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Advances in Marine Biology Vol 54 1st Edition David W.
Sims (Ed.) Digital Instant Download
Author(s): David W. Sims (Ed.)
ISBN(s): 9780123743510, 0123743516
Edition: 1st
File Details: PDF, 4.68 MB
Year: 2008
Language: english
Advances in MARINE BIOLOGY
Series Editor
DAVID W. SIMS
Marine Biological Association of the United Kingdom,
The Laboratory Citadel Hill, Plymouth, United Kingdom

Editors Emeritus
LEE A. FUIMAN
University of Texas at Austin

CRAIG M. YOUNG
Oregon Institute of Marine Biology

Advisory Editorial Board

ANDREW J. GOODAY
Southampton Oceanography Centre

GRAEME C. HAYS
University of Wales Swansea

SANDRA E. SHUMWAY
University of Connecticut

ROBERT B. WHITLATCH
University of Connecticut
Academic Press is an imprint of Elsevier
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CONTRIBUTORS TO VOLUME 54

Kenneth W. Able
Marine Field Station, Institute of Marine and Coastal Sciences, Rutgers University,
Tuckerton, New Jersey 08087
Christin Frieswyk DeJong
Arboretum and Botany Department, University of Wisconsin-Madison, Madison,
Wisconsin 53711
Bridget S. Green
Marine Research Laboratory, Tasmanian Fisheries and Aquaculture Institute,
University of Tasmania, Private Bag 49, Tasmania, 7001 Australia
Charles H. Peterson
Institute of Marine Sciences, University of North Carolina at Chapel Hill,
Morehead City, North Carolina 28557
Michael F. Piehler
Institute of Marine Sciences, University of North Carolina at Chapel Hill,
Morehead City, North Carolina 28557
Charles A. Simenstad
School of Aquatic and Fishery Sciences, University of Washington, Seattle,
Washington 98195
David W. Sims
Marine Biology and Ecology Research Centre, School of Biological Sciences,
University of Plymouth, Drake Circus, Plymouth PL4 8AA, United Kingdom
Marine Biological Association of the United Kingdom, The Laboratory, Citadel
Hill, Plymouth PL1 2PB, United Kingdom
Victoria J. Wearmouth
Marine Biological Association of the United Kingdom, The Laboratory, Citadel
Hill, Plymouth PL1 2PB, United Kingdom
Joy B. Zedler
Arboretum and Botany Department, University of Wisconsin-Madison, Madison,
Wisconsin 53711

v
SERIES CONTENTS FOR LAST FIFTEEN YEARS*

Volume 30, 1994.

Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambs-
head, P. J. D., Pfannküche, O., Soltweddel, T. and Vanreusel, A.
Meiobenthos of the deep Northeast Atlantic. pp. 1–88.
Brown, A. C. and Odendaal, F. J. The biology of oniscid isopoda of
the genus Tylos. pp. 89–153.
Ritz, D. A. Social aggregation in pelagic invertebrates. pp. 155–216.
Ferron, A. and Legget, W. C. An appraisal of condition measures for
marine fish larvae. pp. 217–303.
Rogers, A. D. The biology of seamounts. pp. 305–350.
Volume 31, 1997.
Gardner, J. P. A. Hybridization in the sea. pp. 1–78.
Egloff, D. A., Fofonoff, P. W. and Onbé, T. Reproductive behaviour
of marine cladocerans. pp. 79–167.
Dower, J. F., Miller, T. J. and Leggett, W. C. The role of microscale
turbulence in the feeding ecology of larval fish. pp. 169–220.
Brown, B. E. Adaptations of reef corals to physical environmental
stress. pp. 221–299.
Richardson, K. Harmful or exceptional phytoplankton blooms in the
marine ecosystem. pp. 301–385.
Volume 32, 1997.
Vinogradov, M. E. Some problems of vertical distribution of meso-
and macroplankton in the ocean. pp. 1–92.
Gebruk, A. K., Galkin, S. V., Vereshchaka, A. J., Moskalev, L. I. and
Southward, A. J. Ecology and biogeography of the hydrothermal
vent fauna of the Mid-Atlantic Ridge. pp. 93–144.
Parin, N. V., Mironov, A. N. and Nesis, K. N. Biology of the Nazca
and Sala y Gomez submarine ridges, an outpost of the Indo-West
Pacific fauna in the eastern Pacific Ocean: composition and distri-
bution of the fauna, its communities and history. pp. 145–242.
Nesis, K. N. Goniatid squids in the subarctic North Pacific: ecology,
biogeography, niche diversity, and role in the ecosystem. pp. 243–324.
Vinogradova, N. G. Zoogeography of the abyssal and hadal zones.
pp. 325–387.
Zezina, O. N. Biogeography of the bathyal zone. pp. 389–426.

*The full list of contents for volumes 1–37 can be found in volume 38.

ix
x Series Contents for Last Fifteen Years

Sokolova, M. N. Trophic structure of abyssal macrobenthos.

pp. 427–525.
Semina, H. J. An outline of the geographical distribution of oceanic
phytoplankton. pp. 527–563.
Volume 33, 1998.
Mauchline, J. The biology of calanoid copepods. pp. 1–660.
Volume 34, 1998.
Davies, M. S. and Hawkins, S. J. Mucus from marine molluscs.
pp. 1–71.
Joyeux, J. C. and Ward, A. B. Constraints on coastal lagoon fisheries.
pp. 73–199.
Jennings, S. and Kaiser, M. J. The effects of fishing on marine
ecosystems. pp. 201–352.
Tunnicliffe, V., McArthur, A. G. and McHugh, D. A biogeographical
perspective of the deep-sea hydrothermal vent fauna. pp. 353–442.
Volume 35, 1999.
Creasey, S. S. and Rogers, A. D. Population genetics of bathyal and
abyssal organisms. pp. 1–151.
Brey, T. Growth performance and mortality in aquatic macrobenthic
invertebrates. pp. 153–223.
Volume 36, 1999.
Shulman, G. E. and Love, R. M. The biochemical ecology of marine
fishes. pp. 1–325.
Volume 37, 1999.
His, E., Beiras, R. and Seaman, M. N. L. The assessment of marine
pollution—bioassays with bivalve embryos and larvae. pp. 1–178.
Bailey, K. M., Quinn, T. J., Bentzen, P. and Grant, W. S. Population
structure and dynamics of walleye pollock, Theragra chalcogramma.
pp. 179–255.
Volume 38, 2000.
Blaxter, J. H. S. The enhancement of marine fish stocks. pp. 1–54.
Bergström, B. I. The biology of Pandalus. pp. 55–245.
Volume 39, 2001.
Peterson, C. H. The ‘‘Exxon Valdez’’ oil spill in Alaska: acute indirect
and chronic effects on the ecosystem. pp. 1–103.
Johnson, W. S., Stevens, M. and Watling, L. Reproduction and
development of marine peracaridans. pp. 105–260.
Series Contents for Last Fifteen Years xi

Rodhouse, P. G., Elvidge, C. D. and Trathan, P. N. Remote sensing

of the global light-fishing fleet: an analysis of interactions with
oceanography, other fisheries and predators. pp. 261–303.
Volume 40, 2001.
Hemmingsen, W. and MacKenzie, K. The parasite fauna of the
Atlantic cod, Gadus morhua L. pp. 1–80.
Kathiresan, K. and Bingham, B. L. Biology of mangroves and man-
grove ecosystems. pp. 81–251.
Zaccone, G., Kapoor, B. G., Fasulo, S. and Ainis, L. Structural,
histochemical and functional aspects of the epidermis of fishes.
pp. 253–348.
Volume 41, 2001.
Whitfield, M. Interactions between phytoplankton and trace metals
in the ocean. pp. 1–128.
Hamel, J.-F., Conand, C., Pawson, D. L. and Mercier, A. The sea
cucumber Holothuria scabra (Holothuroidea: Echinodermata): its
biology and exploitation as beche-de-Mer. pp. 129–223.
Volume 42, 2002.
Zardus, J. D. Protobranch bivalves. pp. 1–65.
Mikkelsen, P. M. Shelled opisthobranchs. pp. 67–136.
Reynolds, P. D. The Scaphopoda. pp. 137–236.
Harasewych, M. G. Pleurotomarioidean gastropods. pp. 237–294.
Volume 43, 2002.
Rohde, K. Ecology and biogeography of marine parasites. pp. 1–86.
Ramirez Llodra, E. Fecundity and life-history strategies in marine
invertebrates. pp. 87–170.
Brierley, A. S. and Thomas, D. N. Ecology of southern ocean pack
ice. pp. 171–276.
Hedley, J. D. and Mumby, P. J. Biological and remote sensing
perspectives of pigmentation in coral reef organisms. pp. 277–317.
Volume 44, 2003.
Hirst, A. G., Roff, J. C. and Lampitt, R. S. A synthesis of growth
rates in epipelagic invertebrate zooplankton. pp. 3–142.
Boletzky, S. von. Biology of early life stages in cephalopod molluscs.
pp. 143–203.
Pittman, S. J. and McAlpine, C. A. Movements of marine fish and
decapod crustaceans: process, theory and application. pp. 205–294.
Cutts, C. J. Culture of harpacticoid copepods: potential as live feed
for rearing marine fish. pp. 295–315.
xii Series Contents for Last Fifteen Years

Volume 45, 2003.

Cumulative Taxonomic and Subject Index.
Volume 46, 2003.
Gooday, A. J. Benthic foraminifera (Protista) as tools in deep-water
palaeoceanography: environmental influences on faunal character-
istics. pp. 1–90.
Subramoniam, T. and Gunamalai, V. Breeding biology of the intertidal
sand crab, Emerita (Decapoda: Anomura). pp. 91–182
Coles, S. L. and Brown, B. E. Coral bleaching—capacity for acclima-
tization and adaptation. pp. 183–223.
Dalsgaard J., St. John M., Kattner G., Müller-Navarra D. and Hagen
W. Fatty acid trophic markers in the pelagic marine environment.
pp. 225–340.

Volume 47, 2004.

Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J.,
Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M. A.,
Halliday, N. C., Harris, R. P., Leaper, R., Mieszkowska, N., Pingree,
R. D., Richardson, A. J., Sims, D.W., Smith, T., Walne, A. W. and
Hawkins, S. J. Long-term oceanographic and ecological research in the
western English Channel. pp. 1–105.
Queiroga, H. and Blanton, J. Interactions between behaviour and
physical forcing in the control of horizontal transport of decapod
crustacean larvae. pp. 107–214.
Braithwaite, R. A. and McEvoy, L. A. Marine biofouling on fish
farms and its remediation. pp. 215–252.
Frangoulis, C., Christou, E. D. and Hecq, J. H. Comparison of
marine copepod outfluxes: nature, rate, fate and role in the carbon
and nitrogen cycles. pp. 253–309.

Volume 48, 2005.

Canfield, D. E., Kristensen, E. and Thamdrup, B. Aquatic Geomicro-
biology. pp. 1–599.

Volume 49, 2005.

Bell, J. D., Rothlisberg, P. C., Munro, J. L., Loneragan, N. R., Nash,
W. J., Ward, R. D. and Andrew, N. L. Restocking and stock
enhancement of marine invertebrate fisheries. pp. 1–358.
Volume 50, 2006.
Lewis, J. B. Biology and ecology of the hydrocoral Millepora on coral
reefs. pp. 1–55.
Series Contents for Last Fifteen Years xiii

Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren,

C. P., Holmes, K. E., and Brumbaugh, D. R. The functional value of
Caribbean coral reef, seagrass and mangrove habitats to ecosystem
processes. pp. 57–189.
Collins, M. A. and Rodhouse, P. G. K. Southern ocean cephalopods.
pp. 191–265.
Tarasov, V. G. EVects of shallow-water hydrothermal venting on
biological communities of coastal marine ecosystems of the western
Pacific. pp. 267–410.
Volume 51, 2006.
Elena Guijarro Garcia. The fishery for Iceland scallop (Chlamys
islandica) in the Northeast Atlantic. pp. 1–55.
JeVrey, M. Leis. Are larvae of demersal fishes plankton or nekton?
pp. 57–141.
John C. Montgomery, Andrew Jeffs, Stephen D. Simpson, Mark
Meekan and Chris Tindle. Sound as an orientation cue for the
pelagic larvae of reef fishes and decapod crustaceans. pp. 143–196.
Carolin E. Arndt and Kerrie M. Swadling. Crustacea in Arctic
and Antarctic sea ice: Distribution, diet and life history strategies.
pp. 197–315.
Volume 52, 2007.
Leys, S. P., Mackie, G. O. and Reiswig, H. M. The Biology of Glass
Sponges. pp. 1–145.
Garcia E. G. The Northern Shrimp (Pandalus borealis) Offshore
Fishery in the Northeast Atlantic. pp. 147–266.
Fraser K. P. P. and Rogers A. D. Protein Metabolism in Marine
Animals: The underlying Mechanism of Growth. pp. 267–362.
Volume 53, 2008.
Dustin J. Marshall and Michael J. Keough. The Evolutionary
Ecology of Offspring Size in Marine Invertebrates. pp. 1–60.
Kerry A. Naish, Joseph E. Taylor III, Phillip S. Levin, Thomas P.
Quinn, James R. Winton, Daniel Huppert, and Ray Hilborn. An
Evaluation of the Effects of Conservation and Fishery Enhancement
Hatcheries on Wild Populations of Salmon. pp. 61–194.
Shannon Gowans, Bernd Würsig, and Leszek Karczmarski. The So-
cial Structure and Strategies of Delphinids: Predictions Based on an
Ecological Framework. pp. 195–294.
Professor Alan James Southward, B.Sc, Ph.D, D.Sc, F.L.S.,
1928–2007

Photo credit: G. Braasch, with permission

Obituary

Stephen Hawkins*,† and David Sims*,‡

With the death of Professor Alan Southward aged 79 on 27 October

2007, Advances in Marine Biology lost a greatly respected past editor of
20 years standing, and science lost one of the most influential British marine
biologists of the past 50 years. Taking over as editor of Advances in Marine
Biology in 1986 following the passing away of Founder Editor Sir Frederick
S. Russell F.R.S., he brought an incredibly broad and deep knowledge of
marine biology to his editorial role as well as the gift of a lucid writing style.
This ensured the production of high-quality reviews of lasting importance
and in so doing he helped a great many scientists along the way.
Alan Southward was one of the leading marine biologists of the second
half of the twentieth century. He conducted seminal research in many areas
of marine ecology, principally studying how organisms are impacted by
environmental changes such as climate and pollution, and how they are
adapted to life on the rocky shore and in the deep sea. He was also a world
expert on barnacle taxonomy. Most notably perhaps, between the 1950s
and 1970s, when climate change research was still in its infancy, he demon-
strated important links between climate and biological changes in the sea,
work that laid the foundations for all subsequent studies worldwide.

Early years
Alan was born in Liverpool on 17 April 1928. His father, a fitter, was
involved in traditional Merseyside industries such as Cunard, eventually
working at the Meccano factory. In his early teens he became profoundly
deaf as a consequence of meningitis but had already become interested
in marine organisms from excursions along the shores of the Mersey. He
grew up during the war attending Liverpool Collegiate School before
entering the University of Liverpool. Getting into University was a major

* Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB,
United Kingdom
{
College of Natural Sciences, Memorial Building, Bangor University, Gwynedd LL57 2UW,
United Kingdom
{
School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United Kingdom

xv
xvi Obituary

achievement for a deaf student, especially during times when there were
fewer opportunities for people with disabilities. By the time Alan was in
Part II and Honours he had a circle of friends who took notes for him
whilst he concentrated on drawing the blackboard diagrams. Clearly this
strategy worked: the University of Liverpool awarded him a First Class
Honours degree in Zoology in 1948. During his undergraduate years at
Liverpool he naturally attached himself to the school of marine biologists
under Professor J. H. Orton F.R.S., and under his direction carried out
vacation research on coelenterates. On the advice of Orton he submitted his
first scientific paper on jellyfish feeding and excretory currents to Nature
(Southward, 1949). Many were to follow. In total he produced over 220
publications, some 21 of which were in Nature, an unusually high number
for an ecologist.
Alan first encountered the University of Liverpool’s Marine Biological
Station (then part of Zoology) at Port Erin whilst attending field courses.
When he first went there electric light had not been installed. This did not
put him off, however, and he returned for Ph.D. studies and then stayed for
a University Post Doctoral Fellowship. His Ph.D. work on the intertidal
ecology around the south of the Isle of Man was with the guidance of
Professor Orton, including both rocky and depositing shores. The breadth
and scope of his Ph.D. was impressive, introducing him to ideas of quanti-
tative ecology, species interactions, geographical distribution, effects of
climate change and time series studies. Whilst doing this work he managed
to find time to add to records for the Isle of Man fauna. He also got seriously
involved in photography—a life-long passion (e.g. Southward et al., 1976).
Much of this early work was published in journals such as Transactions of the
Liverpool Biological Society which denied it a wider audience (Southward,
1953a,b)—but it was an invaluable first step for scores of subsequent Ph.D.
studies at Port Erin. These studies, along with those of Jones, Burrows and
Lodge, were some of the first field experimental studies on rocky shores,
pioneering an approach which has contributed hugely to ecological theory
(reviewed in Southward, 1964a).
Alan concentrated largely on rocky shores during his Fellowship. This
involved biogeographic mapping of the major species of British and Irish
shores, laboratory experiments on the causes of these patterns, completion
and write up of Orton’s work on limpet reproduction and follow up work
on the limpet removal experiments of the late 1940s at Port Erin. Much of
the travel for this biogeographic fieldwork was done on a motorcycle
balanced using sight cues only—intrepid as well as pioneering work. During
this period a long-standing collaboration was started with Professor Dennis
Crisp F.R.S. leading to some of the first papers on the influence of climate
on the outcome of competitive interactions in barnacles. It was his discov-
ery of the occurrence of the warm water barnacle Chthamalus in the Isle of
Man (Southward, 1950) that triggered much of his later work, including
Obituary xvii

broad surveys of distribution and studies of the effects of climate change that
were very much ahead of their time (e.g. Southward, 1951; Southward and
Crisp 1952, 1954; for an overview, see Southward et al., 1995). Indeed, the
combination of field surveys, quantitative experiments and long-term stud-
ies, incorporating new methods and analyses were to typify his leading-edge
research for the next 50 years.
Whilst on the Isle of Man Alan met Eve Judges. Whether on a pillion of a
motorcycle, on the shore or at sea, Eve has been a science collaborator and
source of great support to Alan over the years. Theirs was an almost symbi-
otic relationship, as Eve was often Alan’s interface with the spoken word. She
is also a fine scientist of international reputation in her own right, an expert
on polychaetes, Pogonophora and an equal partner in the work on hydro-
thermal vents and chemosynthetic nutrition of animals (e.g. Southward and
Southward, 1958, 1967, 1968; Southward et al., 1981, 2001).

Long-term studies at Plymouth

Alan moved to Plymouth in 1953 when he took up a DSIR Fellow-
ship at the Laboratory of the Marine Biological Association (MBA), marry-
ing Eve soon after arriving. He remained working at the MBA for the rest of
his life. Throughout the 1950s Alan consolidated his reputation in the
ecology of shore animals, completing much of the biogeographic work
(Southward and Crisp, 1956; Crisp and Southward, 1958), testing tempera-
ture tolerances (Southward, 1958a), undertaking laboratory studies of bar-
nacle feeding behaviour (Southward, 1955a,b,c) and, in 1958, writing a
highly influential review on zonation of rocky shores (Southward, 1958b).
Under the stimulus of Sir Frederick Russell F.R.S. his energies were
directed offshore: he took over responsibility for the zooplankton and
young fish surveys as part of the MBA long-term study of the English
Channel, which stretched back to the start of the twentieth century. He
had realised the importance of climatic fluctuations as the most likely
explanation for the inconsistency of the English Channel ecosystem, espe-
cially given that many species reached their biogeographic limits in the
South and South-West of England (Southward, 1960, 1963). Within this
programme he incorporated studies of intertidal barnacles as indicators of
climate change (Southward, 1967). Interestingly, the barnacle biogeo-
graphic work carried out in the UK and overseas led to the discovery that
there were two species of barnacles in Europe masquerading under the name
of Chthamalus stellatus (Southward, 1964b, 1976), given to them by Darwin.
He was awarded his D.Sc. from the University of Liverpool in the early
1960s. He gained much satisfaction from the presence on the platform of the
degree ceremony of a former Dean, who a decade earlier had not been
xviii Obituary

convinced about the wisdom of admitting a deaf student to the university.

With a larger research ship at the MBA capable of working the continental
slope, interests offshore and in deep water were developed in the 1950s and
1960s in liaison with Eve. It was the intention to study what appeared to be
a barnacle zone at 1200 m close to cold-water reefs in the deep water of the
Bay of Biscay. However, poor offshore position finding in those pre-GPS
days resulted in many hauls of mud instead of the rock and coral expected.
But in those hauls were the first pogonophoran tube-worms found in the
Atlantic at the time (Southward, 1958c; Southward and Southward 1958).
Together, they started working on the gutless pogonophoran worms that in
the past had probably been thrown back over the side as ‘gubbins’. The very
cold winter of 1962/63 and a switch back to colder conditions prompted
continuation of long-term studies on the shore and helped maintain the
impetus for the long-term offshore work (Crisp and Southward, 1964;
Russell et al., 1971; Southward, 1974). A very influential review of the
influence of limpet grazing (Southward 1964a) was written and a textbook
on seashore ecology followed in 1965 (Southward, 1965).
Although the work on shores was perhaps less prominent in Alan’s
research by the late 1960s, it was reawakened with a crash when the Torrey
Canyon oil spill contaminated most of the shores of western Cornwall in
1967. Serendipitously, the network of sites that Alan had established for
long-term studies on climate effects on shore animals, came into its own as a
baseline for assessing the aftermath of the spill and the recovery of the
ecosystem. The research on the recovery of shores from oil and the massive
use of dispersants became a much-cited classic (Southward and Southward
1978). The Southwards demonstrated that the chemicals used to disperse
the oil were more toxic to the animals and plants than the oil itself. They
showed that on shores where dispersants had been used some 10–15 years
were needed for recovery of former conditions, whereas, in contrast, only
2–3 years were required on untreated, solely oil-laden shores. The work
also gave valuable insights on the role of limpet grazing in structuring shore
communities, in addition to elucidating mechanisms of succession. Alan’s
innovative and patient research was hugely influential at the time and was,
with other MBA research in the aftermath of the Torrey Canyon, largely
responsible for governments and agencies abandoning the widespread use of
toxic chemicals to tackle oil slicks.
In the 1970s research was concentrated on describing the return of more
northerly species to the English Channel and the work that followed
became a seminal contribution (Russell et al., 1971; Southward, 1974;
Southward et al., 1975). Alan Southward, together with colleagues, were
essentially the first to discover, by documenting in hitherto unparalleled
detail, how marine species respond to climate changes. In the western
English Channel it was noticed that cold-water herrings and plankton, once
common in the 1920s, had declined and were replaced by warm-water
Obituary xix

pilchards and plankton in the 1940s and 1950s. During the 1960s and 1970s
boreal fish and plankton once again dominated. Relating these to fluctua-
tions in the long-term sea temperature records and other physical data
(Southward, 1960; Southward and Butler, 1972), Alan realised that the
shifts in animal distribution and changes in abundance were closely linked
with climate oscillations. The strength of this work was in its breadth and
depth; he set about documenting changes in immense detail, from shore
organisms to plankton and fish, and proposed several biological mechan-
isms. Later work using these data sets together with much older records
from archived newspapers and diaries showed similar fluctuations in herring
and pilchard fisheries occurring off Devon and Cornwall in relation to
climate since at least the sixteenth century (Southward et al., 1988). The
whole series of studies culminated in an excellent review and synthesis
published in Nature in 1980—this described arguably the first large-scale
study providing clear evidence of how ecosystems appear to shift between
different and apparently stable states in relation to climate (Southward,
1980). This review also noted a breakdown in the relationship between
sunspots as an index of solar heat flux and sea temperature, thereby making a
contribution to emerging ideas about human driven climate change.
The 1970s also marked the realisation that Darwin’s panglobal
species Chthamalus stellatus was several species and that European C. stellatus
consisted of two species: C. stellatus Poli and C. montagui Southward
(Southward, 1976). Alan embraced new techniques in collaboration with
Paul Dando to sort out these taxonomic problems, using gel electrophoresis
of enzymes to identify cryptic species (e.g. Dando and Southward, 1980).
Over the years Alan became the European taxonomic expert on barnacles,
revising much of Darwin’s early work on barnacles as well as working on
deep-sea stalked barnacles, culminating in Southward (2008).

Deep Sea discoveries

The late 1970s saw the discovery of hydrothermal vents on the
Galapagos Ridge in the Central Eastern Pacific. The Southward’s long-
standing interest in Pogonophora became suddenly fashionable as closely
related giant vestimentiferan worms were discovered by Alvin dives. Alan
and Eve’s previous work had focused on how small pogonophores might
obtain nutrition from dissolved organic compounds in the sediment
(Southward and Southward 1968). But following the discovery by Colleen
Cavanaugh of endosymbiotic sulphur-oxidising bacteria that supplied the
giant vestimentiferan tubeworms with their nutrition by chemosynthesis,
they quickly discovered that the small pogonophores of the Atlantic conti-
nental slope also contained endosymbiotic bacteria (Southward et al., 1981).
xx Obituary

They involved Paul Dando and David Dixon throughout the 1980s and
1990s in this exciting new endeavour (e.g. Southward and Dixon, 1980).
Further work on the metabolism of the pogonophores’ symbionts bene-
fitted greatly from the practical skills of the group in extracting minute
amounts of bacteria from the worms for use in enzyme assays. Alan in
particular showed a great ability for this highly dexterous and sustained
work on research ships in often rough seas, presumably due in part to his
enviable immunity to seasickness, a fortunate consequence of his deafness.
However, despite much progress during several cruises in the Bay of Biscay,
for example, identifying the chemosynthetic energy source for the slope
pogonophores proved difficult. It was not until cruises in the Norwegian
fjords that the discovery was made of two species of bivalves with endo-
symbiotic bacteria, living alongside the pogonophores, and the finding that
all these organisms were capable of obtaining energy by ‘mining’ iron
sulphides (Dando et al., 1986; Southward et al., 1986; Spiro et al., 1986).
This opened up a new field of research of international importance since
Alan and colleagues were able to demonstrate that organisms obtaining
nutrition from endosymbiotic autotrophic bacteria were found in most
reducing marine sediments from the intertidal to the deep sea.

‘Retirement’ years
Alan was an unfortunate casualty of the re-organisation of the Marine
Laboratories at Plymouth in 1986/1987; he had to retire at the age of 60
instead of 65 because of the new terms of employment offered to MBA staff.
The 80-plus year old MBA time series was stopped in 1988—ironically just
as detection of global warming and its impacts on marine ecosystems were
becoming apparent. Characteristically, Alan bounced back. Leverhulme
funding for a Senior Fellowship was secured providing salary and funding
for another 3 years concentrating on chemosynthetic-driven systems,
research conducted in equal partnership with Eve (Gebruk et al., 1997).
As well as accepting time on research ship cruises in the Norwegian fjords,
the North Sea and the Caribbean, studies were also pursued off the coast of
British Columbia in Canada. He was awarded an Adjunct Professorship of
Victoria University, British Columbia, collaborating with Verena Tunni-
cliffe and her group, and a house was purchased in Canada to be nearer to
the vents. This freedom of action allowed successful applications to the UK
Natural Environment Research Council (NERC) and the European Union
for grants and there was not any hint of retirement. In 1989 Alan was made a
Visiting Professor of Marine Biology at the University of Liverpool Port
Erin Laboratory where his visits to teach and co-supervise students were
Obituary xxi

always much appreciated. After 1987 in so-called retirement, he published

well over 80 papers, books and book chapters.
A bad fall in 1999 stopped work at sea and on the shore, so the focus of
Alan’s work became barnacle taxonomy and advising on the re-start of
long-term series on UK shores and in the Western English Channel
between 1999 and 2006. He completed a Linnean Society Monograph on
barnacles just before his death that was published in 2008 (Southward,
2008). Alan also led a major review of the long-term research conducted
in the Western English Channel by the Plymouth laboratories for more than
100 years, and which appeared in 2005 in Advances in Marine Biology
(Southward et al., 2005). Furthermore, without his presence at the MBA
laboratory much of the long-term data would have become neglected, lost
or deleted from old file formats. His data stewardship has led to a great many
papers of relevance to climate change effects and fisheries (e.g. Sims et al.,
2001, 2004; Genner et al., 2004). Some papers contributed to the recent
report assembled by the Nobel-prize winning Intergovernmental Panel on
Climate Change (IPCC). Alan graciously handed over the MBA time-series
on rocky shore organisms, plankton and fish to younger generations as well
as the editing of Advances in Marine Biology. He was an exquisite editor of
Advances, with such great attention to detail and a real devotion to the task of
helping to produce comprehensive reviews of exceptional clarity across a
breathtaking array of subject areas, allowing both newcomers to a subject
and seasoned experts a thorough understanding. His knowledge of marine
biology was encyclopaedic and the expertise he brought to editing was
equally impressive, not least his lucid writing style that was a pleasure to read
(e.g. Southward and Roberts, 1987). Furthermore, the help he gave to
authors, especially to those from overseas, was way beyond the call of
scientific duty. He particularly welcomed reviews from outside Europe
and the United States, and gave great help and encouragement to many of
these scientists in making their work accessible to an international audience.

His science legacy

Alan Southward mastered a wide range of disciplines and contributed
seminal work in diverse areas of marine biology, from barnacle taxonomy to
quantitative ecology, and from biogeographic surveys to climate change and
long-term studies. Although he followed in the footsteps of the old naturalist
scientists of the early part of the twentieth century, whose interests were often
similarly broad, to say he was a marine naturalist in the older sense of the word
is not sufficient. He was an extremely good marine naturalist but he was also
prepared to use modern analytical and computing techniques to confirm his
observations. Without doubt one of Alan’s most important contributions has
xxii Obituary

been as a pioneer, steward and interpreter of long-term monitoring data sets

to understand how marine organisms respond to environmental fluctuations
(Southward, 1991). Throughout the 1990s it became clear that global climate
change was occurring. There was a growing realisation of the human contri-
bution via greenhouse gases; global warming progressed from speculation to a
generally accepted view. The value of long-term data sets were belatedly seen
as vital to help disentangle human driven global change from natural fluctua-
tions (Southward, 1980) and local and regional impacts such as fishing
(Southward, 1981a), pollution and habitat loss (Southward 1981b). Although
scientists and politicians are now in general agreement that human activity is
affecting Earth’s climate and the oceans, this was not always the case. Alan
Southward realised very early that physical and biological variables measured
frequently and over long periods would be vital for assessing the effects of
climate change on marine ecosystems and he championed this method for
over 50 years (Southward, 1995).
Alan was not only instrumental in setting up new complementary time
series of biological observations in the western English Channel and else-
where during the 1950s and 1960s but was also responsible for invigorating
the maintenance of established time series (dating from 1900) with his vision
that this could lead to greater understanding of complex processes relevant to
society. This he pursued at a time when the biological effects of climate and
other external drivers in marine systems were very poorly understood and
when this work was deemed unfashionable in science and funding for it was
difficult to obtain. However, largely owing to his careful work and strength of
character, these data sets are now reaching maturity and proving of crucial
importance for helping to develop a fundamental understanding of the effects
of climate-linked sea temperature changes on the distribution and abundance
of marine animals and plants. Without Alan’s foresight these valuable time-
series data sets that he pioneered, helped motivate and later championed
would not now be available to the marine science community. In this
sense, he was a scientist very much ahead of his time. The impact of his
research is both broad and long-lasting. Reference (citations) to his early
work on climate impacts on marine animals and plants in particular continues
to grow as a new generation of scientists re-discover its prescience. It is fair to
say that his work laid the solid foundations for subsequent studies worldwide
on the effects of climate fluctuations on marine species. Viewed from this
perspective, his has been a singularly important legacy to marine science.
In addition to his achieving great heights of scientific accomplishment,
Alan, together with Eve, provided much hospitality, humour and support to
the general marine biological community over the years—particularly to
young scientists. The Southwards were always generous and unselfish
collaborators and fine hosts. Alan and Eve were stalwarts at European
Marine Biological Symposia (EMBS) meetings and Alan’s contribution to
conferences was always marvellous: his talks were always stimulating and
Obituary xxiii

scholarly, whilst at the same time being amusing, and his questions and
comments were always helpful and insightful. He was also an outspoken
critic of short-termism in British Science, perhaps stemming from his vision
for the need for long-term observations. Perhaps his breadth of interests also
counted against him, coupled with his plain speaking, but it has been a
surprise to many that there was not more formal recognition of his dis-
coveries and contribution to science other than his honorary Fellowship of
the Linnean Society, in which he took great pride. We all have fond and
amusing memories and much admiration for Alan who was a true gentle-
man of science. He was an inspiration to all that met him and he leaves a
great many friends and a rich scientific legacy.

ACKNOWLEDGEMENTS
We are grateful to many colleagues, and in particular to Gerald Boalch and Paul Dando, for
allowing us to draw on their written accounts of their scientific work with Alan. We also
thank Linda Noble and the staff of the National Marine Biological Library at the MBA for
preparing a full bibliography of Alan’s published work from which the selected references
given here were taken.

REFERENCES
Southward, A. J. (1949). Ciliary mechanisms in Aurelia aurita. Nature 163, 536.
Southward, A. J. (1950). Occurrence of Chthamalus stellatus in the Isle of Man. Nature 165,
408–409.
Southward, A. J. (1951). Distribution of Chthamalus stellatus in the Irish Sea. Nature 167,
410–411.
Southward, A. J., and Crisp, D. J. (1952). Changes in the distribution of the intertidal
barnacles in relation to the environment. Nature 170, 416–417.
Southward, A. J. (1953a). The ecology of some rocky shores in the south of the Isle of Man.
Proc. Trans. Liverpool Biol. Soc. 59, 1–50.
Southward, A. J. (1953b). The fauna of some sandy and muddy shores in the south of the Isle
of Man. Proc. Trans. Liverpool Biol. Soc. 59, 51–71.
Southward, A. J., and Crisp, D. J. (1954). Recent changes in the distribution of the intertidal
barnacles Chthamalus stellatus Poli and Balanus balanoides L. in the British Isles. J. Anim.
Ecol. 23, 163–177.
Southward, A. J. (1955a). Feeding of barnacles. Nature 175, 1124–1125.
Southward, A. J. (1955b). On the behaviour of barnacles. I. The relation of cirral and other
activities to temperature. J. Mar. Biol. Assoc. UK 34, 403–422.
Southward, A. J. (1955c). On the behaviour of barnacles. II. The influence of habitat and
tide-level on cirral activity. J. Mar. Biol. Assoc. UK 34, 423–433.
Southward, A. J., and Crisp, D. J. (1956). Fluctuations in the distribution and abundance of
intertidal barnacles. J. Mar. Biol. Assoc. UK 35, 211–229.
Crisp, D. J., and Southward, A. J. (1958). The distribution of intertidal organisms along the
coasts of the English Channel. J. Mar. Biol. Assoc. UK 37, 157–208.
Southward, A. J. (1958a). Note on the temperature tolerances of some intertidal animals in
relation to environmental temperatures and geographical distribution. J. Mar. Biol. Assoc.
UK 37, 49–66.
xxiv Obituary

Southward, A. J. (1958b). The zonation of plants and animals on rocky sea shores. Biol. Rev.
33, 137–177.
Southward, A. J. (1958c). Abundance of Pogonophora. Nature 182, 272.
Southward, A. J., and Southward, E. C. (1958). Pogonophora from the Atlantic. Nature 181,
1607.
Southward, A. J. (1960). On changes of sea temperature in the English Channel. J. Mar. Biol.
Assoc. UK 39, 449–458.
Southward, A. J. (1963). The distribution of some plankton animals in the English Channel
and approaches. III. Theories about long-term biological changes, including fish. J. Mar.
Biol. Assoc. UK 43, 1–29.
Southward, A. J. (1964a). Limpet grazing and the control of vegetation on rocky shores.
In ‘‘Grazing in terrestrial and marine environments’’ (D. J. Crisp, ed.), pp. 265–273.
British Ecological Society Symposium No.4, Oxford Blackwell Science Publishers.
Southward, A. J. (1964b). On the European species of Chthamalus (Cirripedia). Crustaceana
6, 241–254.
Crisp, D. J., and Southward, A. J. (1964). Effects of the cold winter of 1962–63. South and
South-west coasts. J. Anim. Ecol. 33, 179–183.
Southward, A. J. (1965). Life on the Sea-Shore. p. 153. Heinemann, London.
Southward, A. J. (1967). Recent changes in abundance of intertidal barnacles in South-West
England: a possible effect of climatic deterioration. J. Mar. Biol. Assoc. UK 47, 81–95.
Southward, E. C., and Southward, A. J. (1967). The distribution of Pogonophora in the
Atlantic Ocean. Symp. Zool. Soc. Lond. 19, 145–158.
Southward, A. J., and Southward, E. C. (1968). Uptake and incorporation of labelled glycine
by Pogonophores. Nature 218, 875–876.
Russell, F. S., Southward, A. J., Boalch, G. T., and Butler, E. I. (1971). Changes in
biological conditions in the English Channel off Plymouth during the last half century.
Nature 234, 468–470.
Southward, A. J., and Butler, E. I. (1972). A note on further changes of sea temperature in
the Plymouth area. J. Mar. Biol. Assoc. UK 52, 931–937.
Southward, A. J. (1974). Changes in the plankton community of the western English
Channel. Nature 249, 180–181.
Southward, A. J., Butler, E. I., and Pennycuick, L. (1975). Recent cyclic changes in climate
and in abundance of marine life. Nature 253, 714–717.
Southward, A. J. (1976). On the taxonomic status and distribution of Chthamalus stellatus
(Cirripedia) in the north-east Atlantic region: with a key to the common intertidal
barnacles of Britain. J. Mar. Biol. Assoc. UK 56, 1007–1028.
Southward, A. J., Robinson, S. G., Nicholson, D., and Perry, T. J. (1976). An improved
stereocamera and control system for close-up photography of the fauna of the continental
slope and outer shelf. J. Mar. Biol. Assoc. UK 56, 247–257.
Southward, A. J., and Southward, E. C. (1978). Recolonization of rocky shores in Cornwall
after use of toxic dispersants to clean up the Torrey Canyon spill. J. Fish. Res. Bd. Can.
35, 682–705.
Dando, P. R., and Southward, A. J. (1980). A new species of Chthamalus (Crustacea:
Cirripedia) characterized by enzyme electrophoresis and shell morphology: with a
revision of other species of Chthamalus from the western shores of the Atlantic Ocean.
J. Mar. Biol. Assoc. UK 60, 787–831.
Southward, A. J. (1980). The western English Channel—an inconstant ecosystem? Nature
285, 361–366.
Southward, A. J., and Dixon, D. R. (1980). A note on the free amino acids in some small
species of Pogonophora. J. Mar. Biol. Assoc. UK 60, 171–174.
Southward, A. J. (1981a). Overfishing: is there a solution? Nature 291, 449–450.
Southward, A. J. (1981b). Life on an oily wave. Nature 294, 215–216.
Obituary xxv

Southward, A. J., Southward, E. C., Dando, P. R., Rau, G. H., Felbeck, H., and Flugel, H.
(1981). Bacterial symbionts and low 13C/12C ratios in tissues of Pogonophora indicate
unusual nutrition and metabolism. Nature 293, 616–617.
Dando, P. R., Southward, A. J., and Southward, E. C. (1986). Chemoautotrophic sym-
bionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its
habitat. Proc. R. Soc. B 227, 227–247.
Southward, A. J., Southward, E. C., Dando, P. R., Barrett, R. L., and Ling, R. (1986).
Chemoautotrophic function of bacterial symbionts in small Pogonophora. J. Mar. Biol.
Assoc. UK 66, 415–437.
Spiro, B., Greenwood, P. B., Southward, A. J., and Dando, P. R. (1986). 13C/12C ratios in
marine invertebrates from reducing sediments: confirmation of nutritional importance of
chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 28, 233–240.
Southward, A. J., and Roberts, E. K. (1987). One hundred years of marine research at
Plymouth. J. Mar. Biol. Assoc. UK 67, 465–506.
Southward, A. J., Boalch, G. T., and Maddock, L. (1988). Fluctuations in the herring and
pilchard fisheries of Devon and Cornwall linked to change in climate since the 16th
century. J. Mar. Biol. Assoc. UK 68, 423–445.
Southward, A. J. (1991). Forty years of changes in species composition and population
density of barnacles on a rocky shore near Plymouth. J. Mar. Biol. Assoc. UK 71,
495–513.
Southward, A. J. (1995). The importance of long time-series in understanding the variability
of natural systems. Helgolander Meeresuntersuchungen 49, 329–333.
Southward, A. J., Hawkins, S. J., and Burrows, M. T. (1995). Seventy years’ observations of
changes in distribution and abundance of zooplankton and intertidal organisms in the
western English Channel in relation to rising sea temperature. J. Therm. Biol. 20,
127–155.
Southward, E. C., Gebruk, A., Kennedy, H., Southward, A. J., and Chevaldonne, P. (2001).
Different energy sources for three symbiont-dependent bivalve molluscs at the Lagatchve
hydrothermal site (Mid-Atlantic Ridge). J. Mar. Biol. Assoc. UK 81(4), 655–661.
Gebruk, A. V., Galkin, S. V., Vereshchaka, A. L., Moskalev, L. I., and Southward, A. J.
(1997). Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic
Ridge. Adv. Mar. Biol. 32, 93–144.
Sims, D. W., Genner, M. J., Southward, A. J., and Hawkins, S. J. (2001). Timing of squid
migration reflects North Atlantic climate variability. Proc. R. Soc. B 268, 2607–2611.
Sims, D. W., Wearmouth, V. J., Genner, M. J., Southward, A. J., and Hawkins, S. J. (2004).
Low-temperature-driven early spawning migration in a temperate marine fish. J. Anim.
Ecol. 73, 333–341.
Genner, M. J., Sims, D. W., Wearmouth, V. J., Southall, E. J., Southward, A. J.,
Henderson, P. A., and Hawkins, S. J. (2004). Regional climatic warming drives long-
term community changes of British marine fish. Proc. R. Soc. B 271, 655–661.
Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T.,
Dando, P. R., Genner, M. J., Joint, I., Kendall, M., Halliday, N. C., Harris, R. P.,
Leaper, R., Mieszkowska, N., Pingree, R. D., Richardson, A. J., Sims, D. W., Smith, T.,
Walne, A. W., and Hawkins, S. J. (2005). Long-term oceanographic and ecological
research in the western English Channel. Adv. Mar. Biol. 47, 1–104.
Southward, A. J. (2008). Barnacles: Keys and Notes for the Identification of British Species, p. 140.
Field Studies Council Publications, ShrewsburySyn. British Fauna, New Series Vol. 57.
 C H A P T E R O N E

Maternal Effects in Fish Populations

Bridget S. Green

Contents
1. Introduction 2
1.1. Definition of maternal effects 3
1.2. Maternal effects in fisheries and aquaculture 5
1.3. Scope of review 8
1.4. Fishes and aquatic systems compared to other ecosystems
and taxa 10
1.5. Review overview 10
2. Pathways and Evidence of Maternal Effects 10
2.1. Reproductive mode 11
2.2. Maternal environment 15
2.3. Maternal attributes 34
2.4. Summary of evidence of maternal effects 73
3. Offspring Traits Affected 73
3.1. Response variable selection 79
3.2. Trade-off between offspring size and number 81
3.3. Time course of effects (traits and ontogeny) 81
3.4. Difficulties in studying maternal effects and environment 82
4. Summary 84
Acknowledgements 86
References 86

Abstract
Recently, the importance of the female to population dynamics—especially her
non-genetic contribution to offspring fitness or maternal effect—has received
much attention in studies of a diverse collection of animal and plant taxa. Of
particular interest to fisheries scientists and managers is the role of the demo-
graphic structure of the adult component of fish populations in the formation of
future year classes. Traditionally, fisheries managers tended to assess whole
populations without regard to variation between the individuals within the
population. In doing so, they overlooked the variation in spawning production

Marine Research Laboratory, Tasmanian Fisheries and Aquaculture Institute, University of Tasmania, Private
Bag 49, Tasmania, 7001 Australia

Advances in Marine Biology, Volume 54 # 2008 Elsevier Ltd.

ISSN 0065-2881, DOI: 10.1016/S0065-2881(08)00001-1 All rights reserved.

1
2 Bridget S. Green

between individual females as a source of variation to recruitment magnitude

and fluctuation. Indeed, intensive and/or selective harvesting of larger and
older females, those that may produce more—and higher quality—offspring,
has been implicated in the collapse of a number of important fish stocks. In a
fisheries resource management context, whether capture fisheries or aquacul-
ture, female demographics and inter-female differences warrant serious con-
sideration in developing harvesting and breeding strategies, and in
understanding general population dynamics. Here I review the range of female
traits and environmental conditions females encounter which may influence the
number or quality of their offspring via a maternal effect.

1. Introduction
For almost a century, fisheries biologists have searched for a unifying
theory on recruitment variation and the source of year-class strength in
fisheries populations. Commencing with Hjort in 1914, environmental
factors such as advection and starvation were identified as potential sources
of recruitment variation. A progression of Hjort’s pioneering work sug-
gested a link between egg size, timing of spawning and food availability
(Bagenal, 1971). Numerous advancements on these theories describe vari-
able year-class strength and the dynamics of larval survival as potential
sources of recruitment variation, with each development building on the
theory and evidence from previous hypotheses: match–mismatch (Cushing,
1972), stable oceans (Lasker, 1975), bigger is better (Miller et al., 1988) and
stage-duration (Leggett and Deblois, 1994). Subsequently, predation, com-
petition and larval supply were incorporated into the theoretical framework
(Hoey and McCormick, 2004; Miller et al., 1995; Paris and Cowen, 2004).
The evolution from a population-based, single factor approach to a multi-
variate approach, exploring variations between individuals within a popu-
lation as well as variation between populations has identified numerous
environmental and biotic factors as important sources. Amongst these are
what are commonly referred to as maternal effects, which are the non-
genetic contribution of a female to the phenotype of her offspring. While
the link between size variation of larvae at hatching and strength of recruit-
ment still remains largely theoretical for most populations, it is theory that is
gaining increasing support through laboratory and field experiments
(Bergenius et al., 2002; Meekan and Fortier, 1996; Wright and Gibb,
2005). Though the concept of the value of larger, older or better condition
females to a spawning population has been around since the 1960s
(Nikolskii, 1962), this field of study has only developed and entered
Maternal Effects in Fish Populations 3

mainstream fisheries science in recent years. To advance the field, streamline

ideas and synthesise the importance of maternal effects on offspring varia-
tion—these advancements require further collation of the most up-to-date
findings. The purpose of this paper is to fill this need by reviewing the
occurrence of maternal effects in fish populations.

1.1. Definition of maternal effects

‘Maternal effects’ has multiple definitions, uses and misuses, and the most
appropriate depends on the context in which it is used. The definitions of
maternal effects that are the broadest and most applicable to this review are
that maternal effects are the non-genetic contribution of the female to
offspring condition (Reznick, 1991); or any influence of the parent on
offspring, not caused by shared DNA (Reinhold, 2002); or phenotypic
variation in offspring that is a consequence of the mother’s phenotype rather
than the genetic constitution of the offspring (Roff, 1998). The broadest
misuse of the term occurs when offspring variation is attributed to any trait
of the female without accounting for maternal genetics. Such variation
would be more precisely referred to as ‘female influence’, which does not
imply a separation of genetic and non-genetic effects. See Box 1.1 for
further definitions to be used throughout this review.
The non-genetic sources of variation in offspring can be from either parent,
but as it is the female that provisions the egg with nutrients, hormones and
cytoplasm and generally chooses where to deposit them, she is a more likely
Box 1.1 Glossary of terms used

Additive genetic variance: Phenotypic variance due to different

genotypes, and is the numerator in the heritability ratio.
Broad-sense heritability: The proportion of total phenotypic
variability (H2) due to all genetic effects. The sum of additive variance
þ dominance variance þ epistatic variance is the total genetic variance
and heritability in the broad sense is the ratio Genetic variance/pheno-
typic variance.
Dam: Female parent.
Ecological fallacy: Inferences about the nature of individuals are
based solely upon aggregate statistics collected for the group to which
those individuals belong.
Gametogenesis: Gametogenesis is the production of haploid gametes
by diploid multicellular organisms through the process of meiosis.
Gonochoristic: In a sexually reproducing species where there are at
least two distinct sexes.
4 Bridget S. Green

Box 1.1 (continued )

Heterosis: The biological phenomenon in which an F1 hybrid of two

genetically dissimilar parents shows increased vigor at least over the
mid-parent value (P1+P2/2). Maternal effects are a type of heterosis.
Heritability: Additive genetic variance/phenotypic variance. Herita-
bility is a ratio that describes the amount of phenotypic variation that
can be attributed to the differences in the ‘additive genetic merit’ of
individuals in a population. Differences in additive genetic merit exist if
individuals have different alleles at loci that contribute to measurable
differences in performance. So, to understand heritability, one must first
understand additive genetic merit.
Iteroparity: The repeated production of offspring throughout the life
cycle.
Maternal effects: Phenotypic variation in offspring, that is a conse-
quence of the mother’s phenotype rather than the genetic constitution
of the offspring (Roff, 1998), inherited environmental effects.
Maternal influence: An effect derived from the female that may be
genetic or phenotypic.
Matrotrophy: Provisioning of young with nutrients in excess of those
supplied through the yolk.
Narrow-sense heritability: The proportion of phenotypic variance
that can be attributed to additive genetic variance.
Oogenesis: The production of female gametes (ova).
Oocyte: A female germ cell in the process of developing. Oocytes give
rise to the ovum or egg.
Oviparity: Expulsion of underdeveloped eggs rather than live young.
Oviviparity: The eggs are hatched in the oviduct of the female. The
embryos develop in the uterus until fully grown.
Phenotypic plasticity: The different phenotypic expressions of a
genotype in response to ranging environmental conditions.
Quantitative genetics: The quantification of inherited continuous
traits responsible for phenotypic differences.
Reaction norm: The range of phenotypes an organism can express in
response to environmental variation (Riska, 1991).
Semelparity: A single reproductive season before death, also referred
as ‘big bang’ reproduction.
Sequential hermaphrodite: Where a single organism can be sexually
functional as a male and as a female, and the expression (primary and
secondary sexual characteristics) and function of one gender is followed
by the other, that is, both sexes do not operate at the same time.
Maternal Effects in Fish Populations 5

Sire: Male parent.

Trait: A measurable quality or characteristic.
Transgenerational adaptive plasticity: If the parental environment
is predictive of future environment, then it is advantageous to produce
offspring adapted to the environment in which they are reared
(Mousseau and Fox, 1998); females use current environmental cues to
adjust their offspring investment to future environmental conditions
and is a strategy to increase offspring fitness (Plaistow et al., 2004).
Vitellogenesis: The process of yolk deposition, the process of nutri-
ents being deposited into the oocytes—usually initiated after the first
meiotic division.
Viviparity: The embryo is nourished inside of the female by a placenta,
and females give birth to live young.

source of variation, at least in the initial stages. The bulk of this review will focus
on the female component of non-genetic input into offspring variation. The
male influence will be only briefly discussed in this review (see Section 2.2.7).

1.2. Maternal effects in fisheries and aquaculture

1.2.1. Fisheries
Traditionally, fisheries managers tended to assess whole population dynamics
without regard to variation between the individuals within the population. In
doing so, they overlooked females, and more so, the variation in spawning
production between individual females, as a source of variation to recruit-
ment magnitude and fluctuation. There is now consensus in management of
many heavily exploited stocks—though not yet universally incorporated into
broad-scale fisheries modelling—that spawning stocks are not single entities
with respect to sizes, but are composed of individuals of a range of sizes and
ages that may contribute differently to spawning and recruitment (Marshall
et al., 1998; Marteinsdottir and Thorarinsson, 1998; Scott et al., 1999).
In this review, the argument will be explored that the variation in attributes
of quality between individuals is critical to consider in the stock recruitment
relationship (Scott et al., 1999; Vallin and Nissling, 2000). Traditional models
assume that egg production is directly related to spawner biomass or spawning
stock biomass (SSB) when considered across a whole population and the two
factors are interchangeable in predictive models. The resulting assumption is
that many small individuals will produce as many offspring as a few large
individuals. Where this is not true, models of stock productivity, and the
subsequent fisheries management decisions, may critically underestimate the
contribution of different female size classes to recruitment variation in fish
stocks. In reality, when individual stocks are assessed, spawner biomass is often
6 Bridget S. Green

not related to total egg production (Marshall et al., 1998). To quote Marshall
et al. (2003), ‘The lack of proportionality between SSB [spawning stock
biomass] and egg production means that biomass reference points should be
regarded as being inherently uncertain’ (p. 185). Given isometric scaling laws,
which purport that volume = length3, a female’s capacity to store eggs increases
as a cube of her body length. Longer females theoretically can produce signifi-
cantly more eggs than shorter females. In fact, some fishes have a greater
reproductive capacity than ascribed even by these body-size scaling laws.
In Atlantic cod, Gadus morhua, the smallest fish can produce approximately
300 eggs g1 compared with large cod which can produce approximately 500
eggs g1 (Marshall et al., 1998). The inclusion of size, quality and quantity of
spawners in a fisheries population or stock would lead to more accurate SSB
estimates. Furthermore, the influence of these factors on offspring quality and
the manner in which this feeds into year-class strength need to be incorporated
into a basic stock assessment.
Maternal effects are a major source of phenotypic variation within a
population. Numerous studies have described how a truncation of the age
or size of a fishing population can directly affect the quality of offspring and
recruitment (Longhurst, 2002; Scott et al., 2006), and many have inferred an
effect (Berkeley et al., 2004a). If there was generality in the influence of a
maternal effect on recruitment, then maternal effects would be a key
pathway through which fisheries regulation could manage recruitment
mechanisms (Solemdal, 1997). For maternal effects to be usefully
incorporated in to stock–recruitment (S/R) relationships there must be a
strong and consistent or at least predictable relationship between offspring
quality and attributes of the parent within a species, and this relationship
would become more effective if it existed between species (Ouellet et al.,
2001) or higher level taxonomic or life history grouping. This review will
examine some of the generalities published as maternal effects.
When variation in reproductive output between females is incorporated
into estimates of SSB, accurately predicting recruitment or year-class strength
is difficult because of high variability and uncertainty in the relationship
between the numbers of eggs spawned and juveniles surviving to recruit
(Marshall et al., 2003). This relationship between egg quality and offspring
survival is moderated by environmental conditions. Quantifying recruitment
variation due to maternal effects is potentially very important in estimating
recruitment from SSB if larger or more experienced fish produce more viable
offspring with higher likelihood of surviving a range of environmental con-
ditions. While there are instances where a relationship between SSB or S/R
relationships and the number of eggs produced has been demonstrated
through meta-analysis (Myers and Barrowman, 1996), there is so much
uncertainty in most fisheries models that many attempts to manage stocks
have failed, resulting in further stock declines, or reduction in age and size
classes (Pauly et al., 2002). The most common explanation for a lack of S/R
Maternal Effects in Fish Populations 7

relationship is high mortality in the larval period, estimated at 99.9% (Ferron

and Leggett, 1994). If selectivity of larval mortality could be estimated via
assessment of female quality then better estimates of the S/R relationships
may result. Recruitment models which incorporate female traits such as
variable SSB between years, egg production, and amount of liver lipid are
better predictors of recruitment variation than models that simply rely on SSB
(Marshall et al., 2003). Although a maternal component was stipulated in one
of the early models predicting a relationship between SSB and egg production
(Beverton and Holt, 1957), for example, ‘survival of fry hatched from large
eggs may be better than from small ones’, this caveat was generally over-
looked for the following four decades.
As fishing pressure increases, and the large end of the size distribution of a
targeted population is depleted,1 the relative contribution of each female size
class to spawning output shifts also. Smaller females contribute proportionally
more to stock spawning output under this scenario. While a decrease in size and
age at maturity are common responses to increased fishing pressure, this is
unlikely to compensate for the contribution of larger or higher quality females.

1.2.2. Aquaculture
The importance of female size and other attributes of female quality on the
production of offspring also have implications for another aquatic harvest,
the aquaculture industry, where fish are cultured in artificial systems rather
than harvested from wild populations. As this industry is based on the
production of stock in captivity to supply the food fish requirements of
growing human populations, optimising production and streamlining effort
is the primary goal of most farms. Reproductive output per unit of female
fish is probably the most critical performance measure in this industry, and
consequently the main goal of aquaculturists, as with most animal and plant-
breeders, is to improve the performance of their production stock, in terms
of growth, vigour, disease resistance or environmental tolerance (Lutz,
1997). Traditional aquaculture used selective breeding to select from desir-
able phenotypes, and even with current genetic engineering, the perfor-
mance of the fish is governed by its genetic potential and immediate
environmental conditions (Pickering, 1993). The potential for larger
females to produce better quality and more numerous offspring has focused
research attention onto the identification of maternal effects on a few key
aquaculture species, for example, Atlantic salmon (Refstie and Steine,
1978), rainbow trout (Nagler et al., 2000; Refstie, 1980) and rabbitfish
(Ayson and Lam, 1993) for which there is high quality information.

1
This truncation of larger fish is typical of traditional industrial fishing practices, however, this is changing as
the demographic of export markets shifts and many fisheries supply the Asian market which pays premium
price for plate-sized fish.
8 Bridget S. Green

The existence of maternal effects can have both positive and negative
implications for the aquaculture industry. By enhancing a female’s environ-
ment, production in terms of numbers and quality can be enhanced.
Development of fish stocks with enhanced resistance to commonly encoun-
tered fish pathogens would be highly advantageous ( Johnson et al., 2003).
The disadvantages are that when tailoring a breeding programme to
enhance specific genetic traits, or increase heterosis (see Box 1.1 for defini-
tions), the variation due to maternal effects can interfere with the phenotype
under selection (Falconer, 1981). It is in selective breeding programmes that
maternal effects were first seen as experimental noise (Falconer, 1981).
Aquaculture studies more commonly partition sire and dam components
of variance in offspring traits (Blanc et al., 2005) in attempts to maximise
production and therefore offer a more rigorous approach to the study of
maternal effects. However, the results from studies of maternal effects in
aquaculture are not always directly applicable to natural resource manage-
ment as, for instance, the hatchery environment reduces initial size differ-
ences (Einum and Fleming, 1999).

1.3. Scope of review

Previously, maternal effects have been viewed in many different ways
including as experimental noise (Falconer, 1981), genetic divergence
(Hendry, 2001) and natural variation (Heath and Blouw, 1998), and as
phenotypic plasticity to deal with a variable environment and local adapta-
tion of characters (Mousseau and Fox, 1998). Each approach confers a
slightly different perspective on how maternal effects operate both within
the confines of a genotype and the environment. One of the difficulties in
producing this review was to contain the content to a manageable amount
without excluding themes, papers or species of central importance to the
overall understanding of how maternal effects might operate in fishes. Each
component of maternal effects reviewed has lead to annals on related topics,
which could not be included. For instance, I only briefly review the trade-
off between egg size and number (see Section 3.2), as this topic is compre-
hensively reviewed elsewhere (Hendry et al., 2001; Smith and Fretwell,
1974; Stearns and Koella, 1986). The present review focuses mainly on fish
and any kind of maternal influence where there is a direct link between
mothers and offspring, and it refers back to many other organisms that lend
themselves to experimental manipulation and therefore offer a comprehensive
approach to partitioning out variance due to maternal effects.
There are many female-offspring relationships that have been described
under the general catalogue of ‘maternal effects’ particularly in the fish and
fisheries literature, however many do not strictly adhere to the definition of
maternal effects adopted here, but rather should be considered maternal
Maternal Effects in Fish Populations 9

influences. Disentangling these female influences from true maternal effects

is a laborious task, which can often only be achieved experimentally. This
looser description of female influences encompasses any relationship
between the female and her offspring, including those that are genetic, or
specifically related to the size and/or age of a female and are therefore a by-
product of stage-specific growth rather than an effect of the maternal
environment directly on offspring phenotypic plasticity. In terms of a fish-
eries population, female age and/or size and the looser definition of ‘female
influence’ are equally as important sources of variation to offspring traits as
are the more traditional and tightly defined ‘maternal effects’. The results are
still pertinent to understanding the source of phenotypic variation in young
fishes that might lead to recruitment variability in wild fisheries or different
phenotypes (performance measures) in an aquaculture setting. This review
will provide an overview of both maternal effects and influences.
Studies of maternal effects and the broader maternal influences in fishes
have addressed a few key hypotheses and generalities including
1. Size of female is related to the number of eggs produced and therefore
will affect reproductive potential (Marshall et al., 1998).
2. Qualitative changes in eggs and larvae are due to age and size variation in
female (Solemdal, 1997).
3. Size of egg is related to size of hatchling (Chambers et al., 1989).
4. There is a ‘broad brush’ of relationship between recruitment and quality
and number of female within a population (i.e., stock level correlation
recruitment dynamics).
5. There is a trade-off between the egg size and number, and a general
increase in one results in a decrease in the other (Hendry et al., 2001;
Smith and Fretwell, 1974).
These generalities are not universal in fishes and exceptions will be
discussed throughout this review.
One general thesis to arise from the study of maternal effects in other
organisms, both plant and animals, is that bigger females produce better
quality and/or more abundant offspring, and therefore size and age variation
in parent fishes increases variation in offspring traits that are important to
recruitment. While there are exceptions to this general trend, it is generally
well-supported in the fields of quantitative genetic analysis, plant-breeding
and avian population biology. This literature will be referred to throughout
this review to provide context for the fish, fisheries and aquaculture exam-
ples. In marine systems I have not yet encountered a single example where
the influence of female size has been tracked from parent sources to the
success of the next generation in wild populations. The focus of this review
will be on the early life stages of fishes as this is when maternal effects are
expected to be most evident due to the nature of their transmission.
10 Bridget S. Green

1.4. Fishes and aquatic systems compared to other

ecosystems and taxa
Fishes and aquatic ecosystems have many unique features compared with other
ecosystems and taxa that influence how maternal effects are manifested and
consequently interpreted. Fishes are epitomised by their diversity in morphol-
ogy, habitat associations, reproductive and general biology. Of the vertebrates,
fishes are the most abundant and speciose group, comprising an estimated
24,000 species (Nelson, 1994), and they show the widest variety of adaptive
responses to their environment. They are unique amongst the vertebrates in
having indeterminate growth. Furthermore, they have the most diverse range
of reproductive strategies of the vertebrates, demonstrating every kind of
reproductive strategy that occurs in vertebrates (outlined in Table 1.4,
Section 2.1 and also in Berglund, 1997). Numerous species within the Perci-
formes are sequential hermaphrodites, another unique feature among the
vertebrates. Fishes have colonised a large range of habitats spanning a 46  C
temperature range, and from 3812 m above sea level to 7000 m below it, and a
range of salinities from 0 to 35% (Nelson, 1976). A pelagic larval phase found
in most teleosts, coupled with small size and often cryptic appearance of the
larvae, make it difficult to close the link between maternal quality and
condition and the strength of recruitment. Due to the diversity in both fish
reproduction and ecosystem usage, no single approach can characterise popu-
lation biology. In general, fish reproduction is more similar to invertebrates
such as insects, characterised by the release of thousands of gametes, most of
which will die in the very early stages. Unlike insects though, there are many
limitations in breeding fishes because of the requirement for an aquatic
environment and the large proportional change in size in the early life stages.

1.5. Review overview

The purpose of this present review is to describe the range of sources,
responses and expressions of maternal effect described in fishes. Firstly, the
evidence of maternal effects associated with the maternal environment will
be described; secondly, the evidence of maternal effects and their link to
maternal attributes; thirdly, the traits affected, time course of effects, and
patterns of expression of maternal effects will be summarised; and finally I
will synthesise information about when maternal effects would be most
likely to occur and review the difficulty in studying maternal effects in
fishes, with suggestions as to why maternal effects may not be detected.

2. Pathways and Evidence of Maternal Effects

Maternal effects occur in a wide range of fishes and are expressed in a
variety of offspring traits. The identification of maternal effects and their
pathways varies across species and within species (e.g., see discussion on cod,
Maternal Effects in Fish Populations 11

G. morhua; Ouellet et al., 2001). There are many pathways through which a
female’s phenotype can influence the phenotype of her offspring. Some of
these pathways are unique to fishes while others either do not occur or have
not been examined in fishes. Pathways include female physiology, timing of
spawning within a season, egg provisioning, cytoplasmic inheritance, egg
composition (hormones; McCormick, 1999), toxins (Hammerschmidt
et al., 1999), carotenoids, for example, birds (Blount et al., 2003), and
immunoglobin, for example, birds (Gasparini et al., 2001, cited in
Gorman and Nager, 2004), incubation temperature (birds, citations in
Gorman and Nager, 2004), and behaviour, including spawning and nesting
site choice, and parental care. The latter also includes post-hatching parental
feeding, as displayed in many mammals and birds, which is also a pathway
for a paternal effect in brooding fish with paternal care (Green and
McCormick, 2005b).

2.1. Reproductive mode

The reproductive mode of a fish will influence the pathway of maternal
effects, and the amount of variability in offspring traits. Of the vertebrates,
fish have the widest variety of reproductive strategies, and uniquely, they
exhibit all of the known vertebrate reproductive modes. Reproductive
modes in fishes include: internal or external fertilisation; broadcast or
substrate spawning; oviparity, oviviparity and viviparity; matrotrophy,
semelparity and iteroparity; and parental care or no parental care
(Table 1.1; see Box 1.1 for definitions). Reproduction in any species will
include a combination of these components. For example, guppies (Poecilia
reticulata) have internal fertilisation, are viviparous and semelparous; Atlantic
salmon (Salmo salar) have external fertilisation, ovivipary, and spawn on the
substrate with no parental care; and Atlantic cod (G. morhua) are broadcast
spawners with external fertilisation and no parental care. The diversity and
possible permutations of reproductive strategies in fishes makes the study of
maternal effects in fishes both complex and multifarious.
Within these reproductive strategies are also differences in the level of
female investment to each clutch relative to lifetime fecundity. Some
fishes, for example, Pacific salmon (genus Oncorhynchus, including chi-
nook, chum, coho, pink and sockeye salmon), invest everything in to
one pre-terminal reproductive bout (referred to as semelparity). They
migrate as far as 1600 km to their natal stream to lay eggs in the gravel,
allowing fertilisation by multiple males. Another strategy is to reproduce
only once per year, but over multiple years in a lifetime (iteroparity). For
example, winter flounder, Pseudopleuronectes americanus, migrate from deep
offshore waters to shallow inshore estuarine areas and pair-spawn to
produce negatively buoyant adhesive eggs in mid-winter. Other fish
‘hedge their bets’ (bet-hedging) by reproducing repeatedly on a daily,
Table 1.1 Summary of the range of reproductive features found in fishes

Life history feature Feature sub-category

Reproductive mode (sp) External fertilisation
Internal fertilisation
Parity (sp) Ovipary
Ovivipary
Vivipary
Spawning frequency (sp) Semelparous
Iteroparous
Spawning periodicity (sp) Single batch
Multiple batches
Seasonality of spawning (sp) Winter
Spring-summer
Fall
Aseasonal
Timing of spawning (ind) Early season
Mid season
Late season
Lunar
Duration of spawning (ind) <1 d
Multiple days
Location of spawning (sp) Pelagic, open water
Benthic
Inshore
Reef crest (fish spawn on edge of reef
into water column in big currents)
Mating behaviour (sp) Group spawning
Paired spawning
Harem
Attribute of eggs (sp) Broadcast, separate, buoyant
Attributes of egg placement (sp) Broadcast, grouped, buoyant
Negatively buoyant
Adhesive
Benthic attached
Maternal care (sp) Nest building, tending
Mouth brooding
Feeding of offspring
Defense of offspring
Offspring disinfection
Paternal care Mouth brooding
Pouch brooding
One age class versus multiple
age classes
Allocation of parental products
Dispersal of offspring Dispersive
Non-dispersive
sp ¼ expressed across the species; ind ¼ varies among individuals.
Maternal Effects in Fish Populations 13

weekly, monthly or lunar cycle within a breeding season (usually season-

ally defined) and over multiple years throughout their lifetime (repeat
iteroparity). For example, coral trout Plectropomus leopardus are protogy-
nous sequential hermaphrodites that spawn in groups after aggregating,
releasing positively buoyant pelagic eggs 3–4 nights on a new moon for
3–4 summer months (Samoilys, 1997). The duration and frequency of
gamete release differs in each of these strategies, resulting in opportunities
for the expression of maternal effects over a range of scales: within and
between batches (Chambers and Waiwood, 1996), season (Rideout et al.,
2005b) and years (Manning and Crim, 1998). Changes in gender in the
case of sequential hermaphrodites, and age and size with time, can result in
further differences in the expression of maternal effects within an individ-
ual fish. The likelihood that a female trait such as body size influences the
quality of the egg incubation environment depends on the type of repro-
ductive behaviour and the level of female involvement. Different levels of
female investment provide a range of opportunities for environmental
influences to affect the quality of gametes the female produces. Demersally
spawning fishes are expected to exhibit more variation in offspring traits as
the selection of spawning and larval habitat are influenced by the maternal
phenotype (Einum and Fleming, 2002; Hendry et al., 2001), offering more
pathways for a maternal influence or effect. Hendry et al. (2001) predicted
a gradient of the expression of maternal effects in Canadian freshwater
fishes according to reproductive investment, and found relationships
occurred between egg size and female size in fishes with the most active
role in nest site selection and egg care. The authors concluded that in an
environment where oxygen (or another critical environmental variable) is
limiting for the propagules, being of a large size for the female could be an
advantage in gaining the best territories, tending the nest and choosing
these same qualities in a mate.

2.1.1. Intervention to eggs or clutches to assess maternal effects

There are three commonly used tools in manipulating eggs or clutches to
partition out the effects of genes, environment, parental care and maternal
effects. These include food supplements to the female, cross-fostering, egg
or nest manipulation. Food supplementation has been covered in the
section on prey abundance and quality (Section 2.2.5). Here, I will briefly
discuss techniques used for manipulating eggs and nests.

2.1.1.1. Egg manipulation When the life cycle of the study organism is
too long to allow for controlled genetic crossing to explicitly isolate mater-
nal effects from genetic influences, techniques such as egg manipulation may
be useful (reviewed by Bernardo, 1991). Micro-manipulating yolk quan-
tities is a tool to alter maternal allocation without interfering with the
genetic bequest, and can partition out the pathways for maternal allocation
14 Bridget S. Green

and the resulting trade-off in egg size and number. This technique was
pioneered in lizards and has been coined ‘allometric engineering’ (Sinervo,
1990; Sinervo and Huey, 1990). Egg manipulation allows for the detection
of co-varying factors that would remain undetected in typical correlative
studies. These are difficult to perform in fishes as expertise in microsurgery is
required to penetrate the chorion and remove measured aliquots of yolk
without disrupting developmental processes; however, it has been success-
fully employed in a few species. Yolk-reduced eggs generally produce
smaller hatchlings in zebrafish Danio rerio ( Jardine and Litvak, 2003), her-
ring Clupea harengus (Morley et al., 1999) and lizards (Sinervo, 1990; Sinervo
and Huey, 1990); in the case of the lizard, yolk reduced eggs also resulted in
a reduced sprint speed in hatchlings (Sinervo, 1990; Sinervo and Huey,
1990). The reduction in yolk is designed to duplicate reduced maternal
aliquot to the egg.
Egg size can also be manipulated indirectly, by manipulating the size of the
follicles during vitellogenesis. Again in lizards, large eggs were produced when
the number of follicles is reduced, and conversely when extra follicle growth
was stimulated, smaller eggs were produced (Sinervo and Licht, 1991).
Hormonal injection of female spawners can influence allocation to eggs.
Larvae from female rabbitfish (Signaus guttatus) injected with thyroxine (T4)
were longer and higher survival compared to larvae from sham-injected
females (Ayson and Lam, 1993). Post-fertilisation exposure of eggs to
cortisol in a tropical damselfish Pomacentrus amboinensis resulted in shorter
larvae, and exposure to testosterone decreased yolk utilisation rate
(McCormick, 1999). All three kinds of manipulations serve as surrogates
for partitioning maternal effects on offspring from genetic effects, by using
controlled testing to measure relationships such as egg aliquot and larval size,
and hormone profiles and offspring size, without variation in maternal
genetics.

2.1.1.2. Nest manipulations: Cross-fostering In animals with nest-care,

the care the offspring receive whilst in the nest can introduce phenotypic
variation through the quality of parental care, or the incubation environ-
ment (Green et al., 2006). This source of parental effects can be separated
from pre-oviposition parental effects through cross-fostering. Cross-foster-
ing involves switching eggs or clutches of eggs from the natal parents to
another set of nesting parents to provide incubation. Cross-fostering has
been successfully used in birds (Gorman and Nager, 2004; Saino et al.,
2002a) and reptiles (Crespi and Lessig, 2004). Fishes tend not to accept
step-parenthood as readily, and will cannibalise cross-fostered young
(Amphiprion melanopus, Green, personal observation; Gasterosteus aculeatus,
Frommen et al., 2007). This technique needs development before it is a
useful tool for partitioning maternal effects in fishes.
Maternal Effects in Fish Populations 15

2.2. Maternal environment

One of the broader definitions of maternal effects, as ‘inherited environ-
mental variation’, includes the maternal environment as an integral source
of maternal effects. There are multiple pathways through which the envi-
ronment can influence maternally mediated offspring traits. Firstly, the
environment can act directly on the female and influence her condition
or physiology during oogenesis, which then acts to influence propagule
condition. Secondly, the environment can act directly on the eggs in
the female-selected nesting location. Finally, maternally mediated offspring
traits can interact with the offspring’s environment, after it is liberated from
the female. Environmental factors fluctuate daily, seasonally and randomly,
and all types of environmental shift have the potential to influence maternal
and offspring condition.
The physical parameters of aquatic environments differ markedly from
terrestrial environments. Oxygen is rarely limiting in terrestrial environments;
however, due to low solubility of oxygen in water (water contains 0.03% of
the amount of oxygen in air), it can be limiting in aquatic systems, particularly
in shallow, still freshwater and lentic habitats (discussed in Wootton, 1990). In
contrast, the dramatic temperature fluctuations that shape some terrestrial
environments are rare in aquatic habitats as water acts as a thermal buffer
reducing the extremes. Nevertheless, temperature does fluctuate on a diel and
annual basis in aquatic environments, and can interact with a maternal effect
to influence offspring quality (e.g., anemonefish, Green and McCormick,
2005a). Fishes contend with these and other variables including predator
fields, contamination, flow regimes, salinity and temperature gradients, stress
from competitors and complex habitat structure.
Environmental parameters unique to the aquatic environment influence
spawning and mating behaviour as well as quality of nest or egg release
environment, all of which can be sources of maternal effects. Flow regime
can influence oviposition choice, pertinent in substrate-laying species like
salmon whereby a high flow can wash eggs away and low flow can restrict the
amount of oxygen available to the eggs (Hendry et al., 2001). The number of
ideal egg incubating environments is limited in some aquatic systems, and so
female size and experience can increase their ability to access the best spawn-
ing habitat. Water turbidity influences mate choice in gobies by reducing
visibility and assessment of potential mates which can lead to a reduction in
offspring quality (Jarvenpaa and Lindstrom, 2004; Seehausen et al., 1997).
The maternal environment can affect offspring traits via its effect on the
physiology of the female. For example, if the female is exposed to a toxic
environment then often this toxicity is passed directly onto the offspring
through the cytoplasm. An environment that is socially stressful to the
female through aggressive encounters with conspecifics can increase her
cortisol levels which can act to reduce the size of larvae at hatching, as has
16 Bridget S. Green

been shown for fish (McCormick, 2006) and birds (Saino et al., 2005), and
can bias the sex ratio of offspring in the case of birds (Love et al., 2005).
There are also indirect effects of the maternal environment. Ideal propa-
gule size and subsequent survival will vary with the environment the propa-
gule encounters. Growth advantages at hatching may be transient or may
even be negative in a harsh environment. In salamanders, larvae from large
eggs had a survival advantage in ponds with constant water level, but were at a
disadvantage in seasonally drying ponds (Semlitsch and Gibbons, 1990).

2.2.1. Location of spawning

Spawning site location acts as habitat for developing embryos in benthic
spawning species (Blanchfield and Ridgway, 2005), and provides entry into
circulation patterns critical for transport to suitable recruitment sites in
pelagic spawning species (Paris et al., 2005). Whether the fish is a benthic
or pelagic spawner, the parental choice of spawning site can be critical to the
initial survival of the offspring. Larval transport pathways from spawning
aggregation sites can be a critical link in recruitment magnitude (Paris et al.,
2005). Within a population, herring (C. harengus) spawning site selection is
critical to larval retention and subsequent year class strength (Iles and
Sinclair, 1982). There is some evidence of spawning ground location
influencing growth in Atlantic salmon, as size and age at first spawning
increase with the distance to spawning grounds and river harshness (Schaffer
and Elson, 1975). A more detailed discussion on nest-site selection for
benthic spawning fishes is given in Section 2.3.6.2.

2.2.2. Season of spawning

Seasonal environmental changes characterise high latitude and temperate
aquatic ecosystems, and within these ecosystems, most organisms reproduce
seasonally (Bye, 1990). The length of the breeding season varies within
species along latitudinal gradients (e.g., Fundulus heteroclitus, Schultz et al.,
1996); with age of the individuals (e.g., Atlantic cod, G. morhua, Comeau
et al., 2002) and between species. In a number of species that show a seasonal
migration to spawning grounds, larger, older females arrive first (and in
territorial species gain access to the best territories), for example, brook
trout, Salvelinus fontinalis (Blanchfield and Ridgway, 2005), and spawn first.
Early spawning within a season can provide an extended growing season to
the offspring, and greater access to seasonal food production.
Within individual females, seasonal changes may influence egg quality
during oogenesis. Many iteroparous fishes show a change in the quality or
quantity of eggs produced throughout a spawning season, generally related to
the water temperature, or depletion of female reserves. Chambers (1997) offers a
broader discussion of seasonal trends in variation of offspring traits, particularly
egg size, and rather than repeat the discussion from that volume, I will
report on the main trends that were described. Spring/summer spawning
Maternal Effects in Fish Populations 17

species (referred to as spring spawners) have smaller eggs than autumn/winter

spawners. For many serial spawners (spring spawners), the egg diameter tapers
off as the spawning season advances, for example, haddock Melanogrammus
aeglefinus (Rideout et al., 2005b; Trippel and Neil, 2004), walleye Pollock
Theragra chalcogramma (Hinckley, 1990), turbot Scopthalmus maximus (McEvoy
and McEvoy, 1991), Atlantic cod G. morhua (Chambers and Waiwood, 1996;
Kjesbu, 1989; Ouellet et al., 2001; Trippel, 1998) and goby Pomatoschistus
marmoratus (Mazzoldi et al., 2002). The reverse pattern has been noted
for autumn spawning species, where the eggs increase in size during the
spawning season (Chambers, 1997). The general synthesis of these patterns,
including species that spawn all year-round, is the smaller eggs are produced late
spring through summer when temperatures are relatively warm, and larger eggs
are produced in late autumn through winter when waters are colder (Chambers,
1997). There are exceptions to this general trend, for example, silverside
(Menidia menidia) unfertilised egg diameter was not different between eggs
spawned early or late in the season; however, lower incubation temp caused
significantly greater length at hatching (Bengston et al., 1987).
Other seasonal changes include a within-season change in offspring sex-
ratio, which appears to be maternally determined, for example, male bias
early in breeding season for frog (Sakisaka et al., 2000), and female bias early
in breeding season for fish, M. menidia (Conover, 1984). A seasonal decline
in the size of larval morphological traits, including standard length, myo-
tome height, eye diameter, jaw length, yolk area and finfold area occurred
from early to mid to late season, and survival was reduced late in the season
at low food levels (haddock M. aeglefinus, Rideout et al., 2005b).

2.2.3. Temperature
Temperature fluctuations in aquatic environments are generally less than
those in terrestrial systems because the large heat capacity of water acts as a
thermal buffer; however, temperature still varies on both temporal (e.g.,
daily, seasonal) and spatial scales in aquatic systems. Temperature determines
the rate of metabolism and growth in ectotherms such as fish, and can
modify the trajectory of development in early life history stages. It is one
of the most commonly studied environmental parameters affecting mater-
nally mediated traits in aquatic ectotherms, and can affect offspring traits
though a number of mechanisms. Temperature can directly influence
female metabolism during oogenesis, vitellogenesis or pregnancy, and
once offspring are liberated from the females, the temperature they experi-
ence in the maternally selected environment can further influence pheno-
typic traits (e.g., rotifers Synchaeta pectinata, Stelzer, 2002). Temperature
experienced by the offspring interacts with maternal effects and influences
a range of offspring traits in ectotherms, including growth (A. melanopus, Green
and McCormick, 2005a), gender (M. menidia, Conover, 1984), performance,
such as swimming ability (A. melanopus, Green and Fisher, 2004), survival
18 Bridget S. Green

(A. melanopus Green and McCormick, 2005a), time to hatch (Oncorhynchus

tshawytscha, Heath et al., 1993) and size at hatching (Pleuronectes ferrugineus,
Benoit and Pepin, 1999).
The complexity of the ‘maternal effects’–‘environmental temperature’
relationship is demonstrated in a range of taxa, the eggs of many of which
are generally easier to raise and manipulate in large numbers than for fish. For
most of the experiments described below it would be difficult to replicate the
scale of experimentation on fish. Embryonic survival, age and size at hatching
of the offspring of frogs (Rana temporaria) collected from a range of latitudes
and raised in a half-sibling design with varying temperatures were strongly
affected by an interaction of maternal effects and temperature, whereby frog
embryos from different populations differed in developmental time, not
linearly related to temperature (Laugen et al., 2003a). In a very different
ectotherm taxa, the rotifer, temperature of the maternal environment directly
and considerably affected offspring size through differential maternal alloca-
tion, an effect which snowballed until adult size was reached (Stelzer, 2002).
Rotifers are an ideal model for partitioning out maternal and environmental
effects as they can be bred to reproduce only parthenogenically, thereby
removing the effects of cross breeding (Stelzer, 2002). Temperature may
interact with a large range of female traits to influence offspring, eliciting
sometimes subtle responses, for example, female temperature environment
interacted with the number of mates and influenced egg viability in dung flies
(Tregenza et al., 2003). In squid, temperature was not an important influence
on number of eggs, survival or lipid content in eggs, whereas female
ration had highly significant effects on these measures of offspring quality
(Steer et al., 2004).
In fishes, the effect of temperature on maternally mediated offspring
traits varies considerably between species and with latitude, and there are
large differences in seasonal temperature range with latitude. Tropical and
temperate examples are provided separately here, but as phylogenetic dif-
ferences have not been addressed, an overall difference in the response of
animals from these ecosystems is not implied.
An apparent time-lag between an environmental temperature and the
expression of its influence on offspring through maternal effects depends on
the duration of oogenesis and vitellogenesis, which can occur over many
months in fishes depending on their reproductive strategy. In fishes with
determinate fecundity, where egg production is set before the spawning
season (predominantly a trait of temperate latitude fish), environmental
conditions prior to the spawning season influence female fecundity and
egg size. Warm temperature experienced by herring (Clupea sp.) 60–90 days
before spawning led to a trade-off between egg size and number, resulting
in the production of more numerous smaller eggs (Tanasichuk and Ware,
1987), and reduced temperature arrested vitellogenesis in virgin Atlantic
cod G. morhua (Yoneda and Wright, 2005).
Maternal Effects in Fish Populations 19

The expression of the maternal effect can depend on the prevailing

temperature, influencing a fecund female or acting directly on the released
offspring. Maternal effects interacted with temperature to affect variance in
embryo development time in the yellowtail flounder P. ferrugineus (Benoit
and Pepin, 1999). Sex ratio of Atlantic silverside, M. menidia, was influenced
by a female-temperature interaction when exposed to differences tempera-
tures regimes as embryos and larvae (Conover and Kynard, 1981). Survival of
chum salmon (Oncorhynchus keta) eggs to hatching was highest at a mid-range
egg incubation temperature, and there was an interaction of female size with
incubation temperature resulting in lower survival at extremes of temperature
for eggs from large females compared with eggs from smaller females
(Beacham and Murray, 1985). A number of studies assess maternal or female
effects and temperature effects separately, but do not explicitly analyse (or at
least present the results of) a female  environment interaction (e.g., Bengston
et al., 1987; Heath et al., 1993; H
ie et al., 1999a). Conversely, in aquaculture
studies, females are more generally pooled to examine environmental effects
such as temperature (e.g., Baynes and Howell, 1996; Yang and Chen, 2005),
despite the facilities existing for close examination of these interactions.
The site-attached habits of many tropical species (both pelagic and
benthic spawning) make them ideal models to assess the interaction of
environment and female and its effects on offspring traits. Despite this,
few studies have assessed maternal and temperature effects in tropical fish.
When examined over the range of temperature experienced under natural
conditions, temperature had no apparent effect on the nest-tending beha-
viour of adult the red and black anemonefish, A. melanopus (Green and
McCormick, 2005b). In a diallel cross experiment on the same species,
temperature interacted with male and female parent and influenced growth
rate and mortality of larvae, but not size at metamorphosis, and temperature
interacted with female identity to influence swimming ability of pre-settlement
fish (Green and McCormick, 2005a).

2.2.3.1. Environmental clines in growth Latitudinal or altitudinal clines

in growth and reproductive factors occur in ectotherms, and are generally
thought to be the response of ectotherms to temperature or seasonality
varying along a physical and geographical gradient, for example, lizards
(Forsman and Shine, 1995), fish (Schultz et al., 1996) and frogs (Laugen
et al., 2003b). While such a gradient of effects on offspring traits are sometimes
relegated to genetic drift between geographically isolated populations (e.g.,
fishes; Yamahira and Conover, 2002), maternal effects are also a source of this
variation (e.g., frogs; Laugen et al., 2002). Maternally mediated differences in
egg size contribute to population divergence along with genetic divergence;
however, maternal effects seem not to override the genetic differences
apparent in some populations over a large scale (Laugen et al., 2002). Com-
bined latitudinal and maternal effects have been described in insects
20 Bridget S. Green

(Mousseau and Dingle, 1991), lizards (Sinervo and Adolph, 1994), fish
(Brown et al., 1998) and frogs (Laurila et al., 2002). A meta-analysis of egg
size variation in coho salmon (Oncorhynchus kisutch) attributed the observed
variation in egg size to the variability both within (female) and between
population (latitudinal) effects (Fleming and Gross, 1990).

2.2.3.2. Environmentally determined sex determination In sexually

labile species, the microenvironment in which a female deposits her eggs or
larvae can determine the sex of offspring, providing a unique avenue for the
expression of a maternal effect or influence. Temperature-dependent sex
determination (TSD) operates over seasonal gradients as well as small scale
physical gradients, and is linked to the thermal regime the eggs or larvae
experience. In some reptiles, including crocodilians (Lang and Andrews,
1994), turtles (Ewert et al., 1994) and lizards (Warner and Shine, 2005),
gender is commonly determined by the thermal regime the embryos experi-
ence during a thermosensitive period of embryonic development, and
temperature is explicitly determined by the depth the females bury their
eggs. (Recently, this finding has been challenged and advanced in lizards,
where maternal nutrition also determined gender; Warner et al., 2007.)
In gonochoristic fishes, temperature for development of the larvae and
juvenile can also be critical to the gender determination of the offspring, and
this has been linked back to the timing of spawning, particularly in temper-
ate climates where there are marked seasonal fluctuations (in order of 20  C)
in water temperature, for example, southern flounder Paralichthys lethostigma
(Luckenbach et al., 2003) and Atlantic silverside M. menidia (Conover and
Kynard, 1981). Fishes are facultatively flexible about where and when they
lay their eggs and this can engender a maternal component to sex determi-
nation and consequent sex ratio differences within a population. Addition-
ally, there is significant ‘between female’ variation in offspring sex ratio,
even when the females are experimentally spawned at the same time, for
example, M. menidia (Conover and Heins, 1987a; Conover and Kynard,
1981; Lagomarsino and Conover, 1993). A series of laboratory experiments
demonstrated a maternal (Conover and Heins, 1987b; Conover and
Kynard, 1981) and paternal (Conover and Heins, 1987b) component inter-
acting with a simulated seasonal environmental shift resulting in tempera-
ture-dependant sex determination in M. menidia. Most approaches to
measuring TSD in fishes demonstrate a female effect indirectly by experi-
mentally manipulating temperature of a clutch to simulate seasonal shifts.
Sex determination is generally set late in larval development, for example,
M. menidia (Conover and Kynard, 1981), Odonthesthes bonariensis and Pata-
gonia hatcheri (Strüssmann et al., 1997) or within a restricted window related
to size, for example, marbled sole, Limanda yokohamae (Goto et al., 2000),
though some species are sensitive to TSD throughout larval development,
for example, sea bass D. labrax (Koumoundouros et al., 2002). TSD was not
Maternal Effects in Fish Populations 21

found in northern populations of two cyprinodontid fishes, F. heteroclitus

and Cyprinodon variegates either in the field or in the laboratory (Conover
and Demond, 1991).
The influence of maternal effects through TSD may have fitness implica-
tions. Labile sex determination is an advantage when individual fitness in a
particular environment is gender dependent (Conover, 1984; Conover and
Heins, 1987a) and can occur across a season to favor growth of one sex over the
other if reproductive success depends on size, for example, Atlantic silverside
M. menidia (Conover, 1984), tidewater silverside M. peninsulae (Yamahira and
Conover, 2003), sea bass Dicentrarchus labrax (Koumoundouros et al., 2002),
and two atherinids O. bonariensis and P. hatcheri (Strüssmann et al., 1997).
There are two reported reaction norms for TSD within a population.
Firstly, there is an inverse relationship between temperature during larval
development and proportion of offspring that differentiate as females
(Fig. 1.1; M. menidia, Conover and Kynard, 1981; Odontesthes bonariensi
and P. hatcheri, Strüssmann et al., 1997). That is, as temperature experienced
during larval development increases, the proportion of female offspring in a
clutch decreases, resulting in a male bias at warmer temperatures. The
second reported response is that high and low temperatures induce a male
biased sex ratio and mid-range temperatures induce a 1:1 sex ratio (Fig. 1.1;
southern flounder P. lethostigma, Luckenbach et al., 2003; hirame P. oliva-
ceus, Yamamoto, 1999). The apparent differences in the shape of the
response curve of gender expression to temperature may arise if the range

100

80

60

40

20

0
14 16 18 20 22 24 26 28
Temperature ⬚C

Figure 1.1 Temperature determined sex determination in early life history stages of six
fish species. ‘% females’ represents the proportion of each clutch that expresses the
female gender. —Pejerrey, Odontesthes bonariensis (atherinid) (Str€
ussmann et al., 1997),
D—P. hatcheri (atherinid) (Str€
ussmann et al., 1997), □—southern flounder, Paralichthys
lethostigma (Luckenbach et al., 2003), x—European sea bass, Dicentrus labrax
(Koumoundouros et al., 2002), x—barfin flounder, Verasper moseri (Goto et al., 1999),
▲—hirame, Paralichthys olivaceus (Yamamoto, 1999).
22 Bridget S. Green

of temperatures each species is tested at represents only a portion of the

possible range of temperatures larvae might experience in the wild during
the thermosensitive stage. For example, marbled sole L. yokohamae (Goto
et al., 2000), barfin flounder Verasper moseri (Goto et al., 1999) and sockeye
salmon Oncorhynchus nerka (Azuma et al., 2004) were only tested over two
temperatures, and so it is inconclusive if the relationship between tempera-
ture and sex ration is linear or whether the observed linear relationship is
part of a bell-shaped curve. Most importantly, in the context of maternal
effects, these experiments suggest that seasonal timing of spawning and the
accompanying temperature shifts could introduce a maternal or female
effect on offspring quality due to the influence temperature has on offspring
sex ratio. Maternal effects throughout a spawning season can alter sex ratios
in frogs (Sakisaka et al., 2000) and fishes (Conover and Kynard, 1981). This
is thought to be adaptive to either maximise investment or maximising time
to development of males by producing them early in the season. This is
particularly for species where males can reproduce in their first year, but the
females take two years. By producing males early in the season there is an
increased chance that some offspring will reproduce within 12 months
which increases the parents’ reproductive fitness.

2.2.4. Salinity
Salinity levels of aquatic systems vary from 0 to 36 parts per thousand (ppt)
and some systems fluctuate seasonally due to rainfall or aseasonally due to
oceanic upwellings, downwellings or seeps. Oceanic ecosystems have a
relatively stable salinity around 35 ppt (except the Red and Baltic Seas),
and most freshwater streams by definition have salinities of zero; landlocked
lakes may have high salinities and inland seas, such as the Baltic Sea, may
have distinct haloclines. Salinity in transitional environments at the fringe of
land and sea, such as estuaries, littoral zones and inland seas can fluctuate
widely with season and particularly with rainfall in watershed areas (see
discussion in Wootton, 1990). An interaction of maternal effects and salinity
on offspring quality will most likely occur in estuarine and inshore species
where the largest salinity fluctuations are experienced. Changes in salinity in
transitional environments can create some level of physiological stress in the
resident fishes as the physiological cost of responding to changes in salinity
may be at the expense of processes such as growth or reproduction, and
reproduction in euryhaline species may be inhibited by freshwater influx
(Billard et al., 1981). An interaction of maternal effect and salinity is also of
interest in the aquaculture industry, where an option of rearing anadromous
species in freshwater water without affecting growth or reproduction may
reduce maintenance requirements and costs.
The few studies examining the interaction of salinity and maternal effects
have demonstrated that salinity changes affect a range of both female
reproductive and offspring traits. Mangrove rivulus (Rivulus marmoratus)
Maternal Effects in Fish Populations 23

reared at lowered salinity matured later and at larger sizes than fish at
‘normal’ or high salinities, and also produced fewer, larger eggs which had
higher hatching success and decreased time to hatching (Lin and Dunson,
1995). Salinity exposure of females enhanced the salinity tolerance of their
offspring in the guppy (P. reticulata), increasing survival under high salinity
exposure (Shikano and Fujio, 1998a,b). Indirect interactions between
maternal effects and salinity occurred in Baltic cod (G. morhua) where
neutral buoyancy is critical for egg survival. Oxygen poor water predomi-
nates beneath a halocline of this inland sea, and to compensate, larger
females produced larger eggs with neutral buoyancy at a lower salinity,
which float above the halocline and therefore above the oxygen poor water,
facilitating survival in the unusual conditions of the Baltic Sea (Vallin and
Nissling, 2000). Under high salinity, males can show decreased parental care
of eggs, including reduced fanning and egg-cleaning in the Florida Flagfish
Jordanella floridae (St Mary et al., 2001).

2.2.5. Prey abundance and quality

Prey availability influences the resources available to a female for oogenesis
and reproduction, for example, Atlantic cod G. morhua (Dossantos et al.,
1993). When quality or abundance of food is limited to the adults it may
result in a trade-off in size, quality or number of eggs produced by the
females (Gagliano and McCormick, 2007), or may result in more variability
in offspring quality within a clutch, for example, lizards (Warner et al.,
2007), or reproductive investment may be reduced, for example, lizards
(Du, 2006) and fish Acanthochromis polycanthus (Donelson et al., 2008).
Seasonal cycles or pulses of high quality food can increase the energy
available to a female, which in turn increases female condition, enabling
her to allocate more resources to reproduction and ultimately the number
or quality of offspring, for example, fish P. amboinensis (Kerrigan, 1997;
McCormick, 2003). In polychaete worms (Capitella sp.), an increase in adult
food quality enabled the adults to grow twice as fast, produce more, smaller
eggs, which were larger in volume and energy content than broods pro-
duced by siblings on a lesser diet (Qian and Chia, 1991). In some terrestrial
vertebrates, if food is a marginal resource, the female may skip a reproduc-
tive season in favour of growth, and an increase in size may increase
fecundity the following year, for example, Galapagos finches (Hau et al.,
2004) and water skinks (Schwarzkopf, 1993). Such flexible allocation is not
universal though and some animals will reproduce regardless of the resource
availability, for example, common frogs R. temporaria (Lardner and Loman,
2003). It is more difficult to track seasonal or annual effects of food
availability in fishes as they are highly mobile and difficult to recapture or
observe during spawning.
The effects of prey availability on reproductive investment is most
effectively studied in wild populations where the dynamics of costs and
24 Bridget S. Green

cost avoidance can be measured (Schwarzkopf, 1993) and individual prey

consumption, growth and reproduction can be measured. The discrete
habitat use by many terrestrial vertebrates and insects lends them to such
an examination; in contrast, many fishes are highly mobile and often
difficult to track over any length of time. Tropical fishes are good models
to investigate the effects of food availability on maternal effects and repro-
ductive quality because many species are site attached and lay benthic eggs,
and so female and offspring quality can be tracked over time, relative to
abundances and quality of natural prey items. For example, lipid rich coral
propagules released in a mass spawning event (occurring once per lunar
month over 2 or 3 summer months) increased female condition, and
subsequent eggs spawned had larger yolk sacs and oil globules
(McCormick, 2003). In two similar experiments, wild nesting female
Pomacentrus amboinenesis supplemented with a pulse of high quality food
during the reproductive season produced eggs with larger yolk-sacs than
field controls that were not supplementary fed (Gagliano and McCormick,
2007; Kerrigan, 1997). Increased yolk-sac size, however, did not result in
larger larvae at hatching in either study, an unexpected result which is
symptomatic of the complexity of the influence of field variables on maternal
and offspring traits (Gagliano and McCormick, 2007; Kerrigan, 1997).
The direct effects of prey abundance and nutritional quality on fish
reproduction are more difficult to measure in wild populations of temper-
ate and/or pelagic fish because many fish are mobile and few temperate
fishes guard demersal eggs. Also, typically fishes must be destructively
sampled to determine spawning status. Indirect measures are generally
used to estimates the influence of prey abundance on offspring quality.
Interannual fecundity estimates may be correlated to the quality and
quantity of prey items coinciding with oogenesis, for example, Arcto-
Norwegian cod G. morhua (Kjesbu et al., 1998); or the amount of fat
storage, which is seen as an indicator of nutritional status, for example,
Baltic herring C. harengus (Rajasilta, 1992). Instances of skipped spawning
in female teleosts have been demonstrated microscopically in a variety of
species including G. morhua, P. americanus, Reinhardtius hippoglossus, Hoplos-
tethus atlanticus, M. aeglefinus, Pleuronectes platessa, Acanthopagrus australis,
Solea solea, S. maximus, D. labrax and Microstomus pacificus (Rideout et al.,
2005a). A short modelling exercise in that review demonstrated that there
could be a benefit to total lifetime reproductive output in skipping a
spawning season as chance of mortality is reduced (Rideout et al.,
2005a). Skipped spawning in fishes is believed to be a response to poor
nutrition, although this is typically based on fishes kept in captivity (Ali
and Wootton, 1999; Burton, 1994; Burton and Idler, 1984; Hislop et al.,
1978; Ma et al., 1998; Rijnsdorp, 1990), as there is little definitive field
evidence of reduced food availability causing spawning omission. Gener-
ally, direct evidence of a link between prey abundance and reproduction is
Maternal Effects in Fish Populations 25

difficult to demonstrate in mobile pelagic spawning fish, but can be

inferred through correlative studies.
As noted in other sections of this review, the natural environment is
complex and trade-offs in egg attributes and maternal food abundance
interact with other environmental variables such as offspring prey density,
oxygen availability and competition, making it difficult to isolate maternal
effects as the sole source of offspring variation. Winemiller and Rose (1993)
modelled larval fish survival under different initial size and number scenarios
including prey density. In a virtual variable environment it paid to be big,
but when prey was abundant, more small fishes survived, thereby increasing
parental fitness. In laboratory experiments simulating some level of envi-
ronmental complexity, reproductive quality of R. marmoratus, a self-fertilis-
ing hermaphrodite inhabiting estuaries, was influenced by an interaction of
maternal food availability and salinity. Under high feeding levels, females
produced larger eggs than individuals under low feeding levels, and when
high food was combined with high salinity the size advantage increased (Lin
and Dunson, 1995). One of the pathways through which food availability
affects egg size is within a clutch due to proximity to the blood vessels
within the ovary. Under low prey abundance (food is limiting), eggs
positioned closest to the blood vessels within the ovary gain a size advantage
over those further from the blood vessels (Kamler, 1992).
Efforts to enhance reproductive output in the aquaculture industry
provide numerous examples of the influence of maternal food quality on
fecundity, reproductive output, and egg and larval quality, and while these
are generally not analysed as a true maternal effect (in the narrow sense),
they can be considered a female effect or female influence. As the aquacul-
ture industry is aimed at maximising production whilst minimising cost, a
wide range of broodstock food types, quality and abundances have been
tested for their effects on egg and offspring quality. Fecundity in continuous
spawners with short vitellogenic periods is influenced by essential dietary
nutrients (Izquierdo et al., 2001). Broodstock dietary lipid enhancement
does not always affect traditional fecundity and offspring quality measures
such as egg number, egg weight, fertilisation rate, hatching, survival to and
weight at first feeding; however, increased dietary lipid resulted in a reduced
amount of fatty acids in the eggs and larvae, for example, Atlantic salmon
S. salar (Rennie et al., 2005) and Atlantic halibut Hippoglossus hippoglossus
(Mazorra et al., 2003). Quality of polar lipids (e.g., walleye Stizostedion
vitreum, Czesny and Dabrowski, 1998) and protein (e.g., sea bass D. labrax,
Cerda et al., 1994a,b, 1995) in the maternal diet can affect factors such as egg
buoyancy and egg and larval survival. Dietary supplements of astaxanthin
and paprika powder increased egg production, egg quality and larval sur-
vival in yellowtail (Seriola quinqueradiata), and astaxanthin increased fecun-
dity in striped jack, Pseudocaranx dentex (Watanabe and Vassallo-Agius,
2003). These are only a few of numerous examples of broodstock nutrition
Exploring the Variety of Random
Documents with Different Content
papel oficial, comenzaron a soltar una tras otra las palabrillas
emolientes que eran del caso y que tantas veces habían pronunciado
verbi gratia... «Querido hermano en Cristo, la celestial Jerusalén abre
sus puertas para ti...». «Vas a entrar en la morada de los justos...»
«Ánimo. Más padeció el Redentor del mundo por nosotros».
—Queridos hermanos en Cristo —dijo el reo con cierta jovialidad
delicada—. Agradezco mucho sus consuelos; pero he de advertirles
que no los necesito. Yo me basto y me sobro. Así es que no verán en
mí suspirillos ni congojas... Me gusta que hayan venido, y así podrán
decir a la posteridad cómo estaba Patricio Sarmiento en la capilla, y
qué bien revelaba en su noble actitud y reposado continente (al deci
esto erguía la cabeza, echando el cuerpo hacia atrás) la grandeza de
la idea por la cual dio su sangre.
Pasmados se quedaron los hermanos, así como los frailes, de ve
su serenidad, y le exhortaron de nuevo a que cerrase el entendimiento
a las vanidades del mundo. Sola, de rodillas junto al altar, rezaba en
silencio.
 XXVI

Empezaron los hermanos a servir la comida. Sentose don Patricio a

la mesa, invitando a todos a que le acompañaran. No había
comenzado aún, cuando entró el señor de Chaperón, que jamás
dejaba de visitar a sus víctimas en la antesala del matadero. Como de
costumbre en tales casos, el señor brigadier trataba de enmascarar su
rostro con ciertas muecas, contorsiones y gestos encargados de
expresar la compasión, y helo aquí arqueando las cejas y plegando
santurronamente los ángulos de la boca, sin conseguir más que un
aumento prodigioso en su fealdad.
Saludó a Sarmiento con esa cortesía especial que se emplea con
los reos de muerte, amabilidad indefinible, incomprensible para quien
no ha visto muestras de ella en la capilla de la cárcel; urbanidad en la
cual no hay ni asomos de estimación, porque se trata de un
delincuente atroz, ni tampoco desprecio o encono a causa de la
proximidad del morir. Es una callada fórmula de repulsión compasiva
sentimiento extraño que no tiene semejante, como no sea en el alma
de algún carnicero no muy novicio ni tampoco muy empedernido.
—Hermano en Cristo —dijo don Francisco poniendo su mano, tan
semejante al hacha del verdugo, sobre el cuello del preceptor—
supongo que su alma sabrá buscar en la religión los consuelos...
Esta formulilla era de cajón. Aquel funcionario de tan pocas ideas la
llevaba prevenida siempre que a los reos visitaba.
—Señor don Francisco —replicó Sarmiento levantándose—, s
vuecencia quiere acompañarme a la mesa...
—No, gracias, gracias; siéntese usted... ¿Qué tal estamos de
salud?... ¿Y el apetito?
Lo preguntaba como lo preguntaría un médico.
 —Vamos viviendo —repuso el patriota—. O si se quiere, vamos
muriendo. Todavía no ha llegado el instante precioso en que sea
innecesario este grosero sustento de la bestia... Hemos de arrastrar e
peso del cuerpo, hasta que llegue el instante de dejarlo en la orilla y
lanzarnos al océano sin fin, en brazos de aquellas olas de luz que nos
mecerán blandamente en presencia del Autor de todas las cosas.
Chaperón miró a los frailes, e hizo un gesto que indicaba opinión
favorable del juicio de Sarmiento.
—Y ya que vuecencia ha tenido la bondad de visitarme —añadió e
reo, después de saborear el primer bocado—, tengo el gusto de
declarar que no siento odio contra nadie, absolutamente contra nadie
A todos les perdono de corazón, y si de algo valen las preces de un
escogido como yo (al decir esto su tono indicaba el mayor orgullo), he
de alcanzar del Altísimo que ilumine a los extraviados para que muden
de conducta, trocando sus ideas absolutistas por el culto puro de la
libertad... Sí, señor: se intercederá por los que están ciegos, para que
reciban luz; se recomendará a los crueles, para que hallen
misericordia en su día. Patricio Sarmiento es leal, pío, generoso, como
apóstol de la misma generosidad, que es el liberalismo... En m
corazón ya no caben resentimientos: todos los echó fuera, para
presentarme puro y sin mancha. El mártir de una idea, el que con su
sangre ha puesto el sello a esa idea, ¿me entienden ustedes?, para
que quede consagrada en el mundo, no enturbiará su conciencia con
odios mezquinos. Reconozco que, con arreglo a las leyes, m
condenación ha sido razonable. Vuecencia que me oye no ha hecho
más que cumplir con la ley que se le ha puesto en la mano. Así me
gusta a mí la gente. Venga esa mano, señor don Francisco.
Diole tan fuerte apretón de manos, que Chaperón hubo de retirar la
suya prontamente para que no se la estrujara.
—Además —prosiguió Sarmiento—, yo sé que los que hoy me
condenan, me admirarán mañana, si viven, y los que me vituperan
hoy, luego me pondrán en el mismo cuerno de la luna... Porque esto
durará poco, señor don Francisco: el absolutismo, a fuerza de
estrangular, se sostendrá un año, dos, tres, pongamos cuatro... En
este guisado de vaca —añadió dirigiéndose a uno de los hermanos de
la Caridad—, se le fue la mano a la cocinera: lo ha cargado de sal..
Pongamos cuatro años; pero al fin tiene que caer y hundirse para
siempre, porque los siglos muertos no resucitan, señor don Francisco
porque los pueblos, una vez que han abierto los ojos, no se resignan a
cerrarlos; y así como cada estación tiene sus frutos, cada época tiene
su sazón propia, y los españoles, que hasta aquí hemos amargado de
puro verdes, vamos madurando ya, ¿me entiende vuecencia?, y se
nos ha puesto en la cabeza que no servimos para ensalada
Vuecencias ahorquen todo lo que quieran. Mientras más ahorquen
peor. El absolutismo acabará ahorcándose a sí mismo ¿No lo quieren
creer? Pues lo pruebo. Empezó creando para su defensa y
sostenimiento la fuerza de voluntarios realistas. Son estos unos
animalillos voraces y golosos que no se prestan a servir a su amo, s
este no les alimenta con cuerpos muertos. Una vez cebados y
enviciados con el fruto de la horca, mientras más se les da más piden
y llegará un momento en que no se les pueda dar todo lo que piden
¿me entiende vuecencia?
Don Francisco, sin contestarle, y dirigiendo maliciosas ojeadas a los
frailes, hacía señas de asentimiento. El padre Salmón, que atendía
con sorna a las razones del preso, bajó la cabeza para ocultar la risa
Pero el padre Alelí, que devotamente rezaba en su breviario, alzó los
ojos, y mirando con expresión de alarma al reo, le dijo:
—Hermano mío, veo que, lejos de apartar usted su pensamiento de
las ideas mundanas, se engolfa más y más en ellas, con gran perjuicio
de su alma. Los momentos son preciosos; la ocasión, impropia para
hacer discursos.
—Y yo digo que es menos propia para sermones —replicó
Sarmiento, dando un golpecillo en la mesa con el mango del tenedo
—. Yo sé bien lo que corresponde a cada momento, y repito que
consagraré a la religión y a mi conciencia todo el tiempo que fuere
necesario.
—Bastante ha perdido usted en vanidades.
—Poquito a poco, señor sacerdote —dijo Sarmiento frunciendo las
cejas—, yo nada le quito a Dios. No se quite nada tampoco a las
ideas, que son mi propia vida, mi razón de ser en el mundo, porque
entiéndase bien, son la misión que Dios mismo me ha encargado
Cada uno tiene su destino: el de unos es decir misa; el de otros es
enseñar o iluminar a los pueblos. El mismo que a su paternidad
reverendísima le dio las credenciales, me las ha dado a mí.
—Reflexione, hombre de Dios —indicó el padre Salmón, rompiendo
el silencio—, en qué sitio se encuentra, qué trance le espera, y vea s
no le cuadra más preparar su alma con devociones, que aturdirla con
profanidades.
—Vuestras paternidades me perdonen —dijo Sarmiento grave y
campanudamente después de beber el último trago de vino— si he
hablado de cosas profanas que no les agradan. Yo soy quien soy, y sé
lo que me digo. Sé mejor que nadie por qué estoy aquí, por qué muero
y por qué he vivido. Allá nos entenderemos Dios y yo; Dios, que llena
mi conciencia y me ha dictado este acto sublime, que será ejemplo de
las generaciones. Pero pues las religiosidades no están nunca de más
vamos a ellas y así quedarán todos contentos.
—Esas divagaciones, hombre de Dios —dijo Salmón con puntos de
malicia—, confirman uno de los delitos que le han traído a este sitio.
—¿Qué delito?
—El de fingirse enajenado para poder tratar impunemente de cosas
prohibidas.
—Hablillas —dijo Sarmiento sonriendo con desdén—. Señores
hermanos de la Paz, si tuvieran ustedes la bondad de darme cigarros
se lo agradecería... Hablillas del vulgo. Si fuéramos a hacer caso de
ellas, ¿cómo quedaría el padre Salmón en la opinión del mundo? ¿No
dicen de él que solo piensa en llenar la panza y en darse buena vida?
¿No goza fama de ser mejor cocinero que predicador?... ¿De
frecuentar más los estrados de las damas, para hablar de modas y
comidas, que el coro para rezar y la cátedra para enseñar? Esto dice
el vulgo. ¿Hemos de creer lo que diga? Pues al padre Alelí, que me
está oyendo y que es persona apreciabilísima, ¿no se le acusó en otro
tiempo de volteriano? ¿No le tuvo entre ojos la Inquisición? ¿No
decían que antaño era amigo de Olavide y que después se había
congraciado con los realistas? Esto se dijo: ¿hemos de hacer caso de
las necedades del vulgo?
El padre Alelí palideció, demostrando enojo y turbación. Chaperón
se mordía los labios para dominar sus impulsos de risa. Ofrecía, en
verdad, la fúnebre capilla espectáculo extraño, único, el más singula
que puede imaginarse. Frente al altar veíase una mujer de rodillas
rezando sin dejar de llorar, como si ella sola debiera interceder po
todos los pecadores habidos y por haber; en el centro una mesa llena
de viandas, y un reo que, después de hablar con desenfado y
entereza, recibía cigarros de los hermanos de la Paz y Caridad y los
encendía en la llama de un cirio; más allá dos frailes, de los cuales e
uno parecía vergonzoso y el otro enfadado; enfrente la tremebunda
figura de don Francisco Chaperón, el abastecedor de la horca, el terro
de los reos y de los ajusticiados, sonriendo con malicia y dudando s
poner cara afligida o regocijada; todo esto presidido por el crucifijo y la
Dolorosa, e iluminado por la claridad de las velas de funeral que daban
cadavérico aspecto a hombres y cosas, y allá en la sala inmediata, una
sombra odiosa, una figura horripilante que esperaba: el verdugo.
Don Francisco Chaperón se despidió de su víctima. En la sala
contigua y en el patio encontró a varios individuos de la Comisión
militar y a otros particulares que venían a ver al reo.
—¡Que me digan a mí que ese hombre es tonto! —exclamó con
evidente satisfacción—. Tan tonto es él como yo. No es sino un
grandísimo bribón, que aún persiste en su plan de fingirse demente
por ver si consigue el indulto... Ya, ya. Lo que tiene ese bergante es
muchísimo talento. Ya quisieran más de cuatro... Por cierto que entre
bromas y veras ha hablado con un donaire... Al pobre Salmón le ha
puesto de hoja de perejil, y Alelí no ha salido tampoco muy librado de
manos de este licenciado Vidriera... Es graciosísimo: véanle ustedes..
Por supuesto, bien se comprende que es un solemnísimo pillo.
Y don Francisco se retiró, repitiéndose a sí mismo con tanta firmeza
como podría hacerlo un reo ante el juez, que don Patricio no era
imbécil, sino un gran tunante. Tal afirmación tenía por objeto sofocar la
rebeldía de aquel insubordinado corpúsculo, a quien llamamos antes la
monera de la conciencia chaperoniana, y que desde que Sarmiento
entró en capilla se agitaba entre el légamo, queriendo mostrarse y
alborotar y hacer cosquillas en el ánimo del digno funcionario. Con
aquella afirmación, don Francisco aplacó la vocecilla, y todo quedó en
profundo silencio allá en los cenagosos fondajes de su alma.
 XXVII

Durante la noche arreció el nublado de visitantes, sin que su

curiosidad importuna y amanerada compasión causaran molestia a
reo: antes bien, recibíalos este como un soberano a su corte. Situado
en pie frente al altar, íbalos saludando uno por uno, con ligeros
arqueos de la espina dorsal y una sonrisa protectora, cuya intensidad
de expresión amenguaba o disminuía según la importancia de
personaje. Todos salían haciéndose lenguas de la serenidad del reo, y
en la sala-vestíbulo, inmediata al cuerpo de guardia, oíase cuchicheo
semejante al que suena en el atrio de una iglesia en noches de novena
o miserere. Los entrantes chocaban con los que salían, y la
sensibilidad de los unos anticipaba a la curiosidad de los otros noticias
y comentarios.
Pipaón, que se había presentado de veinticinco alfileres, y parecía
un ascua de oro, según iba de limpio y elegante, estuvo largo rato en
compañía del reo, y le dio varias palmadas en el hombro, diciéndole:
—Ánimo, señor Sarmiento, y encomiéndese a su Divina Majestad y
a la Reina de los cielos, nuestra Madre amorosísima, para que le den
una buena muerte y franca entrada en la morada celestial... Adiós
hermano mío. Como mayordomo que soy de la Hermandad de las
Ánimas, le tendré presente, sí, le tendré presente para que no le falten
sufragios... Adiós... Procure usted serenarse... Medite mucho en las
cosas religiosas... Este es el gran remedio y el más seguro lenitivo..
¡La religión, la dulce religión! ¡Oh!, ¿qué sería de nosotros sin la
religión?... Es nuestro consuelo, el rocío que nos regenera, el maná
que nos alimenta... Adiós, hermano en Cristo; venga un abrazo (al da
el abrazo Pipaón tuvo buen cuidado de que no fuera muy expresivo
para que no se chafaran los encajes de su pechera)... Estoy
conmovidísimo... Adiós; repítole que medite mucho en los sagrados
misterios y en la pasión y muerte de Nuestro Señor Jesucristo..
Quizás nos veamos en el cielo, ¡ay de mí!, si Dios es misericordioso
conmigo.
Este fastidioso discurso, modelo exacto de la retórica convenciona
y amanerada del cortesano, agradó mucho a cuantos le oyeron; mas
don Patricio lo acogió con seriedad cortés y cierto desdén que apenas
se traducía en ligero fruncimiento de cejas. Pipaón salió, y aunque iba
muy a prisa, derecho a la calle, detuviéronle en el patio algunos
amigos.
—Estoy afectadísimo... No puedo ver estas escenas —les dijo
respondiendo a sus preguntas—. Fáltame poco para desmayarme.
—Dicen que es el reo más sereno que se ha visto desde que hay
reos en el mundo.
—Es un prodigio. Pero aquella vanidad e hinchazón son cosa
fingida... ¡Cuánto debe padecer interiormente! Se necesitan los bríos
de un héroe para sostener ese papel sin faltar un punto.
—¡Farsante!
—Perillán más acabado no he visto en mi vida. Seguramente
espera que le indulten; pero se lleva chasco. El gobierno no está po
indultos.
—Entremos... Todo Madrid desea verle. Vuelva usted, Pipaón.
—¿Yo? Por ningún caso —repuso el cortesano estrechando manos
diversas una tras otra—. Voy a una reunión donde cantan la Fábrica y
Montresor... ¡Qué aria de la Gazza Ladra nos cantó anoche esa mujer
Montresor nos dio el aria de Tancredo. ¡Aquello no es hombre, es un
ruiseñor!... ¡Qué portamentos, qué picados, qué trinos, qué
vocalización, qué falsete tan delicioso! Parece que se transporta uno a
séptimo cielo. Conque, adiós, señores..., tengo que ensayar antes un
paso de gavota. Señores, divertirse con el viejo Sarmiento.
Aún no se había separado de sus amigos, cuando salió al patio un
señor obispo que venía también de visitar al reo. Todos se
descubrieron al verle, haciéndole calle. Pipaón, después de besarle e
anillo, le habló del condenado a muerte.
—Mi opinión —dijo su ilustrísima (que era una de las lumbreras de
episcopado)— es que si no constara en los autos, como aseguran
consta de una manera indubitable, que se ha fingido y se finge loco
para hablar impunemente de temas vedados, la ejecución de este
hombre sería un asesinato. Desempeña este desgraciado su pape
con inaudita perfección, y apreciándole por lo que dice, no hay en
aquella mollera ni el más pequeño grano de juicio... A propósito de
juicio, señor de Pipaón, no lo ha tenido usted muy grande fijando para
el lunes la gran fiesta de desagravios a Su Divina Majestad que
celebra la Hermandad de Indignos esclavos del Santísimo
Sacramento, porque siendo el lunes día de la Natividad de Nuestra
Señora, la Real Congregación de la Guardia y Custodia dispone, po
antiguo privilegio, de la iglesia de San Isidro.
Pipaón respondió, mutatis mutandis, que no correría sangre a
causa de un conflicto entre ambas hermandades, y que él respondía
de arreglarlo todo a gusto de seglares y clérigos, sin que se quejaran
el Santísimo Sacramento ni Nuestra Señora, con lo cual y con acepta
la carroza de su ilustrísima para trasladarse a la calle de la Puebla
donde había de hacer el ensayo de la gavota antes de la tertulia, tuvo
fin aquel diálogo.
Avanzada la noche, se cerró la capilla a los curiosos, y también la
puerta de la cárcel, después que entraron seis presos recién sacados
de sus casas por delaciones infames. Una nueva conspiración
descubierta dio mucho que hacer aquella noche y en la siguiente
mañana al señor Chaperón.
Don Patricio se acostó a dormir en la alcobita inmediata a la capilla
pero su sueño no fue muy sosegado. Velábanle solícitos, y siempre
prontos a servir en todo, los hermanos de la Paz y Caridad. Sola no se
apartó de la capilla ni un solo instante ni de día ni de noche.
—Abuelito querido —le dijo al amanecer—, estoy muerta de pena
porque veo que tu conducta no es propia de un buen cristiano.
—Adorada hija —repuso Sarmiento besándola con ardiente cariño
—, si es propia de un filósofo, lo será de un cristiano, porque el filósofo
y el cristiano se juntan, se compendian y amalgaman en m
maravillosamente... Hazme el favor de ver si esos señores hermanos
me han preparado el chocolate... No extraño tus observaciones, hija
mía. Eres mujer y hablas con tu preciosa sensibilidad, no con la razón
que a mí me alumbra y guía. ¡Bendito sea Dios que me permite tenerte
a mi lado en estas horas postreras! Si no te estuviera viendo, quizás
me faltaría el valor que ahora tengo. Una sola cosa me afecta y
entristece, nublando el esplendoroso júbilo de mi alma, y es que
mañana a la hora de las diez..., porque supongo que... eso será a las
diez..., dejaré de recrear mis ojos con la contemplación de tu angelica
persona... Pero, ¡ay!, tú debes seguir viviendo; no ha llegado aún la
hora de tu entrada en la mansión divina; llegará, sí, y entrarás, y e
primero a quien verás en la puerta abriendo los brazos para recibirte
en ellos amoroso y delirante, será tu abuelito Sarmiento, tu viejecillo
bobo.
La voz temblorosa indicaba una viva emoción en el reo.
—Y te llevaré a presencia del Padre de todo lo existente y le diré
«¡Señor, aquí la tienes; esta es, mírala!...». Pero no quiero afligirte
más. Ahora oye varios consejos que debo darte y algunos encarguillos
que quiero hacerte... ¿Está ese chocolate?... Dame la mano para
levantarme, hija mía. ¿Sabes que están pesados y duros mis pobres
huesos?... ¡Ah!, pronto tendrás este bocado, ¡oh carnívora tierra
Pronto, pronto se te arrojará esta piltrafa, que por lo acecinada
demuestra que te pertenece ya. El noble espíritu abandona este
inmundo saco, y vuela en busca de su patria y de sus congéneres los
ángeles.
Levantose delante de Sola, porque estaba vestido. Un hermano le
trajo el chocolate, y quedándose solo con su amiga, le dijo estas
palabras, que ella oyó con profundísima atención:
—Idolatrada hija, mañana a las diez nos separaremos para siempre
Dios me dio la inefable dicha de conocerte, para que mi espíritu se
confortase antes de dejar el mundo. Te condujiste conmigo tan noble y
caritativamente, que no vacilo en declararte merecedora de inmorta
premio. Yo te lo aseguro, yo te lo profetizo —dijo esto cerrando los ojos
y extendiendo solemnemente los brazos en actitud de profeta—, yo te
lo fío, bendiciéndote. Creo tener poderes para ello. Gozarás de la
eterna dicha por tu cristiana acción. Ahora bien: hablando de cosas
más terrestres, te diré que es mi deseo partas en seguida para
Inglaterra a ponerte bajo el amparo de ese hombre generoso que ha
sido tu protector y hermano. Le conozco, y sé que su corazón está
lleno de bondades. Como me intereso también por él, declaro ante t
que ese joven debe tomarte por esposa, de lo cual resultará ventaja
para entrambos: para ti, porque vivirás al arrimo de un hombre de
mérito, capaz de comprender lo que vales; para él, porque tendrá la
compañera más fiel, más amante, más útil, más hacendosa, más
cristiana y más honesta con que puede soñar el amor de un hombre
Tengo la seguridad de que él lo comprenderá así —al decir esto
mostraba la convicción de un apóstol—. Si no lo comprendiese, dile
que yo se lo mando, que es mi sacra voluntad, que yo no hablo po
hablar, sino trasmitiendo por el órgano de mi lengua la inspiración
celeste que obra dentro de mí.
Sola oyó este discurso con recogimiento y admiración, pasmada de
advertir una profundísima concordancia entre la demencia de su amigo
y ciertas ideas de antiguo arraigadas en ella. No acertó a decir una
palabra sobre aquel tema, y su viejecillo bobo se le representó
entonces grande y luminoso, cual nunca lo había visto; más respetable
que todo lo que como respetable se nos presenta en el mundo.
Después de una pausa, durante la cual apuró el pocillo, Sarmiento
prosiguió así:
—Querida hija de mi corazón, voy a hacerte un encargo, atañedero
a cosas terrestres. Las cosas terrestres también me ocupan, porque
de la tierra salí, y en ella he de dejar las preciosas enseñanzas que se
desprenden de mi martirio. El género humano merece mi mayo
interés. La dicha del cielo no sería completa, si desde él no
contempláramos la constante labor de este pobre género humano, sin
cesar trabajando en mejorarse. Los que de él salimos no podemos
dejar de enviarle desde allá arriba un reflejo de nuestra gloria, sin lo
cual se envilecería, acercándose más a las bestias que a los ángeles
Hay que pensar en el género humano de hoy, que es el coro celestial e
inmenso de mañana, y todo hombre es la crisálida de un ángel, ¿me
entiendes? Si las criaturas superiores, al remontarse sobre los
mundanos despojos, miraran con desprecio esta pobre turba inquieta y
enferma a que pertenecieron; si no atendiendo más que al Eterno Sol
hicieran del deseo de la bienaventuranza un egoísmo, adiós universo
adiós pasmoso orden de cielo y tierra, adiós concierto sublime. No, yo
miro a la tierra y la miraré siempre. Le dejo un don precioso: mi vida
mi historia, mi ejemplo, hija mía; ¿sabes tú lo que vale un buen
ejemplo para esta mísera chusma rutinaria? Sí, mi historia será pronto
una de las más enérgicas lecciones que tendrá el rebaño humano para
implantar la libertad que ha de conducirle a su mejoramiento moral
Pero digo yo: ¿es fácil escribir esa historia? No. Bien conocidos son
mis discursos; y aunque yo no los he escrito, como todo el mundo los
tiene grabados en la memoria, no faltará quien los dé a la estampa
Sócrates no dejó escrito nada... Pero si serán perpetuados mis
discursos, habrá gran escasez de datos biográficos respecto a mí
Oye, pues, lo que voy a decirte.
 Tomando a Sola por un brazo, la acercó a sí:
—Viviendo en tu casa —añadió— apunté, no hace dos meses, los
principales datos de mi vida, tales como el día de mi nacimiento, el de
mi bautizo, el de mi confirmación, el de mi boda con Refugio, el de
feliz natalicio de Lucas, el de mi entrada en la enseñanza y otros: son
datos preciosísimos. Como los historiadores han de empezar desde
mañana mismo a revolver archivos y libros parroquiales, yo te encargo
que les saques de apuros. Mira tú: el apunte en que constan esos
datos está escrito con lápiz... Me parece que lo puse debajo del hule
de la cómoda. Búscalo bien por toda la casa, y entrégalo a esos
señores. Al punto sabrás quiénes son, porque no se hablará de otra
cosa en todo el mundo. No te descuides, y evitarás mil quebraderos de
cabeza, y quizás inexactitudes y errores que darán ocasión a
desagradables polémicas.
Sola sintió al oír esto que la admiración despertada por anteriores
palabras del viejecillo bobo, se disipaba como humo. ¡Cuán difícil era
señalar la misteriosa línea donde los desvaríos de Sarmiento se
trocaban en ingeniosas observaciones, o por el contrario, sus
admirables vuelos en lastimoso rastrear por el polvo de la necedad! La
joven prometió cumplir fielmente todo lo que le mandaba.
Al poco rato apareció el padre Alelí preparado para decir la misa, y
empezada esta, Sarmiento la ayudó con extraordinaria devoción y
acierto, tan seguro en las ceremonias como si hubiera sido monaguillo
toda su vida. Soledad la oyó con gran edificación, acompañada de los
hermanos y de algunos empleados de la cárcel. Después, por orden
del señor Chaperón, se cerró la capilla al público.
 XXVIII

Poniendo sobre todas las cosas su anhelante deseo de llega

pronto al fin de la jornada vital, que era el comienzo de su triunfo
Sarmiento deploraba que la justicia de aquellos tiempos hubiese fijado
en cuarenta y ocho horas el plazo de la preparación religiosa. Con diez
o doce horas había bastante, según él. Los dos frailes que le asistían
aprovecharon la ocasión de su soledad para hablarle recio en e
negocio de la salvación, logrando que don Patricio atendiese a este, y
consintiera en oír el trasnochado sermoncillo que preparado traía e
padre Salmón. Después de comer, cuando Sola, vencida por e
cansancio, había cedido al sueño y dormitaba sentada, el padre Alel
logró hacerse oír de Sarmiento con mayor interés. Por la noche
pareció que el espíritu del buen viejo se recogía y como que se
amilanaba algún tanto, mostrándose además en su rostro y cuerpo
cierto desmayo o fatiga. El patriota no permanecía ya en pie, sino
recostado con abandono en el sillón, fijando la vista en el suelo cual s
cayera en meditación taciturna. Silencio profundísimo reinaba en la
cárcel; las velas se habían consumido bastante y ardían en el último
cabo de ellas, elevando entre la vacilante luz el negro pábilo caduco, y
derramando cera amarilla en grandes chorros sobre los candeleros y
sobre el altar. El crucifijo y la Dolorosa parecían entregados a un sopo
misterioso. Nunca como en aquella hora había parecido la capilla
tristísima y lúgubre. Su ambiente de panteón daba frío, su luz tenue
convidaba a morirse y enterrarse. Era la madrugada del último día.
No fue insensible el espíritu de Sarmiento a esta influencia externa
y conociéndolo Alelí, le dijo que ya le quedaban pocas horas; que
viese lo que hacía si no deseaba arder perpetuamente en los infiernos
Al oír esto, mirole Sarmiento con desdén, y levantándose del sillón, se
puso de rodillas.
 —Puesto que su paternidad quiere que confiese, confesaré —dijo
lacónicamente.
—No es preciso que se arrodille usted, hermano mío —indicó e
buen fraile levantándole—. En estos casos permitimos al penitente que
haga la confesión sentado para evitarle cansancio.
—Yo prefiero estar de rodillas, porque no soy de alfeñique —dijo e
reo volviéndose a hincar—. Ahora, si vuestra paternidad tiene oídos
oiga... Yo amo a Dios sobre todas las cosas. ¿Cómo no amarle, si es
fuente de todo bien, manantial de toda idea, origen de toda vida? E
dio la idea moral al mundo, y el mundo, después de mil luchas
disputas y sangre, aceptó la ley moral que felizmente lo rige. Después
le dio la idea política, es decir, la libertad, para que se gobernase, y
todavía el mundo no la ha aceptado en su totalidad. Estamos en la
época de la predicación, del martirio...
—Basta —dijo Alelí con enfado—. Está usted profanando el nombre
de Dios con absurdas afirmaciones. Poco adelantamos por ese
camino, hermano querido. Confiese usted su amor a Dios sin mezcla
de extravagancia alguna. Me basta con eso por ahora, y adelante.
—Confieso —añadió el penitente— que con frecuencia he jurado su
santo nombre en vano, y además que he usado votos y ternos, pues
adquirí tiempo ha la pícara costumbre de sacar a todo el chilindrón y la
chilindraina; pero, con perdón de vuestra reverencia, creo que pecados
como este no llevan a casa de Pedro Botero. Tampoco he santificado
las fiestas como está mandado..., desidia, pura desidia y abandono
En el cuarto, ¿qué he de decir sino que jamás he faltado a él ni en
pensamiento? Pues en lo de matar, si alguien perdió por mí la vida, fue
en leal acción de guerra y cuando el honor de mi bandera así me lo
mandaba. No obstante, un pecado grave tengo en lo tocante a este
mandamiento, y ese lo voy a confesar aquí con la boca y con e
corazón, porque ha tiempo pesa sobre mi conciencia; y aunque estoy
muy arrepentido, paréceme que jamás logro echar de mí la mancha y
peso que me dejó. Hallándose preso y encadenado un vecino mío
padre de esta joven que me acompaña, pidió un vaso de agua y se lo
negué. ¡Qué infame bellaquería! Pero válgame mi contrición sincera y
el cariño ardiente que después he puesto en la bendita hija de aque
desgraciado.
—Adelante —murmuró Alelí satisfecho de que hubiese algún
pecado evidente que justificase su ministerio.
 —Del sexto no diré más sino que después de la muerte de m
Refugio, que acaeció hace veintidós años, he observado castidad
absoluta, a pesar de ser solicitado para faltar a aquella preciosa virtud
por más de una hembra que no debió de ver en mí saco de paja
Tampoco he robado jamás a nadie ni el valor de un alfiler, y en el ramo
de mentir, si alguna vez falté a la verdad, fue en negocios baladís y de
poca monta.
—Alto, alto —dijo Alelí con interés sumo, viendo llegado el tema que
abordar quería—. Usted ha mentido, y ha mentido gravemente po
sistema sosteniendo un papel engañoso con la terquedad del hombre
más perverso. Es opinión general que usted se finge demente
poseyendo en realidad un claro juicio; es público y notorio, y así consta
en la causa, que todos esos disparates con que ha divertido a Madrid
son obra del talento más astuto, para poder vivir en una sociedad que
proscribe a los revolucionarios. Vamos a ver, hermano mío: repare
usted delante de quién está, mire esa imagen sacratísima, considere
que le restan pocas horas de vida, considere que ya no es posible e
engaño, y ábrame su corazón, arroje la máscara, y dígame si, en
efecto, este hombre exaltado que vemos es un hábil histrión. ¡Ah!
hermano mío, aseguran que usted sostiene su papel, esperando que
le indulten por tonto... ¡error, error, porque no es ese el camino de
indulto! Más fácil le sería conseguirlo con una confesión franca de su
pecado... Al menos, haciéndolo así tendrá el perdón de Dios y la gloria
eterna.
—¡Yo farsante, yo histrión, yo..., yo! —exclamó Sarmiento clavando
ambas manos, como garras, en su pecho.
Miraba al padre Alelí con los ojos encendidos y con expresión de
sorpresa, que bien pronto se tornó en amargo desdén.
—Usted no me comprende... —dijo levantándose—. Vaya usted a
confesar colegiales, señor padre Alelí. Me confesaré solo.
Y arrodillándose delante del altar, alzó las manos, y sin quitar los
ojos del Crucifijo habló así:
—Señor, Tú que me conoces no necesitas oír de mi boca lo que
siente mi corazón, que pronto dará su último latido, dejándome libre
Sabes que te adoro, que te reverencio, y que ejecuto puntualmente la
misión que me señalaste en el mundo. Sabes que la idea de la
libertad, enviada por ti para que la difundiéramos, fue mi norte y m
guía. Sabes que por ella vivo y por ella muero. Sabes que si comet
faltas, me he arrepentido de ellas con grandísima congoja. Sabes que
perdono de todo corazón a mis enemigos, y que me dispongo a roga
por ellos, cuando mi espíritu pueda hablar sin boca y ver sin necesidad
de ojos. Mi confesión está hecha públicamente. Óigala todo el que
tiene oídos.
Y después, volviéndose al fraile, que absorto le miraba, díjole:
—Ahora, padre Alelí, espero que no tendrá vuestra paternidad
reverendísima inconveniente alguno en darme el pan eucarístico. Bien
se ve que puedo recibir a Dios dentro de mí. Estoy puro de toda
mancha: soy como los ángeles.
Entonces viose una cosa extraña, que por lo extraña parecía
horrible en aquel sitio y ocasión. El padre Alelí no pudo evitar una
sonrisa. Diríase que esta brilló en la fúnebre capilla como un reflejo
mundano dentro de la región de los difuntos. Pero tornó al punto a la
seriedad, y gravemente dijeron a dúo ambos frailes:
—No podemos dar a usted la Eucaristía, desgraciado hermano.
Mientras Sola acudió a consolar a Sarmiento, que parecía muy
contrariado por aquella negativa, Alelí llevó aparte a Salmón y le dijo:
—Es más tonto que hecho de encargo. Yo repito que ajusticiar a
este hombre es un asesinato, y Chaperón, los jueces que le
sentenciaron y nosotros que le asistimos, estamos más locos que él
Yo no puedo ver este horrible espectáculo. ¿Pero no es evidente que
ese hombre es necio de capirote? Estamos coadyuvando a una obra
inicua. ¡Y esperábamos que confesase su comedia!
—Como siempre le tuve por mentecato de una pieza, no me he
llevado chasco. No sé para qué nos traen aquí.
—Ni yo. Voy a hablar con Chaperón.
—Yo no me tomaría el trabajo de hablar con nadie.
—Pues yo sí.
—Pues yo no.
Poco después de esto, el reo vio personas y objetos con una
claridad que le conturbó sobremanera sin saber por qué. Era que
había avanzado el día y la capilla recibía un poco de luz, ante la cua
palidecía ligeramente la de las soñolientas velas, casi consumidas
Aquel débil resplandor del astro rey hizo daño a la retina y al espíritu
del anciano, sin que su entendimiento pudiera explicarse la razón de
ello.
 —Es de día —dijo con cierto asombro, y al punto se quedó
taciturno.
Los hermanos de la Caridad aparecían más compungidos que en e
día anterior, y rezaban devotamente arrodillados ante el altar. Salmón
rogó al condenado que se sentase, y poniéndose junto a él, hízole
exhortaciones encaminadas a apartar su alma del tremendo abismo a
cuyo borde se encontraba.
—Pocas horas me restan —murmuró el patriota dando un gran
suspiro—. Mi alma será más fuerte cuanto más cerca esté el instante
lisonjero de su liberación. ¿Cuántas horas faltan?
—No cuente usted las horas... ¿Qué valen dos ni tres horas
comparadas con la eternidad?
Sarmiento no respondió. Observaba los ladrillos del piso y fijaba su
vista con minuciosidad aritmética en todos aquellos que tenían e
ángulo gastado. Diríase que los contaba.
—¿En dónde está mi hija? —dijo de súbita moviéndola cabeza con
ansiedad—. Sola, niña de mi corazón, no te separes de mí.
Sola se arrojó llorando en sus brazos. Notó que tenía las manos
frías y temblorosas.
—Dentro de poco dejaré de verte, ¡ay! —exclamó el viejo haciendo
esfuerzos verdaderamente heroicos para dominar su emoción—. ¡Que
sea tan flaca y miserable esta humana naturaleza, que ni aun teniendo
por segura la entrada en la morada celestial, pueda mirar con absoluto
desprecio los afectos del mundo!... Aquí me tienes más valiente que
un león (sus labios temblaban al decirlo, y su voz era como el ronco
trinar de un ave moribunda), y, sin embargo, esto de separarme de ti
esto de dejarte sola...
Se pasó la mano por la frente, y durante un rato tapose los ojos.
—No sé por qué está triste el día —murmuró con disgusto—. ¡Qué
ruido hay en la cárcel!... ¿Qué voces son esas? Parece un canto
desacorde o un graznido de pájaros llorones. ¿Qué es eso?
Soledad no contestó nada, y apoyó su frente sobre el pecho de
anciano. A la capilla llegaba una repugnante música llorona de gritos
humanos que parecía formada de todos los rencores, de todos los
sarcasmos, de todas las lágrimas y de todos los suspiros encerrados
en la cárcel.
El padre Alelí, que había salido al amanecer, volvió muy cabizbajo
y sin hablar una sola palabra al reo ni a los demás, preparose para
decir la misa. En tanto, uno de los hermanos departía con Sarmiento
de cosas religiosas, sabedor de que estas habían de llevar gran alivio
y fuerzas al espíritu del reo.
—Hoy —le dijo— celebramos en Santa Cruz los mayordomos de
esta Real Archicofradía misa solemne de rogativa para implorar los
divinos auxilios en la última hora del pobre condenado a muerte. Ya
sabe usted que nuestro santísimo padre Pío VII ha concedido
indulgencia plenaria a todos nosotros y a los fieles que asistan a esa
misa y hagan oración por la concordia de los príncipes cristianos
extirpación de las herejías y exaltación de la fe católica.
—De modo —dijo Sarmiento con amarga ironía— que en esa misa
se hace oración por todo menos por mí.
—No, hermano mío, no —dijo el cofrade con la melosidad del beato
—; que también habrá lo que llamamos ejercicio de agonía, donde se
hace la recomendación del alma del reo; luego siguen las jaculatorias
de agonía y se cantará el ne recorderis. Los más bellos himnos de la
Iglesia y las piadosas oraciones de los fieles acompañan a usted en su
tránsito doloroso..., ¿qué digo doloroso?, gloriosísimo. Piense usted en
la pasión de Nuestro Señor Jesucristo, y se sentirá lleno de valor. ¡Oh
feliz mil veces el que abandona esta vida miserable libre de todo
pecado!
El hermano inclinó la cabeza a un lado, bajando los ojos y cruzando
las manos en mística actitud. Después rezó en silencio.
Alelí dijo la misa, que oyó Sarmiento como el día anterior, de rodillas
y con profunda atención. Al concluir sentose con muestras de gran
cansancio; mas ponía mucho empeño en disimularlo.
—¿No quiere usted tomar algo? —le dijo uno de los hermanos—
Hemos preparado un almuerzo ligero. ¿Se siente usted mal, hermano
querido? Vamos, un huevo frito y un poco de jamón... ¡Si para eso no
se necesita gana! —añadió viendo que el reo hacía signos negativos
con la cabeza y con la mano—. Sí, lo traeremos, y también un vaso de
vino.
—No quiero nada.
—¿Ni café?
—Tomaré el café por complacer a ustedes —repuso Sarmiento
sonriendo con tristeza.
Alelí se sentó junto a él, y tomándole la mano se la apretó
cariñosamente diciéndole:
 —Hermano mío, en nombre de Dios y de María Santísima, a cuya
presencia llegará usted pronto, si sabe morir como cristiano en estado
de contrición perfecta, le ruego que no me oculte sus pensamientos, s
por ventura son distintos de lo que ha manifestado aquí y fuera de
aquí.
—Si yo ocultara mis pensamientos, si yo no fuera la misma verdad
—replicó don Patricio con entereza más noble—, no sería digno de
este nobilísimo fin que me espera... ¡Ah!, señores, la taimada
naturaleza nos tiende mil lazos por medio de la sensibilidad y de
instinto de conservación; pero no, no será mi grande espíritu quien
caiga en ellos. Vamos, vamos de una vez.
Y se levantó.
—Calma, calma, hermano mío; aún no es tiempo —le dijo Alel
tirándole del brazo—. Siéntese usted. Por cierto que no es nada
conveniente para su alma esa afectación de valor y ese empeño de
sostener el papel de héroe. Una resignación humilde y sin aparato
una conformidad decorosa sin disimular el dolor, y un poco de
entereza que demuestre la convicción de ganar el cielo, son más
propias de esta hora que la fanfarronería teatral. Usted está nervioso
desazonado, inquieto, sin sosiego; tiémblanle las carnes, y se cubre su
piel de frío sudor.
—El que era Hijo de Dios sudó sangre —afirmó Sarmiento con brío
—; yo, que soy hombre, ¿no he de sudar siquiera agua?... Vamos
pronto. Repito que deseo concluir.
Entonces sintiose más fuerte el coro de lamentos, y al mismo
tiempo ronco son de tambores destemplados.
—He aquí las tropas de Pilatos —observo Sarmiento.
—Hermano, hermano querido —le dijo Alelí abrazándole—. Una
palabra sola de verdadera piedad, de verdadera religiosidad, de amo
y temor de Dios. Una palabra, y basta; pero que sea sincera, salida de
fondo del corazón. Si la dice usted, todos esos pensamientos livianos
de que está llena su cabeza, como desván lleno de alimañas, huirán a
ver entrar la luz.
—Cristiano católico soy —afirmó Sarmiento—. Creo todo lo que me
manda creer la Iglesia, creo todos los misterios, todos los sagrados
dogmas, sin exceptuar ninguno. He oído misa, he confesado sin omiti
nada de lo que hay en mi conciencia, he deseado ardientemente
recibir la Eucaristía, y si no la recibí ha sido porque no han querido
dármela. ¿Qué más se quiere de mí? ¡Oh Señor de cielos y tierra! ¡Oh
tú, María, Madre amantísima del género humano!, a vosotros vuelvo
mis miradas, vosotros lo sabéis, porque veis mi rostro, no este de la
carne, sino el del espíritu. Los que no ven el de mi espíritu, ¿cómo
pueden comprenderme? Hacia vosotros volaré invocándoos, llevando
en mi diestra la bandera que habéis dado al mundo, la bandera de la
libertad, por la cual he vivido y por la cual muero.
Salmón y Alelí movieron la cabeza. Su pena y desasosiego eran
muy profundos. Soledad, sin fuerzas ya para luchar con su dolor
estaba a punto de perder el conocimiento. Don Patricio, dicho su
último discurso, examinaba una grieta que en el techo había y después
la costura del paño del altar. Creeríase al verle que aquellos dos
objetos insignificantes merecían la mayor atención.
Varias personas entraron en la capilla, todas decorando sus caras
con la aflicción más edificante. Levantose el reo, y sin dejar de
observar la costura del altar, habló así solemnemente:
—Cayo Graco, Harmodio y Aristogitón, Bruto..., héroes inmortales
pronto seré con vosotros... Y tú, Lucas, hijo mío, que estás en las filas
de la celestial infantería, avanza al encuentro de tu dichoso padre.
Los frailes, puestos de rodillas, recitaban oraciones, empeñándose
en que el reo las repitiera; pero Sarmiento se apartó de ellos
afirmando:
—Todo lo que puede decirse lo he dicho en mi corazón durante la
misa y después de ella.
Oyose el tañido de la campana de Santa Cruz.
—Tocan a muerto —dijo Sarmiento—. Yo mandaría repicar y alza
arcos de triunfo, como en el día más grande de todos los días. ¡Ya veo
tus torres, oh patria inmortal, Jerusalén amada! ¡Bendito el que llega a
ti!
El alcaide le saludó, enmascarándose también con la carátula de
piedad lastimosa que pasaba de rostro en rostro, conforme iban
entrando personajes. Después separáronse todos para dar paso a un
hombre obeso, algo viejo, vestido de negro, cuyo aire de timidez
contrastaba singularmente con su horrible oficio: era el verdugo, que
avanzando hacia el reo, humilló la frente como un lacayo que recibe
órdenes.
Don Patricio sintió en aquel momento que un rayo frío corría po
todo su cuerpo desde el cabello hasta los pies, y por primera vez