
the nurses who were disappointed of their charge.
“Poor nurses, they must have felt it very much!” she exclaimed.
“But tell them not to mind, for they shall be paid the same as if they
had had my child.”
In February, 1852, an heir to the throne was once more expected,
and the birth of the Infanta Isabella was celebrated by the usual
solemn presentation. When the King showed the infant to his
Ministers, he said to the Generals Castaños and Castroterreño:
“You have served four Kings, and now you have a Princess who
may one day be your Sovereign.”
 It was on February 2, 1852, that the dastardly attempt was made
on the life of the Queen, just before leaving the palace for the
Church of Atocha, where the royal infant was to be baptized. The
Court procession was passing along the quadrangular gallery, hung
with the priceless tapestries only displayed on important occasions,
when Manuel Martin Merino, a priest of a parish of Madrid, suddenly
darted forward from the spectators lining the way, with the halberdier
guard. The petition in the cleric’s hand and his garb of a cleric led to
his step forward being unmolested, and the Queen turned to him,
prepared to take the paper. But the next moment the other hand of
the assassin appeared from under his cloak with a dagger, which he
swiftly aimed at the royal mother. Fortunately, the Queen’s corset
turned aside the murderous weapon, and, although blood spurted
from her bodice, the wound was not very deep; but she was at once
put to bed and placed under the care of the royal physicians.
The royal infant was promptly seized from the arms of its mother
at the moment of the attack, by an officer of the Royal Guard, and for
this presence of mind the soldier was afterwards given the title of the
Marquis of Amparo.
With regard to the assailant, the Queen said to her Ministers:
“You have often vexed me by turning a deaf ear to my pleas of mercy
for criminals, but I wish this man to be punished immediately.” And,
with the outraged feeling of the object of such a dastardly deed,
Isabella turned to the would-be murderer, and said: “What have I
ever done to offend you, that you should have attacked me thus?”
During the trial in the succeeding days the Queen softened to the
criminal, and said to her advisers: “No, no! don’t kill him for what he
did to me!”
However, justice delivered the man to the hangman five days
after his deed.
 The efforts to discover Merino’s accomplices were fruitless, and it
was thought that the deed had been prompted more by the
demagogue party than by the Carlists.
The cool, cynical manner of the cleric never left him even at the
moment of his execution.
When the priest’s hair was cut for the last time, he said to the
barber: “Don’t cut much, or I shall catch cold.”
The doomed man’s request to say a few words from the scaffold
was refused. When asked what he had wished to say, he replied:
“Nothing much. I pity you all for having to stay in this world of
corruption and misery.”
The ovation which the Queen had when she finally went to the
Church of Atocha to present the infant surpasses description.
Flowers strewed the way, and tears of joy showed the sympathy of
the people with the Queen in her capacity as mother, and at her
escape from the attempt on her life.
From 1852 to 1854 Isabella failed to please her subjects, and the
outburst of loyalty which had followed the attempt on her life
gradually waned. Curiously indifferent to what was for her personal
interest, as well as for the welfare of the country, Isabella turned a
deaf ear to the advice of her Ministers to dissolve a Cabinet which
was under the leadership of the Count of San Luis, who was known
to be the tool of Queen Maria Cristina, now so much hated by the
Spaniards. Miraflores wrote a letter to Isabella, advising the return of
Espartero, the Count of Valencia, but the letter never reached its
destination.
Remonstrances which had been made upon the Government
were now directed straight to the Throne.
“You see,” said her advisers, “how the persons whom you have
overwhelmed with honours and favours speak against you!”
 The Generals O’Donnell and Dulce finally took an active part
against the Ministry, supported by the Queen-mother and Rianzares.
The Count of San Luis was a man of fine bearing and charming
manners. He had been conspicuous in his early days for his
banquets and gallantries, but he had also been known for many a
generous deed to his friends; and it was noticeable that when the
tide of favour left him he was deserted by all those to whom he had
been of service.
The birth of another royal infant in 1854 excited little or no
interest in the capital, where discontent with the reigning powers was
so evident. General Dulce was accused in the presence of the
Queen and San Luis of having conspired against the Throne. This
the officer indignantly denied on the spot, declaring that never could
he have believed in the perfidy which had prompted the report.
At last the storm of revolution broke over Madrid, and the parties
of the Generals O’Donnell and Dulce came into collision with those
of the Government. Insulting cries against the Queen-mother filled
the streets, and during the three days’ uproar the house of Maria
Cristina, in the Calle de las Rejas, was sacked, as well as those of
her partisans. The furniture was burned in the street, and Maria
Cristina took refuge in the royal palace.
After the Pronunciamento of Vicalvaro and O’Donnell to the
troops, it was evident that the soldiers of the Escorial would also
revolt against the Government.
It was then that Isabella was filled with the noble impulse to go
alone to the barracks of the mutinous regiments and reason
personally with them. With her face aglow with confidence in her
soldiers and in herself, she said: “I am sure that the generals will
come back with me then to Madrid, and the soldiers will return to
their barracks shouting ‘Vivas’ for their Queen.”
 But this step, which would have appealed with irresistible force to
the subjects, was opposed by the Ministers, who objected to a
course which would have robbed them of their portfolios by the
Sovereign coming to an understanding with those who were
opposed to their opinions.

T H E C O U N C I L O F M I N I S T E R S O F I S A B E L L A I I . D E C L A R E S WA R
AGAINST MOROCCO

From a Painting by R. Benjumea

At this time Isabella received from the Infanta Josefa, daughter of

the Infanta Louisa Carlota and Francisco de Paula, a letter which
showed that the Princess had inherited her mother’s hatred of the
Queen-mother, Maria Cristina; for she wrote:
 “Your Majesty should distrust the artificial and partial counsels of
the Queen-mother. This lady, to whom you owe your birth, is
sacrificing you to her insatiable greed of gold. Beyond your life you
do not owe anything to Maria Cristina. She has done nothing for
Spain that you should give her submission and obedience in your
conduct as Queen. Hardly had Your Majesty’s father gone down to
his grave than his widow gave you the pernicious example of an
impure love, which began in a scandal, and ended, ten years later, in
a morganatic marriage, to the incalculable harm of the country.
“Maria Cristina is lax in the principles of morality, which ought to
be the foundation of the education of Princes, and she knew not how
to inculcate them in the mind of Your Majesty. Whilst you were a
child, she did nothing but accumulate money and arrange for her
future booty.
“The disinterestedness and the generous sentiments which
enrich Your Majesty’s heart, and the high tendencies which have
shone in your mind, and which have only been suffocated by the
pettiness of your entourage, are exclusively a gift from Heaven, and
under favourable circumstances they would have developed into
great and glorious deeds. When the time arrived for the marriage of
Your Majesty—an event of such import to your destiny—Your
Majesty knows that the Queen-mother only used her influence to
make you marry a man whose sole merit lay in his power of
ministering to her omnivorous nature. Never did a mother behave in
such a self-interested way in what concerned her daughter’s
domestic happiness! And now she continues the soul of the
Government, counselling Your Majesty for her own ends, and with
utter disregard of the wishes of the people.”
This letter, which gives an idea of the dissensions of the Royal
Family, and the expression of feeling against Maria Cristina, was
shared by the people. Indeed, the hatred of the Queen-mother was
publicly shown after she took refuge in the royal palace. The Plaza
de los Ministros resounded with the cries from the townsfolk of
“Death to Cristina!” A storm of stones broke all the windows of the
palace. The soldiers fired on the people. The palace gate of El
Principe had to be guarded by two cannon commanding the Plaza
de Oriente. Twelve guns were stationed in the great courtyard called
the Plaza de las Armas, and all the cavalry at Madrid was
summoned to the defence of the royal abode; and during the siege
there was serious anxiety that the provisions would not last long.
Queen Isabella sought to encourage and support her mother, but
she saw that the stream of public hatred was now too strong to be
stemmed.
The arrival of Espartero in Madrid, on July 29, raised the siege of
the palace, and the people, delighted at the sight of their favourite
leader, gave a loyal ovation to Queen Isabella when she appeared at
a window of the palace.
The days from July 17 to August 28 were fraught with anxiety for
the Queen of Spain. The cries for the dismissal of the Queen-mother,
and for her trial for the appropriation of State moneys, could no
longer be silenced, and the day came when the royal lady found that
her personal safety demanded her departure from the country. So,
accompanied by a mounted escort, Maria Cristina submitted to the
decision of Espartero, as the mouthpiece of the people, and she
finally bade farewell to her weeping daughter at the palace door, and
left the country, never more to return.
Espartero made a crusade against the undue priestly influence at
Court. The weak-minded King was quite under the power of “the
bleeding nun,” as Patrocinio was called, and his constant visits to her
apartments in the palace were said to have been in search of
spiritual counsel, with which she was supposed to be miraculously
endowed by reason of the wounds in her forehead and hands, which
refused to be healed, as they were said to be illustrative of those of
the Saviour. The Queen and all the Royal Family became
hysterically hypnotized by this phenomenon.
But Espartero soon put an end to the matter by having the lady
put under the authoritative care of a doctor, who had her hands tied
so as to prevent her irritating the wounds; and thus in a short time
the supposed miracle was over, and the power of the religieuse and
her brother, the Archbishop Claret, was at an end.
Espartero had O’Donnell as his Minister of War. Dissensions
broke out again in the Cabinet, and O’Donnell reaped the success of
his camarilla influence at the midnight Council meeting held before
the Queen in July, 1856. For when Espartero found that his
measures for the new Constitution were rejected, he offered his
resignation; and then, to his surprise, the Queen, by a prearranged
concert, turned to his colleague with her sweetest smile, saying, “I
am sure you won’t abandon me, will you?” and he was sworn in as
Prime Minister the following day.
But O’Donnell had a powerful rival for favour at the palace in the
person of Narvaez, a General of some fame, whose alert, dapper
little figure, said to have been improved by corsets, made him
popular at Court as a dancer.
This officer was extremely arrogant, and noting that the
grandees, by right of their special prerogative, stood covered in the
royal presence during the ceremony of the King washing the feet of
the poor, and feeding them in the historical Hall of Columns, he
promptly put his own cocked hat on his head, and bade his officers
do the same.
O’Donnell, who was of a heavier, clumsier build than his rival,
suffered much at the sight of the success of Narvaez in the arts of
society. One day at a state ball at the palace the two Generals stood
in readiness to conduct the Queen through the mazes of the rigodon.
As Prime Minister, O’Donnell considered that the distinction of taking
Isabella’s hand for the figures was his by right, but Isabella could not
resist the temptation of having for a partner a man distinguished as a
follower of Terpsichore, and she therefore singled out Narvaez as
her partner.
In a fury at what he considered a public slight, O’Donnell gave in
his resignation the next day as President of the Council, and General
Narvaez was chosen to fill the vacant place.
It was well known at Court that the British Ambassador, Bulwer
Lytton, was working against the Court of Spain in England, and
consequently he was an object of great aversion to the military
leader of the Government.
Irritated at the Englishman’s assumption of authority, Narvaez
said one day to Bulwer Lytton that Spain did not interfere with the
affairs of Queen Victoria like England did with those of Isabella II. To
this remark the British diplomat returned that Victoria did not owe her
throne to foreign intervention, as Isabella did.
One day Narvaez was in his bureau in a great state of irritation
about some action of the British Ambassador, when Bulwer Lytton
was announced. He drew a chair close to Narvaez, and, although
the Spaniard pushed his back, drew his seat still closer. Upon this
Narvaez jumped up in his excitable manner, and then, wishing to
seat himself again, he missed the place and found himself lower
than he wished.
Upon this the Ambassador made some remark which added fuel
to the fire of the General’s wrath, and, advancing to the Englishman,
he made him rise from his seat, took him by the neck, and kicked
him so that he nearly fell to the ground. The Ambassador took his
papers for England that day, and this incident doubtless added to the
bitterness with which Bulwer reported on the affairs of Spain.
 The incident just related, of this last interview of Sir Bulwer Lytton
with the Spanish Premier, was evidently never reported in all its
bearings, but enough was known for it to be seen that the
Ambassador was apt to embroil matters. For in “The Letters of
Queen Victoria,” vol. ii., p. 207, Her Majesty writes:

“May 23, 1848.

“The sending away of Sir H. Bulwer[17] is a serious affair, which

will add to our many embarrassments. The Queen, however, is not
surprised at it, from the tenor of the last accounts of Madrid, and
from the fact that Sir H. Bulwer has, for the last three years, been
sporting with political intrigues. He invariably boasted of being in the
confidence of every conspiracy, though he was taking care not to be
personally mixed up in them; and, after their various failures,
generally harboured the chief actors in his house under the plea of
humanity. At every crisis he gave us to understand that he had to
choose between a revolution and a palace intrigue, and not long ago
he wrote to Lord Palmerston that if the Monarchy with the
Montpensier succession was inconvenient to us, he could get up a
Republic.”

[17] “Lord Palmerston had written a letter to Bulwer (which the

latter showed to the Spanish Premier) lecturing the Spanish Queen
on her choice of a Minister. This assumption of superiority, as Sir
Robert Peel calls it, led to a peremptory order to leave Spain in
twenty-four hours.—Editor.”

But Isabella’s realm was still torn by insurrections. In January,

1860, the Prefect of the Police reported that a rebellion was being
prepared in Spain against the throne by the Carlist party, under Don
Carlos Luis de Bourbon y de Braganza, Count of Montemolin. When
justice was prepared to take its course against the insurrectionists,
Don Carlos wrote to Isabella, saying:
“I am certain that your compassionate heart, which has always
shown pity for the unfortunate, will not fail to have mercy on your
cousins, and not deny the pardon that we crave.”
This mercy was also eloquently pleaded for by the unhappy
mother of the delinquents. So, obedient to the impulse of her kind
heart, Isabella said to the weeping parent: “Be at rest; your son shall
not die.”
However, the Carlist family soon forgot the clemency of the
Queen, and the letter of Juan de Bourbon, son of Don Carlos,
Ferdinand’s brother, showed that the spirit of animosity burnt as
powerfully as ever in the breast of the claimant to the throne.
“Twenty-seven years you have reigned,” ran the Prince’s letter to
his royal cousin, “and you must confess that the hand of God has not
helped you. I know the country; I know equally well that your heart is
good, and that you do good when you can, and you regret the evils
which afflict Spain. But you try in vain. You cannot fight against
Providence, which never wills that evil should prosper. Be assured,
dear cousin, that God did not choose you to make the happiness of
Spain, and that Divine Providence has denied you the lot of being a
great Queen. Descend, Isabella—descend from the throne! Show
yourself great in this matter, and take the place to which you have a
claim in my family as my dear cousin, and as having occupied the
throne for so many years, and do not expose yourself to final
disaster and bring ruin on the family.”
 CHAPTER XII
COURT INTRIGUES

1864–1868

On November 28, 1857, “the birth of Alfonso XII.,” as Martin Hume

says, “added another thong to the whip which the King-Consort
could hold over the Queen for his personal and political ends, and it
also had the apparently incongruous effect of sending Captain Puig
Moltó into exile.”
Of course there were the usual rejoicings at the birth of a Prince,
but things were far from satisfactory at the Court. The Queen had
now a taste of personal power and a higher notion of her own
political ability. The Congress was in slavish servitude to the palace,
and, acting in accordance with this sentiment, it had managed to get
rid of the men in the Senate who had been working for the
constitutional privileges of the country which would have led to the
indispensable protection of the prerogative of a true suffrage; and
freed from these patriots, the press was silenced and Parliament
was suspended.
The return of Maria Cristina, the Queen’s mother, was another
step which added to the unpopularity of Isabella II. Once more
wearied out with waiting for the realization of constitutional rights, the
people’s exasperation was voiced by the soldiers at the barracks of
San Gil, within view of the royal palace of Madrid. O’Donnell at once
took steps for the suppression of the insurrection.
 The cries of “Viva Prim!” “Viva la Libertad!” showed that the spirit
of republicanism was rampant.
Swiftly as O’Donnell went to the scene of action, Narvaez was
before him, and so the Prime Minister had the mortification of seeing
his rival carried into the palace to be tended for the slight wound he
had received in the conflict.
The rebellion was soon quelled, and the insurgents were shot;
but disinterested advisers of the Queen might have shown her that
such émeutes proved that the fire of discontent was smouldering,
and with a strong Government for the constitutional rights for which
the country was clamouring the revolution of 1868 would have been
avoided.
On the day following the San Gil insurrection a man of influence
at the Court went to plead pardon for two of the insurgents from Her
Majesty herself.
The interview was characteristic of the kind-heartedness of the
Queen.
After waiting for half an hour in the antechamber, the gentleman
was shown into the royal presence.
“You have been quite lost,” said Isabel graciously, as her visitor
bent over her hand. “It is a thousand years since you have been to
see me.”
Whilst excusing himself with courtly grace, Tarfe noticed that
during the two years in which he had been absent from the palace
the Queen had grown much stouter, and had thus lost some of her
queenly dignity. She seemed distrait and troubled, and the red lids of
her limpid blue eyes gave her an expression of weariness. They
were, moreover, the eyes of a woman who had been brought in
contact with the encyclopædic array of the various forms of the
despoilers of innocence.
 The petitioner submitted his plea for mercy for his friends by
saying that his request was backed by a letter from the holy Mother,
begging her to write two letters to General Hoyos for their release. To
the delight of the intercessor, the Sovereign at once wrote the letters.
When this was done, the surprise of the courtier was increased when
the Queen, who was generally mañanista, said in a quick, nervous
tone: “Do not delay giving these letters; do not wait till to-morrow; do
it to-day!”
Before leaving the royal presence, Tarfe ventured to say that
O’Donnell was much upset by the events of the preceding day, and
the Queen replied in a tone curiously devoid of feeling: “Yes, I like
O’Donnell very much.” This she said three times in the same
passionless voice, and then, seeing that he was dismissed, Tarfe
took leave of Her Majesty; and after fulfilling the mission to Hoyos,
he went to see O’Donnell at his palace of Buenavista.
The General declined to believe the reports of his friends, of the
intrigues which were to compass his fall.
The victor at Tetuan was more able to repel the open advance of
an enemy than the underhand plots of a palace.
But when Ortiz de Pinedo suddenly came in, and said, “Gonzalez
Brabo has left San Juan de Luz to-day, and he is coming to form a
Ministry with Narvaez,” the General was somewhat taken aback.
On the following morning, after finishing a long despatch for the
royal signature, he repaired to the palace, and, anxious to know the
real state of affairs, he submitted to Her Majesty the list of
appointments to the Senate-house, many of which had been
suggested by Isabel herself.
To the surprise of the Minister, the list was rejected by the Queen
in a cold, disdainful way, so O’Donnell found himself forced to offer
his resignation. This was accepted with the usual meaningless
smiles and compliments.
Then O’Donnell returned to his house, where his friends were
waiting for him. His face betrayed his rage and mortification, and,
throwing his gloves on the table with an angry gesture, he
exclaimed:
“I have been dismissed just as you would dismiss one of your
servants.”
“My General,” exclaimed one of the partisans of the ex-Minister,
“the camarilla delayed the change of Ministry for two days after the
mutiny; why was that? And Ayala returned because it was better for
Narvaez that we should have the odium of shooting the insurgents.
Now he can take his place in Parliament with all the airs of
clemency.”
O’Donnell, who could not deny the truth of this remark, took
General Serrano by the arm into another room, but they could plainly
hear their indignant followers saying: “Eso, señora, es imposible!”
The Marquis of Miraflores says that a General Pierrad, the head
of the Pronunciamento, told a chief of the halberdiers that he had
better tell the Queen that there were no means of putting down
meetings, and this for two reasons: Prim and his friends only wanted
a change in the power by a disciplined Pronunciamento, but the
artillery, through some strange influence, would not recognize
military chiefs. He who said this was to have been shot down by
them; he saw them drunk and faithless to their commands. This
communication was made to the Queen. In 1867 an important
interview took place in the Palace of Madrid between Isabel II. and
her sister, the Duchess of Montpensier.
It will be remembered that, after the adventures of the royal
couple in the revolution of 1848, the Duke and Duchess retired to
Seville, where they lived in the Palace of San Telmo with all the state
dignity of sovereigns. The Queen had made the Duke an Infante of
Spain, and he had also been appointed Captain-General.
The Duke decided to take his wife to Madrid to counsel her sister
to adopt a more liberal policy. The Duchess was expecting another
child, but she was advised not to postpone her visit to the royal
palace of Madrid. The interview was far from satisfactory, for Isabella
had no intention of allowing Montpensier to have an active part in the
Government. So the Princess returned to Seville, and Isabella
afterwards wrote her a letter, in which she expressed displeasure at
her aims. This letter received an angry reply, first from the husband,
and then from the wife. So a coldness grew up between the sisters,
and, indeed, Isabella’s want of confidence in Montpensier was
proved by the subsequent events in 1868, when Prim himself
rejected the Duke’s offer to raise forces in his favour.
During all this time the little Prince of Asturias, who was nine
years old when the insurrection broke out in the barracks of San Gil
for Prim, was pursuing his education in the palace. The style of the
Prince’s education is given in the remark of the royal child’s playmate
to his father, when he had been to spend a day at the palace.
“Papa,” said the boy, “Alfonso does not know anything. He is
taught nothing but religion and drilling. After the religious lesson,
which was very dull,” the child continued, “Alfonso was given a spear
and a sword, and he waved them about so much that Juanito and I
were afraid he would hurt us.”
A record was kept of the little Prince’s doings during the day. His
frequent colds, his coughs, his acts of devotion, his appetite at
meals, his games, his toys, his little tempers, his deeds of
obedience, were all entered in the register as signs of his
temperament and as indications of his future character as a man.
 The Prince’s apartments were dreary. The windows were high up
in the thick walls, the ceilings were low, and, as a grandee says
when speaking of this fact, it seemed strange that the light and air so
essential for a child should be insufficiently supplied to a future King.
General Pavia, who was gentleman-in-waiting to Alfonso, only
shrugged his shoulders at this remark, but Señor Morphy ventured to
say: “That is our opinion, but she who commands, commands.”
When the grandee was introduced to the little Prince, he returned
the salutation with the manner of one accustomed to it, but with a
pretty smile which was very attractive.
“Yes,” said his attendant, “His Royal Highness is better to-day. He
only has a little cough now, but the doctor says he is not to be tired
with lessons to-day; he is only to rest.”
“Last night,” said the General, “His Highness asked for his lead
soldiers to play with in bed. He did not want to say his prayers. So I
had to fetch the new prayer-book which Her Majesty sent a few days
ago, and I read the prayers whilst he repeated them after me. So in
this way he said his prayers, but not willingly.”
Hereupon Alfonso protested, saying: “But this morning, Marquis, I
said my prayers without your reading anything.”
“Yes, yes,” returned the gentleman; “but Your Highness did not
want to get up, so I had to read stories to you until the doctor came.”
A few pages from the diary of the young Prince of Asturias gives
some insight into the dreary daily life of the delicate child:
“October 1, 1866.—His Highness breakfasted at 11 o’clock. At 1
o’clock he had drilling till 1.40. At 2 o’clock a writing lesson with
Señor Castilla; at 3 o’clock religion with Señor Fernandez; 4.30, rice
soup as usual; 4.50 he went up to the rooms of Her Majesty to go for
a drive with her.
 “October 4.—His Highness played about till 2.15. He had no
lessons to-day, as being Her Majesty’s saint’s day. At 2.43 he went
up to the Queen’s apartments to assist at the reception. He wore the
uniform of a sergeant, with the Cross of Pelayo. The ceremony over
at 6.15, when His Highness came down with Señor Novaliches, as a
boot hurt him (not the Marquis, but His Highness). The said Marquis
took off the boot, and carefully examined the foot, but he found
nothing to account for the pain. Mention is made of this circumstance
as the Chief of the Chamber of His Highness thinks it fitting to do
so....
“October 6.—My Lord Prince lunched at 12 o’clock. I gave him
his lessons. He went to the Church of Our Lady of Atocha. He went
to bed at 10 o’clock, and slept ten hours. He took some chocolate,
made his confession at 9.30, and Father Fernandez celebrated
Mass.
“October 9.—He breakfasted with appetite. He had his lessons at
the marked hours, and he was somewhat restless. At 4 o’clock he
took some soup, and went out for a walk with the Mayordomo, Señor
Marquis de Novaliches, Professor Sanchez, and Juanito. He had
supper at 8 o’clock, and played till 10 o’clock with Juanito, but left off
when he knocked his left leg against a table. He slept from 10
o’clock till 9 o’clock in the morning. He got up at 9.30 without feeling
any pain in his leg from the blow. He did his orisons, assisted at the
Mass in his room; he went out for a walk with his Mayordomo,
returned at 11 o’clock, and assisted at the Mass with Their Majesties
and the Princesses; and at 11.45 he had his hair cut.”
As Perez Galdos says in his works, the long hours of religious
instruction every day would have qualified the little Prince for the
Council of Trent. When any Bishops came to visit Isabella, they were
sent to the apartments of her little son; and thus Morphy writes in the
register: “I gave the lesson to His Highness in the presence of the
Bishops of Avila, Guadix, Taragona, and of other dioceses whose
names I do not remember.” And Losa wrote: “He opened his eyes at
8.30; he dressed and gave thanks to God; he took his chocolate with
appetite, and at 10 o’clock had his religion lesson in the presence of
the Cardinal of Burgos, who was pleased with his progress, and
noted that His Highness was ‘magnificent in everything.’”
Courtiers who were true of heart saw with apprehension the
artificial character of the Prince’s education.
“Ah!” said a man who would gladly have been frank with the
Queen, but he felt he was powerless against her crowd of flatterers,
“Alfonso is a very intelligent child. He has qualities of heart and mind
which would give us a King worthy of the people, were they only
properly cultivated; but we shall never see this ideal realized,
because he is being brought up like an idiot. Instead of educating the
boy, they are stultifying him; instead of opening his eyes to science,
life, and nature, they blind them so that his sensitive soul remains in
darkness and ignorance.”
The same courtier implored the Prince’s educators to give the lad
a chance. “Take him out of this atmosphere of priests and nuns, and
devotional books by Father Claret. If you want Alfonso to be a great
King, let him breathe the pure air of fine deeds. Take him away from
the gloomy atmosphere of the royal palace; let him inhale the fresh
breezes of liberty. His talents will develop, and he will become a
different boy.”
It was indeed true the little Prince was in an unnatural
atmosphere in the palace, where the tunic of the nun Patrocinio had
become an object of worship, and where the King, in his stuffy
apartments, gave himself over to the study of relics which were
brought to him at a high price by the priestly folk, who made harvest
out of his credibility.
The situation of Queen Isabella is graphically given by the
historian Galdos in the reflections of a loyal courtier whilst having,
with his wife, an audience of Isabella II.:
“Oh, your poor Majesty!” he said to himself. “The etiquette
invented by the set-up gentlemen of the Court to shut you off from
the national sentiment prevents me telling you the truth, because it
would hurt you to hear it. Even those on the most intimate terms with
you shut you out from the truth, and they come to you full of lies. So,
kind-hearted Isabella, you receive the homage of my gilded untruths.
All that I have said to you this afternoon is an offering of floral
decorations, the only ones received on royal altars.... You, who are
more inclined to the ordinary and the plebeian than other Kings—you
let the truth come to you in external decorative, and verbal matters,
but in things of public consequence you like nothing but lies,
because you are educated in it, and falsity is the religious cloak, or
rather the transparent veil, which you like to throw over your political
and non-political errors. Oh, poor neglected, ill-fated Queen...!”
The reflections of the courtier were here interrupted by Isabella
saying to his wife: “Maria Ignacia, I want to give you the ribbon of
Maria Luisa.... I shall never forgive myself for not having done it
before. I have been very neglectful—eh?”
The Marchioness was eloquent in her thanks, and Beramendi
could only say: “Señora, the kindness of Your Majesty is
unbounded.... How can we express our gratitude to Your Majesty?”
But the Marquis said to himself: “We take it, because even as you
accept our lying homage, so we receive these signs of vanity. King
and people we deceive each other; we give you painted rags of
flattery, which look like flowers, and you bestow honours on us which
take the place of real affection.”
Isabella continued: “I must give you a title of Count or Viscount,
which your son can take when he comes of age.”
 The Marquis’s wife returned: “Our Queen is always so good; that
is why the Spaniards love her so.”
“Ah, no, no!” exclaimed Isabella in a melancholy tone, “they do
not love me as they did.... And many really hate me, and yet God
knows I have not changed in my love for the Spaniards.... But things
have got all wrong.... I don’t know how it is ... it is through the heated
passions of one and the other. But, Beramendi, it is not my fault.”
“No, indeed,” returned the courtier; “you have not caused this
embroiled state of affairs. It is the work of the statesmen, who are
moved by ambition and egoism.”
This indeed was true, for even as Serrano used the Queen’s
favour to his own ends, and had his debts twice paid by Her Majesty,
he was the first to lead the country against her.
“Do you think that matters will improve, and that passions will
calm down?” asked Isabella anxiously.
“Oh, señora, I hope that the Government will confirm your
authority, and that those that are in rebellion will recognize their
error.”
“That is what they all say,” said Isabella, with a little satirical
smile. “We shall see how things will turn out. I trust in God, and I
don’t believe He will forsake me.”
“Ah!” said Beramendi to himself, whilst his royal mistress
continued in the same strain of religious trust to his wife, “do not
invoke the true God whilst you prostrate yourself before the false
one. This god of thine is an idol made of superstition, and decked in
the trappings of flattery; he will not come to your aid, because he is
not God. I pity you, blind, generous, misled Sovereign.... Those who
loved you so much now merely pity you.... You have been silly
enough to turn the love of the Spaniards to commiseration, if not to
hatred. I see your goodness, your affection, but these gifts are not
sufficient to rule a nation. The Spanish people have got tired of
looking for the fruit of your good heart.”
When Isabella gave the sign of dismissal of the courtier and his
wife by rising to her feet, he said to himself sadly:
“Good-bye, Queen Isabella; you have spoilt your life. Your reign
began with the smiles of all the good fairies, but you have changed
them into devils, which drag you to perdition.... As your ears are
never allowed to hear the truth, I cannot tell you that you will reign
until O’Donnell will permit the Generals to second Prim’s plans. Oh,
poor Queen! you would think me mad if I said such a thing to you;
you would think I was a rebel and a personal enemy, and you would
run in terror to consult with your devilish nuns and the odious set
which has raised a high wall between Isabella II. and the love of
Spain. Good-bye, lady of the sad destiny; may God save your
descendants, as He cannot save you!”
The good-heartedness of the Queen was, indeed, seen by all
about her, and there are people still at the Palace of Madrid who
remember seeing Her Majesty take off her bracelets and give them
to the beggars which infest the royal courtyard. All the best impulses
of Isabella were turned to her own ruin for the want of true patriots,
who by supporting the constitutional rights of the nation would have
secured the sovereignty to the Queen. The self-interested conduct of
the generals and statesmen, whose command in the camarilla of the
palace meant rule over the heart of Her Majesty, tended naturally
only to the overthrow of personal rivals, and to the neglect of the
welfare of the land.
Prim therefore became the hope of the nation. With his return to
the capital, thought the people, crushed down by taxation and
deprived of constitutional liberty, there will be an end to the camarilla,
Narvaez, and Patrocinio, and we shall have the pure fresh air of
disinterested policy.
 The death of O’Donnell at Biarritz relieved Narvaez of the fear of
his rival’s return, but the General had the mortification of seeing his
royal mistress utterly in the hands of Marfori, who had been raised
from the position of Intendente of the Palace to the position of
supreme personal favour.
When the Queen heard of O’Donnell’s death, she is reported to
have said: “He determined not to be Minister with me again, and now
he can never be.”
The Queen now committed the suicidal act of making Gonzalez
Brabo Prime Minister in the place of Narvaez. The poor lady seemed
quite to have lost her head, and there was no one to put her on the
right path, surrounded as she was with harpies.
According to a letter from Pius IX., found in the Princess’s prayer-
book in the royal palace after the Queen had taken flight, the Pope
counselled the marriage of the Infanta Isabella with a Neapolitan
Prince. Even whilst the fêtes of the marriage were going on,
Gonzalez Brabo was concerting with the revolutionary Generals, and
the name of “Prim and Liberty!” was heard on all sides, and
messengers were sent to consult with the leader of the Republican
party in London.
The supporters of the Montpensier party hoped that the
dethronement of Isabella would mean the acceptance of the
Duchess of Montpensier as Queen, and her husband as Prince-
Consort. But this idea was soon nipped by Monsieur de Persigny, the
President of the Privy Council of the Emperor of the French, saying
to Olozaga, who was then Spanish Ambassador at Paris, that he
would never consent to the crown of Spain being on the head of
either the Duke or the Duchess of Montpensier.
After the historic day of September 29, 1868, when Prim made
his successful coup at Cadiz, the Royal Family fled to San
Sebastian.
 The haste with which the flight was made could be seen in the
collections of jewels and money which had been thrust into bags
which were after all left behind.
In the Hôtel d’Angleterre of the seaside resort Isabella still
seemed to expect a miracle to take place in her favour. A throne
does not fall every day, and a crowd hovered about the hotel to see
how the Queen would accept her overthrow.
A murmur of satisfaction broke out among the bystanders when
the loyal-hearted Marquis de Beramendi was seen entering the
hotel. “That is a good thing,” they said, “for Isabella will listen to his
advice, which is certain to be wise.”
The courtier’s remarks to the Lady-in-Waiting were short and to
the point.
“I have come to tell you,” he said, “that, if the Queen keeps to the
good idea of abdicating, certain infatuated people ought to be kept
from opposing it. I have had direct news from Serrano, and he says
that, if Doña Isabella will abdicate in favour of Don Alfonso, he will
save the dynasty, and she herself will be saved. The Duke of Torres
will not put obstacles in the way of this course.”
“Better than that,” returned the Lady-in-Waiting, in a voice which
a cold rendered almost inaudible, “I thought that Her Majesty had the
same idea, ‘that she had better go to Logroño, and abdicate in
favour of the Prince of Asturias in the presence of Espartero.’”
“That’s admirable!” said Beramendi.
“And then, after abdicating, the Queen will depart immediately for
France, leaving the new King in the power of the Regent Espartero.”
“Admirable! splendid!” cried Beramendi; “but there is not a minute
to lose.”
“The departure will be arranged this evening.”
 “But, my God, I fear delays will be fatal; I am afraid that some bad
friend, some plotting courtier of the camarilla, will spoil this saving
step——”
“Well, I must go upstairs now,” returned the lady. “The Señora,
Don Francisco, and Roncali, are busy with manifestoes for the
nation.”
“And Spain will say, ‘Manifestoes to me!’ Now is the time to show
the country fine deeds, and not empty rhetoric.”
On the following morning, when Beramendi went to the hotel, he
came upon Marfori; and although he had had little to do with this
nephew of Narvaez since royal favouritism had raised him to such
undue importance, he said, in a tone of assumed respect: “So Her
Majesty is going direct to France? Something was said about her
travelling to Logroño?”
Upon this Marfori frowned angrily, saying: “You don’t understand,
my dear Marquis, that it would be very humiliating for the Queen of
Spain to ask protection from a General, although he bear the name
of Espartero. All concert with Progressists is dangerous. The Queen
is leaving Spain under the conviction that she will soon be recalled
by her people.”
“I knew it was useless to say more. Don Carlos Marfori was busy
giving orders to the servants. I regarded him with resentment,
because he was the personification of the evil influence which
brought the Queen to her ruin.
“His Arab type of handsomeness, with his large mouth and heavy
jaw, was eloquent of sensuality, and his obesity robbed him of the
attraction which he had possessed in earlier days. He was
impetuous, overbearing, and wanting in the courtesy common to a
superior education.”
 The Marquis was then taken into the presence of the Queen, and
as he bent over her hand she whispered: “You know we have given
up the idea of going to Logroño. No more humiliations! I am going
away so as not to aggravate matters, and to prevent bloodshed; but I
shall be recalled, shall I not?”
“I had to console Her Majesty with one of the usual Court lies,
and the Royal Family soon took its departure, the Queen leaning on
the arm of Don Francisco, the little Infantas with their Ladies-in-
Waiting, and the Prince of Asturias, in a blue velvet suit, led by
Señora de Tacon. The poor little fellow looked pale and sad; his
great eyes seemed to express the royal and domestic sadness of the
scene, and nothing was now wanting but the order for departure.”
Marfori was always much disliked by people at Court. It was in
the summer of 1867. Many courtiers and ladies of high rank were
promenading in the beautiful gardens of La Granja. The soft, well-
kept turf of the shady alleys by the countless sparkling fountains set
off the beauty of the dresses, when, with his usual courtly grace,
General Narvaez advanced to meet the Countess of Campo Alange.
This illustrious lady, whose salons in Madrid were graced by the
highest in the land, was soon to give a ball.
“I have received your invitation,” said the General, after he had
greeted the Countess.
“It is almost the first that I have sent,” returned the lady.
“I have just met Marfori,” said the Duke of Valencia, “and he tells
me he has not received his.”
“Neither will he,” replied the lady sharply.
“And why, being a Minister?” queried the General in surprise,
knowing how the slight to the Queen’s favourite would be resented at
Court.
 “Simply because Cabinet Councils are not held at my house,”
returned the lady caustically, firm in her decision to show her dislike
of the man.
General Narvaez, whose dapper figure and perfect dancing made
him always a welcome guest at the Spanish Court, was still
unmarried when he had to withdraw to Paris as an exile. He had
always been fond of feminine society, but, gay butterfly as he was,
he did not fix his affections upon any one lady.
The beautiful Leocadia Zamora had been once the object of the
officer’s attention, and, indeed, the charming way she accompanied
herself on the harp fascinated other admirers beside the Count of
Valencia. She was a constant visitor in the salons of the Countess of
Montijo, where the lovely Eugénie shone with the brilliance and
charm which were so soon to be transported to the Court of France.
But fate did not reserve the joy of a happy marriage for the lovely
Leocadia, and the sweet spirit, disillusioned by an unhappy love,
retired to a convent in Oviedo, where she passed the rest of her life
performing the duties of a Lady Abbess.
It was said that it was the gallant Don Salvador de Castro who
had taken Leocadia’s heart captive, when she was young; and,
indeed, it is not surprising if this report be true, for he was a typical
courtier of his time, and when he was home from his duties as
Ambassador in Italy he seemed to dwarf all the attractions of the
lady’s other admirers. Leocadia was, in truth, a star of the Court of
Spain, and the beautiful picture by Frederick Madrazo shows the
perfection of her charms, with no other ornament than a white rose
to adorn her simple white dress. Salvador de Castro was honoured
by the friendship of King Francis II. and Queen Maria Sophia when
the Italian Revolution robbed them of the throne of the Two Sicilies,
and he was able to render them marked services and prove himself
as loyal a friend as he was perfect a gentleman. After the
capitulation of Gaeta, the King and Queen rewarded his loyalty by
granting him the title of Prince of Santa Lucia, with the gift of the
beautiful palace on the banks of the Tiber which is known by the
name of the Farnesina, whilst the gardens were sold to the Emperor
Napoleon. The place was deserted, and so near to its ruin that
sheep and goats fed in its grounds, and the custodian took his meals
in the beautiful hall of the frescoes of Sodon.
It was in this palace that Michael Angelo painted a head on the
wall, which is known by the name of “The Visiting Card,” as he left it
as a sign of his call on Raphael when the artist was out.
The Prince of Santa Lucia had the palatial dwelling restored, and
he gave magnificent entertainments in this palace, of which it was
not destined that the lovely Leocadia should be mistress. Indeed, the
lady abandoned all thoughts of love and pomp when she entered a
convent in Oviedo, where she ended her days as Lady Abbess;
whilst the daughter of her old admirer wedded the Marquis of Bey,
and made a mark in Court society of Madrid.
But to return to the gallant little General. His affections were at
last taken captive by another friend of the young Empress of the
French, the beautiful daughter of the Count of Tacher. The Empress
Josephine had belonged to this family, and her parents, the Duke
and Duchess de Tacher de la Pogerie, were much beloved by Queen
Marie Amélie, wife of King Louis Philippe.
It was General de Cordova, who had played such an important
part during the Regency of Queen Maria Cristina, who first took him
to the house of the Tachers. When Narvaez paid a second visit to the
palace on the Boulevard Courcelles, he found that nobody was at
home; and he was waiting in the drawing-room for the return of the
lady of the house, when the daughter came in, looking beautiful in a
white dress, but with her face tied up.
“Are you ill?” asked the General, with concern.