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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
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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.

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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
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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
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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
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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
4 Biology of Oysters

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

Hyote spines Hollow, tubular, and cylindrical shell outgrowths arising at the shell margin
Labial palps Ciliated flaps which form lips at the mouth and function in feeding
Ligament (Fig. P1.1): This refers to the shape of the ligament, which is triangular and arched, with the resilifer of the right valve
Alivincular-arcuate elevated and the attachment area of the lateral ligament impressed; the ligament of the left valve is a mirror
image of the right valve
Pallial line Impression left on the internal surface of the shell by the insertion of muscles of the mantle margin (cp the
“scar” left by the insertion of the adductor muscle)
Promyal chamber A space between the visceral mass and the mantle facilitating water flow from the gills to the exhalent
cavity
Resilium The central part of the ligament, located in a special groove of the shell (the resilifer)
Shell (Fig. P1.2): Calcite and aragonite are different forms of calcium carbonate. Oyster shells are predominantly calcitic, in
Calcite/Aragonite contrast to the primitive, aragonitic, condition in the Bivalvia. The calcite is of two types which differ ultra-
structurally (see Carriker, 1996), prismatic, and foliated; the latter is typical of the oysters and forms the bulk
of the shell, where it also contributes to the “structural chambers” commonly found in older individuals. In
oysters aragonite is limited to the attachment areas of the adductor muscle (the myostracum) and the lig-
ament (ligostracum)
Shell plicae Folds of shell that extend posteriorly from the bourrelets, especially evident in young individuals of
crassostreinids

The following table (Hu, Lutz, & Vrijenhoek, 1992) distinguishes between the larvae of Crassostrea and Ostrea (Fig. P1.3):

Crassostrea Ostrea
General morphology Knobby or beak-shaped umbo Round shell with large, moderately prominent
directed umbo directed dorsally; L > H
posteriorly; shell skews backward;
generally H > L
Shell:
Prodissoconch I length 65–88 μm 110–192 μm
Prodissoconch II long. axis Rotated 30 degrees Rotated <20 degrees
Provinculum:
Length 50–71 μm 70–100 μm
No. of teeth Two on each side of provinculum One anterior and one posterior on left valve, two on right
Tooth shape Rectangular Square or triangular
Central apparatus Well defined Partially developed
Obscured teeth Posterior Anterior

Fam. Ostreidae
Subfam. Crassostreinae
Tribe Striostreini
Genus Saccostrea
85
Fam. Ostreidae
92 Subfam. Crassostreinae
Tribe Crassostreini
Genus Crassostrea
Fam. Ostreidae Fam. Ostreidae
Subfam. Lophinae Subfam. Ostreinae

Fam. Gryphaedae
Subfam. Pycnodonteinae

FIG. P1.1 A phylogenetic tree representing relationships among living oysters, based on the morphological characters listed above (see Harry,
1985); the numbers are “bootstrap” percentages that indicate the levels of statistical support that apply to the structure. At the family level,
Ostreidae and Gryphaedae are sister groups. (From Littlewood, D. (1994). Molecular phylogenetics of cupped Oysters based on partial 28S rRNA
gene sequences. Molecular Phylogenetics and Evolution, 3(3), 221–229).
Another random document with
no related content on Scribd:
So, when the hatter reached the house of his friend, he found him in
great perplexity over this matter, for each of those to whom the
Westland children had been assigned had some special reason for
asking to be excused the service; and when he saw Drayton, he
made up his mind that he had come to him on a similar errand.

"I know what thou past come to say to me, friend, for thou art not the
first visitor I have had concerning this business. Of course, Dame
Drayton is fearful for her own children, and hath sent thee to say she
cannot take these, though—"

"Nay, nay; the word of the Lord to my wife is, that these little ones
should not be separated the one from the other, and she desires me
to say to thee that she would prefer to have them all, an it so please
thee."

"She will take all these children!" exclaimed the Quaker in a tone of
astonishment.

"Even so, friend; for she deems it but adding to their burden of
sorrow at this time to be parted the one from the other."

"And what sayest thou to this?" asked the other, looking keenly at
the hatter; for he was not a wealthy man, but had to work hard for
the maintenance of his family, and to add thus to his burden was no
light matter.

"I can but follow the word of the Lord in me, and that is that I take
these little ones until their parents can claim them at my hand."

"Be it so, then; and the Lord bless thee in thy work, for thou hast
lifted a heavy burden of care from my mind anent this matter. I have
chosen a discreet messenger to bring them from their home, lest one
of us being known should draw the attention of the authorities to
what we were doing, and that might end in our being lodged in gaol
with our brother Westland."
"But how shall I know this messenger?" asked the hatter. "I can go at
once to Triggs' Stairs and meet him."

"Nay, it is a woman who hath chosen this difficult service; and if thou
art in doubt concerning who it is, by reason of other passengers
being near, ask her the way to the Dyers' Garden; for by that signal
was she to know to whom she might deliver the children."

"I will not fail thee," said the hatter. "And when I have taken charge of
these little ones, I will bid her come to thee and give a due account
of how she hath sped on her errand."

And, saying this, Master Drayton bade his friend farewell, and went
at once to the waterside, where he feared the messenger would be
waiting for him.
 CHAPTER II.

DAME DRAYTON.

THE Thames in the reign of Charles the Second was the great
highway of traffic for the city of London. There were no steamboats,
it is true, but watermen, duly licensed by the city authorities, and
wearing badges,—much as cabmen do at the present time,—were
always ready with their boats to take passengers wherever they
might want to go; then there were wherries, and splendidly
decorated barges for pleasure parties; so that the river was always a
scene of busy traffic, and especially towards dusk on a summer
evening, for then people would be returning home, or hastening to
embark; so that the time had been well chosen for the coming of the
Westland children, for they were more likely to escape observation
now than earlier in the day.

Triggs' Stairs was a well-known landing-place, not very far from his
own home; and the hatter went by the shortest cuts, through the
busy narrow streets leading to the river, for fear of keeping the
messenger waiting, and thus attracting the attention of watermen
and passengers alike.

But just as Master Drayton reached the top of the landing-stairs a

boat touched the platform below, which the hatter felt sure had
brought those he was seeking. The children were neatly clad, but
there was a sad woe-begone look in their faces, and two of them
seemed to shrink behind the young woman who sat between them.
She too looked anxious, until she caught sight of the hatter, and then
she seemed to gain more confidence, and led the children up the
steps as briskly as their wet and dangerous condition would permit.

"Thee are sent to us by our brother Staples," she said, almost before
the question of identification could be asked.
"Yea, I am here to take charge of the little ones; but thou wilt come
and see my wife, and tell her what is needful to be told," returned
Master Drayton; for he noticed that only a very small bundle had
been brought with them, and this was carried by the elder girl. She
was about thirteen, he judged, and singularly like her father, as he
had seen him a day or two before, when he stood in the court of the
Lord Mayor, and was condemned to lose his ears, and then be
transported as an obstinate schismatic, dangerous to the king and
his authority.

It was not the habit of Quakers to talk in the streets, and so they
walked towards Soper Lane, which was close to the river, without
asking any further questions, for fear of being overheard by some
one passing.

Deborah opened the street door, and received them with a smile of
welcome, as she explained that her mistress was in her own room;
which Master Drayton knew how to interpret, and went himself to tell
her the children had come.

"And none have dared to make them afraid, since the Lord had them
in His keeping," said his wife with a pleasant smile; and she
hastened to the keeping-room to welcome these strangers to their
new home.

"My own little girls, who are to be your sisters, you know, were
obliged to go to bed, they were so sleepy, but you will see them in
the morning;" and as she spoke she kissed each of the shy,
frightened little strangers, putting an arm around each, while she
spoke to the Friend who had brought them.

"They were hiding in the cellar when I reached the house; for it
seems that our brother hath given great offence to his neighbours by
his plainness of speech when he preached and denounced their
wickedness, and so they had revenged themselves upon him, by
well-nigh stripping his dwelling as soon as he and his wife were
taken to prison. Even the clothes seem to have been stolen, for I
could find none but these," she said, touching the little bundle that
had been placed on the table.

"I think the soldiers took some of the things," said the elder girl at this
point; "but mother had said, 'Thee stay with thy sisters in the cellar,'
just before they dragged her away, and Dorothy was so frightened
when we heard the people running up and down stairs, that I could
not go and see what they were doing."

"That was wise of thee, dear child," said Dame Drayton with a sigh;
for she could not help wondering what would happen to her own
darlings if she and her husband should ever fall into similar trouble.
Sometimes it seemed impossible that they could long escape
suspicion, and then anyone might denounce them who happened to
bear them any ill-will.

The messenger who had brought the children did not stay long, for
the streets of London were no fit place for a woman after dusk, even
though she might be staid and discreet; and so, as soon as the
necessary particulars had been given, Master Drayton put on
another hat and coat, to go with her to the Friend who had
undertaken to manage the affair for the committee of suffering.

While her husband was gone, Dame Drayton took the children to the
little bedroom she had prepared for them near her own, and the
nervous, frightened manner of the two younger girls fully justified
what her fears had been concerning them.

They clung to their elder sister, trembling even at the kind attentions
of their friend, lest she should attempt to tear them from this last
protector.

"Thee will let us sleep together," said the little mother, as she took a
hand of each of her younger sisters, and led them upstairs. "We are
not hungry now, only a little tired with the fright," she explained,
when Dame Drayton would have had supper brought into the
keeping-room for them.

"Certainly ye shall sleep together, and to-morrow I hope we shall

learn to know each other better;" and she shut the children in to
themselves, for she could see that it would be kinder to leave them
now, than to press any attentions upon them, or to ask them any
further questions. Before she went to bed, however, she gently
opened the door and looked in, but found to her relief that they were
sound asleep in each other's arms; and they did not rouse the next
morning until all the house was astir, and the sun peeping in at their
windows.

"This is Bessie Westland, and these are her little sisters, Rose and
Dorothy," said Dame Drayton the next morning, introducing the new-
comers to her own children and the family assembled at the
breakfast table.

One of the apprentices had just raised his horn of small ale to drink,
but at the name of Westland he paused, and looked first at the new-
comers, and then at his companion; for the name of Westland had
been heard of a good deal during the last few days, and the lads
were not likely to forget it.

The hatter noticed the look that passed between the two boys, and it
did not tend to make him feel more comfortable; for although it was
known that he was a strict and godly citizen, the fact of his being a
Quaker he desired to keep secret as far as possible, but he feared
now that the coming of these children might be the means of its
discovery.

Dame Drayton had also noticed the surprised looks in the lads'
faces; but she felt sure they might be trusted not to mention what
they had heard out of the house, for they were steady, quiet, reliable
lads, and their occupation kept them out of touch with many of the
more turbulent of their class. Their parents were steady God-fearing
people; and so Dame Drayton put aside all fear of mischief coming
to them through the apprentices.

The children were naturally shy of each other at first; but by degrees
this slipped off like a garment there was no further need to use, and
the first question Bessie asked was about her mother and father.

"When can I go and see them, Martha Drayton?" she asked.

There was no disrespect in the girl's tone; but she came of a more
stern and uncompromising family of Quakers, and would have
looked upon it almost as a sin to use any title of courtesy, however
much she might revere the individual. Dame Drayton knew all this,
but it came upon her with something like a shock, to be addressed
as "Martha Drayton" by this child, and she paused for a minute
before answering her question.
Then she said, slowly and cautiously, "Dear child, thou hast been
placed in our care by the committee of suffering. They will nathless
see to it that ye see your father in due time; but thou must not run
into needless danger, or bring suspicion upon this household."

"Art thou ashamed of being a Quaker, then, as our enemies call us?"
asked the girl rather severely. "To tremble and quake because of sin
was a mark that we were children of the Highest, my father said, and
should we be ashamed of that?"

"Nay, nay, we should be unworthy of our high calling if we were to

despise the work of the Spirit in our hearts; but dost thou not see,
Bessie, that if we were to prate in the streets of these things, we
should bring trouble and sorrow upon those whom God hath given
us to protect?"

"But the trouble and sorrow would be good for them an it came to
them," said Bessie Westland.

"Even so; but if I could not offer thee and thy sisters a safe abiding-
place now, the trouble and sorrow of thy father and mother would be
increased tenfold."

The girl loved her father very dearly, and would have suffered
anything herself to lessen his affliction, and so this view of the matter
touched her a little; and Dame Drayton took this opportunity of
pressing upon her the need of caution.

"We are not called to raise up to ourselves enemies needlessly. It is

only when some truth is to be held firmly and unflinchingly, that we
may thus brave the law and the mob who alike are against it."

"But my father held that it was the duty of a true friend of sinners to
preach the truth to them at all times, whether they would hear, or
whether they would forbear," said Bessie after a minute or two.

"Then, my dear child, if that was the voice of God to him, he could do
no other than obey it, and God hath honoured him in calling him to
witness to that truth. If the same word came to me, I too must obey;
but the voice of the Spirit in my heart was, that I should shield and
protect thee and thy sisters, and thus comfort the heart of those
called to suffer for His name's sake."

"But—but if thee art a true Friend, would not the word of the Lord be
the same to thee as to my father?" said Bessie after a pause.

"Nay, that is where thee makest so grave a mistake," said Dame

Drayton, sitting down by Bessie's side, and drawing little Rose close
to her. "The Lord hath a word of guidance for each if we will but
listen and obey it, without seeking to follow what He may say to
another. See now, He hath made me the mother of tender children,
and given to thee the care of little sisters, which is next in honour to
that of being their mother. Now His word to us will be in accord with
this, to guide and direct us in our duty, how to walk before them in
love."

"But my mother—?" began Bessie.

"Thy mother is a brave and true Friend, following the word of the
Lord, I doubt not," said Dame Drayton quickly; "but because she did
that which the Lord, bade her do, it doth not follow that thee should
do the same, for the voice of the Spirit may have altogether another
word for thee, and thou must listen to that word and follow it, though
it lead thee in the way thou wouldest shun. Just now, thou art longing
to proclaim to all London that thou art of the despised sect of
Quakers, and by this thou wouldest bring grave trouble upon all this
household, for the Lord Mayor would not send to arrest a girl like
thee, but the man and woman who harboured thee, and so we
should be sent to the Bridewell, and thou and my own little ones
become an added burden to our brethren."

"Would they not send me to prison?" said Bessie, in a disappointed

tone.

"I trove not; though King Charles may profess to think men and
women are plotting against his throne, he would scarcely accuse a
child like thee, and so thou and thy sisters would but be cast forth
upon the world again. Wilt thou try to think of this, Bessie; and to
remember that the Lord ever speaks to us of the duty that lies
nearest to our hand, if we will but listen and obey, instead of seeking
to follow the word He may have given to another? This is how so
many mistakes are made, dear child. We think that the word spoken
to another must be for us also, and so our ears are deafened to the
true message that the Spirit is trying to make us hear and
understand."

"But dost thou not think my father obeyed the voice in his heart?"
asked Bessie quickly.

"Yea, verily, dear child. Nought but the strength that God alone can
give can help even a Friend to bear testimony to the truth before
such cruel enemies; but dost thou not see that, while some are
called to be martyrs for the truth, others are commanded to take up
the cross of everyday life, and bear it meekly and patiently, though it
lead not to such honour and renown as the martyr may claim? This
is what we are called to, dear child. Thou and I must take care of the
little ones at home, not denying our faith if any ask us concerning it,
but seeking not to thrust it before the eyes of men; content to be
unnoticed and unknown, but ever listening to the voice that will not
fail to make itself heard in our hearts, if we will but listen with a
simple mind."

Bessie bowed her head, but she was only half convinced of the truth
her friend had spoken. Her father had declared again and again that
they had no right to sit calmly doing the everyday work of life, while
sinners were perishing for lack of the word of life.

He had not scrupled to denounce his neighbours who went to church

as formalists and hypocrites, and even in the church itself had stood
up and warned parson and people alike, telling them that God could
be worshipped in the open fields, in the house or shop, better than in
a steeple-house; and he had gathered crowds around him in the
fields beyond Southwark, and taught them the truth as he had
received it from the lips of George Fox, the founder of their Society.
He was a true and ardent disciple of Fox, counting nothing dear so
that he might proclaim the truth, the whole truth—as he thought—for
in the tenacity with which he held to the little bit he had been able to
grasp, he failed to see that he could not grasp the whole. That those
whom he denounced so unsparingly also held the truth as they
perceived it, or at least another facet of the precious gem, casting its
inspiring light upon them, was dark to him.

This had not been heeded by the authorities at first, and Westland,
like many another earnest man, was allowed to preach and teach
sinners the error of their ways, and warn them of the wrath to come.
For to make men tremble and quake, and cry to God for mercy
through the Lord Jesus Christ, was the object of all the Quakers'
preaching, and the term "Quaker" had been given them in derision
on account of this.

For a time these people had been allowed to follow their own way
without much interference from the authorities; but their unsparing
denunciation of vice and wickedness, whether practised by rich or
poor, doubtless raised the resentment of the king, though a political
reason was the one put forward for their persecution. The safety of
the throne, it was pretended, called for the suppression of these
illegal meetings, as sedition was being taught under cover of religion.

So Westland was an early victim, and suffered the loss of his goods,
for everything he possessed had to be sold to pay the fine inflicted
upon him. But so far from deterring him from doing what he
conceived to be his duty, this did but make him the more determined
to teach and preach upon every occasion possible.

The next time, a short term of imprisonment, and one ear was cut off
by way of punishment. But almost before the place was healed he
was preaching again, and denouncing steeple-houses, and those
who put their trust in them.

This time the authorities were determined to silence him, and so he

had been condemned to lose his other ear, and then be sent as a
slave to one of His Majesty's plantations in America, and all London
was ringing with the name of Westland, and the punishment that had
been dealt out to him as an incorrigible Quaker.

CHAPTER III.
AUDREY LOWE.

"MOTHER, am I truly and verily bound 'prentice to Master Drayton?"

asked one of the lads when he went home that night.
His mother was a widow, and lived a mile or two from Soper Lane,
and moreover was so busily employed in lace-making all day that
she heard very little of what went on around her unless her son
Simon brought home news that he had heard during the day, or on
his way home at night, so that his next question as to whether she
had heard the name of Westland only made the widow shake her
head as she counted the threads of her lace to make sure that she
was not doing it wrong.

"Has Master Drayton taken another apprentice of that name?" asked

his mother, not pausing in her work to look at her boy's face, or she
would have seen a look of horror there as he answered quickly—

"It isn't quite so bad as that, mother."

"What do you mean, Sim?" she asked. "Dame Drayton is our Dame
Lowe's own sister, and a godly woman, I have heard, as well as her
husband—godly and charitable as the parson himself," added the
widow, "or he would not have taken thee to learn the trade and
business of a hatter without price, merely because I was a widow
known to the parson and his wife."

"Oh yes, they are godly and kind; but did I ever tell you, mother, that
one of the rules of the workshop is that we shall not speak more than
is needful?"

"And a very wise rule too, if proper work is to be done," said his
mother quickly.

"That may be; but you have heard of the Quakers, mother?"

"Oh yes, a set of infidel people who speak against the king and the
church, and rebel against all law and order. A most pestilent and
unruly people, I have heard; but surely—"

Sim folded his arms and leaned upon the table, the guttering candle
lighting up his face so that his mother could not fail to see the fright
and horror depicted there as he said—
"I believe Master Drayton is a Quaker, mother."

"Nay, nay, Sim; 'tis a thing impossible. Dame Lowe told me her sister
was a godly Puritan like ourselves; more stiff in her opinions
altogether than she and the parson, for Dame Drayton had
counselled that he should give up the church rather than use the
new prayer-book, since he could not believe and accept all that was
taught in it, and—"

"It would have been a bad case for us if Parson Lowe had refused to
conform to the new rule, like so many did," interrupted Sim at this
point.

"Yes, it would; and a worse case for his wife and children, for they
might have starved by this time instead of living in a comfortable
house, with money to help the poor as well as themselves, and I
must say, since these changes came, parson has been even more
strict and attentive to his duties, though none could complain of him
before."

"But what has that to do with Master Drayton being a Quaker?"

asked the lad, a little impatiently.

"Why, cannot you see, Sim, that all the family are of so godly a sort,
that they would not be likely to take up with all the unruly and wild
notions that these pestilent people teach?"

"I don't know what the Quakers teach, but I know that one fellow
named Westland has had his ears cut off, and now three girls of the
same name have come to live with us in Soper Lane. If they were
not Quakers themselves, would they take in a disgraced Quaker's
children?"

The widow looked at her son for a minute as if she thought this
argument was unanswerable, but after a minute's pause she said—

"They are kind and godly folk, you say, and so it may be they are not
of this pestilent sect that hath been suffered to spring up to speak
evil of dignities, though they succour these children."

But although the widow said this, she decided to go and see her
friend the vicar, and have a word with his wife too if it was possible,
for it would never do to let her son—her only child—become
contaminated, even though he was being taught his trade without the
cost of a penny to herself.

During the rest of the evening she asked the boy a good many
questions about his work in Soper Lane, and the ways of the
household, but there seemed no fault to be found with anything,
though doubtless the household was ruled strictly, as most Puritan
homes were. Still, what Sim had told her about Westland made her
uncomfortable, and before she went to bed she decided to go to the
vicarage the next morning as soon as Sim had started to Soper
Lane, and doubtless the parson or Dame Lowe would be able to
explain everything, and set her fears at rest.

But when she went, she heard from the maid-servant that the vicar
was ill in bed with a bad cold, and that she would have to wait a little
while to see her mistress.

"Then I will wait," said the widow, for she had scarcely been able to
sleep for thinking of the peril to which her boy might be exposed if it
should be true that his master was a Quaker, as he suspected.
Dame Lowe would be able to set her fears at rest, she hoped, and
the moment the lady entered the room the widow began a recital of
her trouble.

At first she was too full of what she had to say, and how frightened
she had become, to pay much attention to the lady herself, but after
a minute or two she noticed that she was trembling, and her face
had become as white as the lace ruffle she wore round her neck.

"I—I am afraid you are ill, madam," said the widow, stopping short in
her recital, and looking hard at the lady.
"Just a little faint. I have been anxious about the vicar, you see—but
go on with your story. What did your boy say was the name of these
children?"

The lady spoke eagerly, and looked almost as frightened and

anxious as her visitor, though she was careful not to let her know
that it arose from the same cause, and spoke of the vicar's illness as
being a little alarming, and having upset her.

"But tell me about those children who have gone to live at the house
in Soper Lane. Who did you say they were?"

"Well, now, Sim couldn't be quite sure, of course; but he is a careful

lad, and he says there was a Quaker of the same name had his ears
cut off for heresy only a day or two ago. Of course, I told Sim that his
master, being a godly and charitable man, might have had
compassion on these witless children without being himself a
Quaker."

"Then it is suspected that Dame Drayton and her husband are both
Quakers. Is that what you mean, Tompkins?"

The lady's mood had changed during the last few moments, and she
looked hard at the widow and spoke in a severe tone, as though
such a charge as she brought was not to be believed.

"I—I don't know what to think," said the widow. "Of course, as
Madam Drayton is your sister she could scarcely be infected with
such heresy as these wild Quakers believe."

"I trow not, indeed. My sister was brought up in a true godly fashion,
but the same charity that moved Master Drayton to take Simon as an
apprentice without fee or reward, because you were a poor widow
known to me to have lost so much by the plague and the great fire,
may have moved her to help these poor children, if no one else
would do it."
"Then you think my Sim would be quite safe there?" said the widow
in a deprecating tone.

Madam Lowe looked surprised at the question. "Why should he not

be safe?" she asked. "You told me the other day that he was learning
his trade very well, and had certainly improved in his manners."

"But—but if his master should be a Quaker it would be little better

than sending him where he would catch the plague, this new plague
of heresy that is abroad, and for my Sim to turn Quaker would be
worse than losing the others by the pestilence." And at the thought of
all the sorrow and suffering she had endured through this scourge,
the Widow Tompkins fairly burst into tears.

"There, don't cry—I am sure you are frightening yourself for nothing.
I know my sister to be a gentle godly woman; no more like the wild
fanatic Fox than you are. She attends her own parish church as you
do, and therefore you may rest content that Sim is safe."

The widow allowed herself to be comforted by this assurance.

"It's all we've got to hold fast by in the way of knowing what to
believe, for there's been so many changes in religion, as well as
other things the last few years, that simple folk like me, who have no
learning, hardly know what they ought to believe sometimes; but to
have Sim turn Quaker would just break my heart, when I was looking
forward to a little comfort after all my trouble."

"Oh, Simon will be a good son, and a comfort to you, I have no

doubt," said the lady, rising to dismiss her visitor. "Take care that he
is at church by seven o'clock next Sunday morning, for the vicar is
going to catechise all the lads and wenches of the parish, and it will
not do for Simon to be absent from his place in the chancel."

"My son will be early. I am glad the vicar is going to give them a
wholesome reminder of what they ought to know and do, as
respectable citizens and members of the Church of England. It will
help to stop this wild Quaker heresy, I trow."
The lady smiled and nodded her assent; but she was too impatient
for her visitor to go to make any verbal reply to this, and as soon as
she had closed the street door she went upstairs to a little room
where a girl sat sewing.

"What is the matter, mother?" she asked as the lady seated herself,
and buried her face in her hands.

For a minute or two the lady sat thus, and when she removed them
she was looking white and anxious.

"Oh, Audrey, I wish I had never persuaded your father to—" But
there she stopped, for the girl's wondering eyes told her she was
speaking of things she had long ago resolved to bury in her own
heart. "My dear, I want you to go and see your Aunt Martha," she
said quickly.

"Aunt Martha?" repeated the girl in a tone of wonder.

"Have you forgotten her, Audrey? It is not so many years since you
saw your aunt."

"But I thought you said she died in the time of the first plague," said
the girl, still looking at her mother with a puzzled expression in her
face, as if trying to recall some memory of the forgotten relative.

"Nathless you will remember her again when you see her," said
Dame Lowe, in answer to her daughter's puzzled look. "I want you to
go to her this afternoon, and say that the Widow Tompkins, who is
the mother of one of her husband's 'prentice lads, hath been here
with a tale about Quakers that is disgraceful to any godly
household."

"The Widow Tompkins is always in a fright about something,"

returned Audrey slightingly. "What did she say about the Quakers
and my Aunt Martha? What has she to do with them?"
"Nothing, I wot; but Master Drayton, her husband, is not always so
discreet as he should be, and Simon hath brought home some tale
to his mother about Quaker children being harboured in the house.
Your aunt ought to be told that this is known, and will soon become
the talk of the town if they are not sent away."

"Would you like me to bring the children here, mother, to save Aunt
Martha the trouble of them?"

The lady looked at her daughter, aghast with horror at the proposal.

"Audrey, you must not speak so lightly of such matters. For us to be

suspected of any touch with these Quakers would mean ruin, and we
might be thrown out of house and home, like so many clergymen's
families have been, for it is known that your father always felt they
were unjustly treated, though he signed the declaration that saved us
from being turned into the streets like beggars. This is why I want
you to go and see your aunt to-day, for if people think the Draytons
are Quakers they may suspect us next. Oh dear! why will people go
wild about religion like this man Fox? It is sure to bring disgrace
upon somebody. As if the fire and the plague had not caused misery
enough in London, they must now begin making fresh trouble about
religion, just as I hoped things were getting more settled and
comfortable."

"Mother dear, do not look so troubled about this. Surely God can
take care of us and of London too. How is my father now?"

"Not much better, and I do not want him to hear about this, or it will
make him anxious and unfit to catechise the children in church on
Sunday morning. Now, Audrey, we shall have dinner at eleven, and
then I should like you to go to your aunt, who lives in Soper Lane,
and you can see for yourself who these Quaker children are, and
find out whether your aunt still goes to the parish church, for I hear
these fanatics call it a steeple-house, and will by no means join in
the prayers as they are set forth in the prayer-book."
The errand in itself was not at all to the taste of a girl like Audrey; but
the dim recollection she had of her aunt made her desirous of seeing
her once more, and she could only wonder how and why it was that
her mother had been silent concerning Dame Drayton, for they had
but few relatives, and Audrey herself was the only child now. Two
had died during the great plague, and she could only suppose that it
was because her aunt lived in the City, and her mother still had a
lingering dread of the plague returning, that she had not heard this
aunt spoken of for so long a time.

Although they lived within easy walking distance of the City, and she
knew her father sometimes went there on business, she did not
remember ever having seen it herself, for they lived in the
fashionable suburbs of St. Martin-in-the-Fields, and generally went to
walk in the westerly direction among the fields and green lanes. The
parish did not wholly belie its name as yet, for they lived in the midst
of the open country, although so near London. Her old nurse was to
walk with her, and call for her at Soper Lane at four o'clock, that they
might reach home before sunset, for although their way lay through
the best and most fashionable thoroughfares in the town, they were
by no means safe from footpads. Although the Strand was the
residence of many of the nobility, and Fleet Street had most of the
best shops lining its footway, these were generally shunned by
travellers after sundown—unless they were on horseback, armed
and attended by two or three stout serving-men.

So Audrey and her nurse set out on their journey about half-past
eleven, and less than a mile from her own home, Audrey was in a
place altogether new to her.

"I wonder why we have not come this way to walk before," said the
girl looking round at the handsome houses in the Strand.

But the 'prentice lads in the front of their masters' shops in Fleet
Street, all eager to press their wares upon their notice, were not a
pleasant feature of the scene to Audrey.