ResearchPDF Available

Marine Biodiversity and Ecosystem Functioning

Authors:
Marine Biodiversity &
Ecosystem Functioning
Heip, C., Hummel, H., van Avesaath, P., Appeltans, W., Arvanitidis, C., Aspden, R.,
Austen, M., Boero, F., Bouma, TJ., Boxshall, G., Buchholz, F., Crowe, T., Delaney, A.,
Emblow, C., Feral, JP., Gasol, JM., Gooday, A., Harder, J., Ianora, A., Kraberg, A.,
Mackenzie, B., Ojaveer, H., Paterson, D., Rumohr, H., Schiedek, D., Sokolowski, A.,
Somerfield, P., Sousa Pinto, I., Vincx, M., Węsławski, JM., Nash, R.
This publication comprises a synopsis of the results from the MarBEF project (2004-2008).
The success of the project was made possible by the MarBEF partner institutes and associate
members. Our acknowledgments to all who contributed research findings and articles for this
publication, and to those whose work does not feature in these pages.
Editor – Róisín Nash
Chapter coordinators Chris Emblow, Ward Appeltans, Mel Austen, Geoff Boxshall,
Fred Buchholz, Tasman Crowe, Carlo Heip, Herman Hummel, Henn Ojaveer, Dave Paterson,
Pim van Avesaath, Doris Schiedek
Task team – Christos Arvanitidis, Rebecca Aspden, Nando Boero, Alyne Delaney, Jean-Pierre
Feral, Pep Gasol, João Gonçalves, Andy Gooday, Jens Harder, Adrianna Ianora, Brian Mackenzie,
Heye Ruhmor, Paul Somerfield, Isabel Sousa Pinto, Magda Vincx, Jan Marcin Weslawski
EC officers: Hartmut Barth, Piia Tuomisto
Design – Cóilín MacLochlainn
Illustrations – © Ferdinando Boero (concept); Alberto Gennari (art); Fabio Tresca (graphics)
© Copyright MarBEF 2009
All rights reserved. No part of this publication may be reproduced or transmitted
in any form or by any means without permission.
This publication to be refered to as: Heip, C., Hummel, H., van Avesaath, P., Appeltans, W.,
Arvanitidis, C., Aspden, R., Austen, M., Boero, F., Bouma, TJ., Boxshall, G., Buchholz, F., Crowe,
T., Delaney, A., Emblow, C., Feral, JP., Gasol, JM., Gooday, A., Harder, J., Ianora, A., Kraberg, A.,
Mackenzie, B., Ojaveer, H., Paterson, D., Rumohr, H., Schiedek, D., Sokolowski, A., Somerfield,
P., Sousa Pinto, I., Vincx, M., Węsławski, JM., Nash, R. (2009). Marine Biodiversity and
Ecosystem Functioning. Printbase, Dublin, Ireland. ISBN number.
Marine Biodiversity and Ecosystem Functioning EU Network of Excellence
Sustainable development, global change and ecosystems
GOCE-CT-2003-505446
I-Going where no one has gone before 1
What is it all about? 2
Why an EU network of excellence? 8
II - Exploring the unexplored 13
Treasure chest of information 14
Discoveries 19
Climate change 34
Impacts of disturbance 43
Valuation and marine planning 50
The rise and fall of biodiversity 58
III - Future issues 63
What lies ahead 64
IV - Reaching the next generation 69
Public outreach 70
Training and education 73
World Conference in Valencia 75
The economic force of SMES 77
V-Building global partnerships 79
Joint ventures and durable integration 80
VI - Appendices 85
Declaration of Mutual Understanding 86
The Valencia Declaration 90
MarBEF research projects, data and outreach 93
Table of Contents
Marine biodiversity is an all-inclusive term to describe the total variation among living organisms in
the marine realm, i.e., life in the seas and oceans. Marine systems have a series of characteristics
which distinguish them from terrestrial systems, and marine organisms play a crucial role in almost
all biogeochemical processes that sustain the biosphere while also providing a variety of goods and
services which are essential to mankind’s well-being. Biodiversity loss is one of the major
consequences of the unsustainable use of the Earth’s resources, and the aim of the establishment
of a European network on marine biodiversity and ecosystem functioning (MarBEF) was to start to
understand the large-scale, long-term changes in marine biodiversity.
MarBEF, an EU Network of Excellence, was a new way of thinking, with a bottom-up approach,
which brought together over 700 scientists from around Europe to integrate their research
excellence. The skills and expertise of these scientists, from a variety of disciplines within marine
science, was combined to address the scientific challenges on the most topical marine biodiversity
questions, to provide new insights at a scale of research never before attempted. This core strategic
research programme consisted of three research themes, namely: 1) Patterns of species diversity, 2)
What structures species diversity? and 3) The socio-economic consequences of biodiversity change.
The first challenge MarBEF scientists surmounted was the creation of a baseline from which trends
in marine biodiversity change could be detected at the relevant spatial and temporal scales. The
integration of 251 datasets, provided by more than 100 scientists from 94 institutions in 17
countries, brought new insights to ecosystem processes and distribution patterns of life in the
oceans. MarBEF has captured 5.2 million distribution records of 17,000 species.
MarBEF published 415 scientific publications, 82% of which are open-access as a result of MarBEF
joining the Open Archives initiative. These papers include several on new species discoveries, and
over the last three years a total of 137 species new to science have been added to the European
Register of Marine Species (ERMS). Recent advances in molecular technologies employed by MarBEF
scientists have indicated that a single seawater sample may contain up to 10,000 different types of
organisms, and the key microbes participating in biogeochemical cycling in different areas around
Europe have been identified. These results, along with further studies, will enable us to link
biodiversity with ecosystem functioning.
Cold-water marine caves are shown by MarBEF scientists to exhibit strong faunal and ecological
parallels to the deep sea and provide a refuge during episodes of warming. Another study on a
different marine habitat, deep sea vents, shows that the distribution of the assemblages on the
surface of vents is related to the position of the fluid venting and resulting temperature gradients.
MarBEF scientists apply the most advanced genetic technologies to study marine biodiversity and
phylogeographic structures and the results of such studies are used to help improve the way
fisheries are managed and inspected and to detect any decline of species.
MarBEF scientists working in the area of chemical ecology have discovered that bacteria
communicate with each other using single molecules, some diatom species produce chemicals that
induce abortions and birth defects in their copepod grazers, and dinoflagellates can produce potent
neurotoxins that can be transferred up the marine food chain. All of these discoveries allow a better
understanding of the role of secondary metabolites in maintaining marine biodiversity and in
driving ecosystem functioning. i
Executive Summary
MarBEF scientists identify, for the first time, distinct and potentially vulnerable populations on the
climate-change-induced edge of survival. One of the remarkable scientific findings by the network
is that, contrary to expectations, warming effects lead to higher biodiversity in the Arctic and to
simultaneous food shortages for the top predators. Concurrently, rising temperatures contribute to
an overall increase in fish species diversity in the North Sea, changes in phytoplankton assemblages
are recorded in Mediterranean waters, and shifts in different elements of the deep sea-bed
communities at the Porcupine Abyssal Plain are attributed to the North Atlantic Oscillation (a
climatic phenomenon).
Evolutionary effects of fishing on fish biodiversity have indicated that fish populations may be
becoming more vulnerable (and less resilient) to perturbations such as fishing, climate change and
invasive alien species. Also, increased river inputs, due to climate change, may alter food webs and
fisheries. MarBEF scientists show that alterations of key species abundances affect ecosystem
functioning more than changes in species diversity, and only some types of human disturbances
have strong effects on the stability of rocky shore assemblages.
MarBEF scientists identify and define specific ecosystem goods and services provided by marine
biodiversity and suggest that a goods and services approach has the capacity to play a fundamental
role in the ecosystem approach to environmental management. Marine biological valuation in the
form of maps developed by MarBEF have the potential to be used as baseline maps for future
spatial planning in the marine environment. MarBEF develops a demonstration prototype of a
decision support system (MarDSS) for identifying and selecting alternative solutions for the
protection of marine biodiversity.
MarBEF scientists have focused on and identified many critical marine biodiversity issues, which are
now much clearer than before, but MarBEF has also revealed areas of weakness that require
concentrated effort, namely: impacts of global climate change; synergy of anthropogenic impacts
additional to global warming; coastal management; phase shifts: alternate stable states; habitat
diversity; ecosystem function; biodiversity diversity; the role of species; biodiversity at a genetic
level; microorganism diversity, and marine biotechnology.
ii
1
Going where no one has gone before
What is it all about?
What is biodiversity?
A definition of biodiversity that is simple and
yet comprehensive enough to be fully
operational (i.e., responsive to real-life
management and regulatory questions) is
unlikely to be found. However, intuitively
biodiversity equals the diversity of life on Earth.
According to the Convention on Biological
Diversity, biodiversity is ‘the variability among
living organisms from all sources including,
inter alia, terrestrial, marine and other aquatic
ecosystems and the ecological complexes of
which they are part; this includes diversity
within species, between species and of
ecosystems.’
Biodiversity thus encompasses genetic diversity,
species richness and habitat heterogeneity
(rather than ecosystem variability). These three
components are linked, obviously so between
genes and species and somewhat less clearly
between species and habitats. Because these
three aspects are not easily reduced to a simple
physical unit that can be studied, biodiversity is
a somewhat abstract and even mythical
concept.
In practice and also in public perception, and
implicit in the day-to-day practice of many
scientists, biodiversity often equals species
richness, the number of species in a certain
area or volume of the biosphere. Species
richness and genetic diversity are studied and
understood using organisms and their
molecular products but increasingly, attributes
of whole plant and animal communities and
habitats can be measured, e.g., through remote
sensing.
Biodiversity present today is the result of over
two billion years of evolution, shaped by natural
processes and increasingly by humans, whose
impact is now leading rapidly to the sixth great
extinction crisis in the history of life on Earth.
What is marine biodiversity?
The three domains of life, bacteria, archaea and
eukarya, are present in the marine environment.
In addition to which, there are viruses,
infectious agents that are unable to grow or
reproduce outside a host cell. Almost 230,000
species of marine plants and animals, and a few
thousand bacteria and archaea, have been
scientifically described. This known biodiversity
represents only a fraction of the number of
species existing in most groups (possible
exceptions are the better known macrophytes
and seagrasses of coastal environments and the
pelagic macroscopic fauna and flora of the open
ocean).
For animals and microbes, the exploration of
environments that are difficult to access, such
as the deep-sea floor, chemosynthetic
environments or marine caves, and the
application of new technologies are constantly
yielding new species at a higher taxonomic
level, and in some cases up to phylum level.
The availability of rapid sequencing
technologies has shown that variability in the
microbial domain, including the small
eukaryotes, is extremely high and that tens of
thousands of ‘species’ may occur in a single
litre of sea water. The estimates of the number
of marine species that remain to be described
are therefore very uncertain.
Why marine biodiversity
is so important
The theoretical foundations as well as the
experimental approach required to understand
marine biodiversity are very poorly developed in
general, particularly so when compared to
terrestrial ecology. In fact, the whole literature
is so dominated by theory developed for
terrestrial ecosystems that until recently one
could hardly find mention of a marine
biodiversity field. One basic question is whether
terrestrial and marine systems are similar
2
3
11Life originated in the sea and is therefore much older than life on land. As a
consequence the diversity at higher taxonomic levels is much greater in the sea, where
there are fourteen endemic (unique) animal phyla in comparison to only one endemic
phylum on land. There is also a remarkable diversity of life-history strategies in marine
organisms. The sum total of genetic resources in the sea is therefore expected to be much
more diverse than on land.
2The physical environment of the seas and land is totally different. Marine organisms live
in water; terrestrial organisms live in air. Environmental change in the sea has a much
lower frequency than on land, both in time and in space.
3Marine systems are more open than terrestrial ones and dispersal of species may occur
over much broader ranges. Although most species in the ocean are benthic and live
attached to or buried in a substratum, in coastal seas a very large proportion have larvae
that remain floating in the water for a period of days to months. These high dispersal
capacities are often associated with very high fecundities and this has important
consequences for their genetic structure and their evolution.
4The main marine primary producers are very small and often mobile (phytoplankton),
whereas on land primary producers are large and static (plants). The standing stock of
grazers in the sea is higher than that of primary producers; the opposite is true on land.
Ocean productivity is on average far lower than land productivity. In the largest part of the
ocean, beneath the thin surface layers, no photosynthesis occurs at all.
5High-level carnivores often play key roles in structuring marine biodiversity, but are
exploited heavily, with unquantified but cascading effects on biodiversity and ecosystem
functions. This does not occur on land, where the ecosystems are dominated by large
herbivores and increasingly by humans, who monopolise about 40% of the total world
primary production.
6A greater variety of species at a higher trophic level is exploited in the seas than on the
land: man exploits over 400 species as food resources from the marine environment,
whereas on land only tens of species are harvested for commercial use. Exploitation of
marine biodiversity is also far less managed than on land and amounts to the strategy
that hunter-gatherers abandoned on land over 10,000 years ago, yet exploitation
technology is becoming so advanced that many marine species are threatened with
extinction. Insufficient consideration has been given to the unexpected and unpredictable
long-term effects that such primitive food-gathering practices engender (Duarte
et al.,
2007).
7All pollution (of air, land and freshwater) ultimately enters the sea. Marine biodiversity
is thus most exposed to and critically influences the fate of pollutants in the world. Yet
marine species are probably least resistant to toxicants. The spread of pollutants in marine
food chains, and therefore the quality of marine food, is uncontrollable by man.
The distinctive features of marine biodiversity
(Heip
et al.,
1999)
enough to allow theory from one domain to be
used for the other. Most probably this is not the
case. Marine systems have a series of
characteristics which distinguish them from
terrestrial systems (see panel, page 3).
There is probably less species diversity and
more genetic diversity in the marine
environment than on land. If one looks at the
arthropods, the insects and chelicerates on land
and the crustaceans in the oceans, the
difference is striking. A single tree in a tropical
forest may harbour over a thousand species of
insects, whereas the entire planet harbours only
eighty species of euphausiids. This indicates
that the mechanisms of speciation are very
different in the sea and that competition for
resources does not constitute a dominant
selective pressure (although you will find more
species in fine-grained marine sediments than
in the water column).
The upper water column has a very dominant
vertical gradient in light availability and nutrient
concentration, but more species may exist in
the plankton (especially the micro- and
picoplankton) than one might expect. This was
called the paradox of the plankton by
limnologist GE Hutchinson (1959) and was later
applied to the marine environment by Margalef
(1968).
However, no studies have attempted to define
resources in the sea at the same level of detail
as is customary in the terrestrial environment.
Overall, the smaller number of marine species
make it reasonable to assume that the
mechanisms of diversity generation and
maintenance are different on land and sea.
Goods and services
Marine organisms play a crucial role in almost
all biogeochemical processes that sustain the
biosphere, and they provide a variety of
products (goods) and functions (services) which
are essential to mankind’s well-being. Goods
include marine foods (about 100 million tonnes
produced annually) and natural substances,
ingredients for biotechnology and
pharmaceuticals, and even land (e.g., the
carbonate platforms that make up the
Bahamas), and these substances are mainly
delivered by macroscopic organisms.
The rate and efficiency of the processes that
marine organisms mediate, as well as the range
of goods and services that they provide, are
determined by interactions between organisms,
and between organisms and their environment,
and therefore by biodiversity. These
relationships have not yet been quantified and
we are at present unable to predict the
consequences of loss of biodiversity resulting
from environmental change, in ecological,
economic or social terms.
Besides goods, marine ecosystems deliver
services that are essential to the proper
functioning of the Earth. These services include
regulation of climate, the production and
mineralisation of organic material, the storage
of carbon, the storage and detoxification of
pollutants and waste products from land, the
buffering of the climate and of climate change,
coastal protection (mangroves, dune-beach
systems, coral reefs) and regulation of the
biogeochemical cycles in general.
4
Many species of coastal plankton are active for a short time and
remain in the sediments as resting stages, sometimes for very
long periods.
© F Boero, A Gennari, F Tresca
Marine organisms play crucial roles in many of
the biogeochemical processes that sustain the
biosphere. The carbon and nitrogen cycles are
dominated by ocean processes and by micro-
organisms in the oceans, but the interplay
between natural processes and human activities
is becoming increasingly important.
Two examples of major processes involving
carbon and nitrogen are primary production
and nitrogen fixation. A limited number of
species account to a large extent for the
magnitude of these processes, and the
characteristics of such species, as shaped by
natural selection, may be important to
understanding global change.
Thirty years ago, the major carbon fixers in the
oceans had not yet been discovered.
Cyanobacteria of the genera
Prochlorococcus
and
Synechococcus,
organisms of around 1m
in size, are now known to be responsible for as
much as 30% of all global primary production.
It is not clear what impact human activity may
have on the biodiversity of microorganisms in
the open sea, or what the consequences might
be. One example of an interaction is the
limitation of primary production by iron
availability in large parts of the world’s oceans;
this limitation could be modified by direct
(fertilization) or indirect (climate change)
human action. Another possible impact is
increasing CO2uptake by seawater, leading to a
lowering of pH (greater acidity). This may have
important consequences for organisms such as
Emiliania,
which besides being photosynthetic
are also important calcifiers.
When this simple picture holds – i.e., that
overall the goods in the oceans are provided by
macro-organisms and the services by micro-
organisms – it is clear that the marine food web
should be a central point of attention and
research to clarify the consequences of human
activity. Only in a multidisciplinary approach
can we hope to understand what the
interactions between species and
biogeochemical cycles really mean in terms of
global change. This requires more directed
exploration, description and experimentation
effort as well as a modelling framework. This
framework can only be put together by a new
scientific network.
Valuation and use
of marine biodiversity
The economic value of harvestable marine
biodiversity is very high, and the valuation of
goods and services has been the subject of
much research and debate. Although it is
possible to attribute monetary value to many
goods and services and to show that this value
can be extremely high, it is also important to
recognize that non-use values such as
intellectual interest, aesthetic pleasure and a
general sense of stewardship towards the non-
human life of our planet are important
prerequisites for public support of the
conservation and sustainable use of the marine
environment.
Biodiversity is a key consideration in
understanding human exploitation of the living
resources of the oceans, whether they be fish,
invertebrates, natural products or enjoyment
and beauty of the environment; it all depends
heavily on which species we are considering. If
one species of fish disappears, it cannot just be
replaced by another: taste is species-specific
and so are human consumer interests. In terms
of conservation of natural resources and
sustainable exploitation of living marine
resources, marine biodiversity is therefore very
important.
It is clear that exploitation of marine
biodiversity has increased dramatically in
intensity over the last century. With the
increasing power and range of fishing vessels,
more and more large species have seen their 5
populations plummet. Larger and then smaller
whale species were the first to go, and while
these species are now protected, they are still
only recovering. Large predatory fish such as
tuna have been decimated in recent years. Tens,
perhaps hundreds, of millions of sharks are
mutilated and slaughtered each year. Bottom
trawling has destroyed benthic habitats
worldwide. Deep-sea fish such as the orange
roughy have become increasingly targeted as
the fisheries descend to water depths greater
than 1km. The worldwide decimation of the top
trophic levels of the marine food webs have
cascading effects down to the level of the
phytoplankton.
Fisheries and aquaculture put heavy pressure
on a number of species. Both demersal and
pelagic fish species have undergone major
changes in abundance and population
structure, even in the vast areas of the open
ocean. Aquaculture puts an additional pressure
on fish stocks as the most valued species are
often fed on other fish species and as genetic
diversity is eroded. The continued effects of
pollution and eutrophication are well
documented around the world, especially near
industrial areas and where agricultural activities
are high. The introduction of exotic species,
where humans serve as a vector, is accelerating
enormously, mainly due to transport in ballast
water and the physical removal of
biogeographical barriers. This threatens to
change biological communities and lower the
global marine gene pool, as successful species
tend to be the same in different places.
Habitats are also being changed and destroyed
by a number of human activities, including
dredging (sand and gravel exploitation), deep-
sea mining (oil and gas exploitation), bottom
trawling, the blasting of reefs and the clearing
of mangroves. Perhaps most alarming is the
rapid deterioration of coral reefs worldwide,
which seems to be due mainly to rising water
temperatures and increasing phosphate
concentrations. Deep-water corals in Europe are
increasingly subject to destruction by fisheries
activities and may in the future suffer from
ocean acidification.
Marine conservation
Is marine biodiversity being lost?
Loss of marine biodiversity has been
documented extensively for larger vertebrate
and a few invertebrate species which are
directly exploited by man. One of the most
spectacular examples is the loss of diversity in
pelagic fish due to the long-line fisheries of a
number of nations (Myers & Worm, 2003).
Marine turtles worldwide, including in Europe,
have undergone dramatic declines. Marine birds
are the most important victims of accidental oil
spills, such as recently from the
Erika
in Brittany
in 1999 and the
Prestige
off Spain in 2003.
Marine mammals such as monk seal, harbour
porpoise and some dolphin species have
disappeared from some areas. However, there
are examples of spectacular recoveries of
marine mammal populations after protection,
such as several seal species in Europe and sea
lions, sea otters and some whale species
elsewhere.
Only a few marine species have gone
completely extinct, as far as we know. Still, the
threat is there and protection of marine species
and conservation of marine areas are on the
political agenda and have been for many years.
In many EU countries coastal marine reserves
exist that protect high diversity areas and may
serve as reserves from which other areas can be
repopulated. Slowly but surely, marine
protected areas in the Natura 2000 framework
are being established. Fisheries are regulated
by establishing quotas for individual species,
based on a virtual population analysis based on
abundance and size. Because basic statistics
exist for a number of fish populations, the
long-term trends of biodiversity of pelagic and
6
demersal fish are known for a number of areas.
The spectacular decline of large pelagic fish
species due to long-line fishing by a number of
countries has been mentioned. In general, the
average trophic level as well as the average size
of exploited fish populations has decreased
over the last decades. This is the concept of
fishing down the food chain. Since top
predators are removed, the structure of the
food chain changes as well. Smaller species
tend to increase in number, putting more
grazing pressure on the zooplankton, which in
turn releases the phytoplankton. Such changes
may therefore increase primary production and
the capacity of the oceans to absorb excess
CO2, but this is very speculative. Nevertheless,
the notion that fisheries regulations require an
ecosystem approach has gained momentum
and is now appearing in many policy
documents. 7
One reason why it is so difficult to clearly
establish the reasons for changes in biodiversity
is that, besides changes in food webs due to
direct human exploitation, there are also long-
term changes that are probably due to climatic
factors. One of the best known examples is the
changing distributions of copepod species in
the Atlantic Ocean, as described in the work of
Gregory Beaugrand and his colleagues from
SAPHOS (Beaugrand
et al.,
2002). Over the last
decades there has been a gradual shift in
copepod distributions from south to north. This
shift may be having direct consequences for
fisheries as there appears to be a positive
correlation between the abundance of copepods
and that of gadoid fish.
References
Beaugrand G, Reid PC, Ibanez F, Lindley JA, Edwards M
(2002). Reorganization of North Atlantic marine
copepod biodiversity and climate.
Science
296
1692-1694.
Duarte CM, Marba N, Holmer M (2007). Rapid
domestication of marine species.
Science
316
382-383.
Heip C, Warwick RM, d’Ozouville L (1999). A European
Science Plan on Marine Biodiversity. European
Science Foundation, Strasbourg.
Hutchinson, GE (1959). Homage to Santa Rosalia or Why
are there so many kinds of animals?
Am.Nat.
93
145-159.
Margalef R (1968). Perspectives in Ecological Theory.
Chicago University Press.
Myers RA, Worm B (2003). Rapid worldwide depletion
of predatory fish communities.
Nature
423
280-283.
As with climate change, biodiversity loss
is one of the major consequences of the
unsustainable use of the resources of the
Earth. This is as true for the marine
environment as it is for the terrestrial
one.
It is difficult to judge which biodiversity
changes are due to direct human impact,
but most evidence suggests that coastal
and open ocean marine species are under
heavy pressure in most parts of the world
from the following five major factors:
Overexploitation of resources
Pollution and eutrophication
Introduction of invasive ‘alien’
species
Habitat destruction (e.g., reefs,
mangroves, habitat loss as a result
of sand and gravel exploitation,
etc)
Global climate change and
acidification of the sea.
Threats to marine
biodiversity
The introduction gave an overview of the
reasons and arguments that led to the creation
of the MarBEF (Marine Biodiversity and
Ecosystem Functioning) Network of Excellence
(NoE). MarBEF (www.marbef.org) was the first
initiative of its kind funded under the EU Sixth
Framework Programme.
Networks of excellence were a new way of
thinking, designed to strengthen scientific and
technological excellence on a particular
research topic through the durable integration
of the research capacities of the participants.
They aimed to overcome the fragmentation of
European research by gathering the critical
mass of resources and expertise needed to
provide European leadership.
For MarBEF, the network represented a huge
challenge and a huge opportunity. It brought
together over 700 scientists from 95 separate
institutes in 24 European countries with the aim
of integrating research from a variety of
disciplines within marine science and providing
training, exchange and outreach opportunities
and initiatives that will be of huge importance
both to science and society.
Better integration of research helps to support
the legal obligations of the EU and its member
states and of associated states for the
Convention on Biological Diversity, the OSPAR,
HELCOM, Barcelona and Bucharest Conventions,
as well as EU directives (Bird Directive, Habitat
Directive, Water Framework Directive and more
recently the Marine Strategy Framework
Directive).
MarBEF NoE
The challenges and obstacles
The new instrument and the dimension of the
network posed a challenge to the management
of MarBEF. MarBEF was the first NoE to be
installed and therefore the corresponding
managerial and administrative mechanisms had
to be adjusted. The increasing number of
members in the MarBEF NoE, and the
corresponding increase in the managerial
burden and amount of paperwork (despite the
efforts of the European Commission to
streamline the administration of FP projects),
together with the finite resources for the
management of the consortium, were
challenges to manage in a timely and proper
fashion.
The success of the network was achieved only
through the huge efforts and patience of the
management team and the individual MarBEF
members who, like all research institutions,
were more interested in the science than in the
project management and paperwork. It was
through the integration made possible by the
network – which created so many unique
scientific challenges and new insights – that
the related managerial burden was sufficiently
counterweighted. This involved a high degree of
adaptability of the MarBEF members.
Recipe for success:
a bottom-up approach
Despite the burden of deadlines for reportage,
the many forms that needed to be completed,
and uncertainties in budget and planning, the
members kept on supporting and focusing on
the goals of the network. Although one may
think this is normal, we believe that the way
MarBEF was organised and managed
significantly contributed to its success.
MarBEF had a strong, bottom-up approach
involving the members from the start and
allowing them to propose and participate in
joint integrative research activities, training
exercises and workshops that supported the
main aims of the NoE. This increased the
commitment of the members to the project, and
thus the integration.
A novel approach
8
9
The science
In Europe, we have world-class marine
scientists with outstanding skills and expertise
in their disciplines. MarBEF united these
eminent marine scientists under one network,
thereby bringing this dispersed scientific
excellence together to create a virtual European
centre of excellence in marine biodiversity and
ecosystem functioning.
One of the basic problems that was at the heart
of the MarBEF proposal in 2003 was the
challenge of understanding large-scale and
long-term changes in marine biodiversity in
Europe. Although a number of studies on
marine biodiversity existed, there was no
programme that tried to establish the baseline
from which trends in marine biodiversity
change could be detected at the relevant spatial
and temporal scales. Such a baseline would
encompass an inventory of the marine species
in Europe (now at about 32,000 plants and
animals). One of the first objectives that were
formulated within MarBEF was to bring together
the numerous data on marine biodiversity
species richness that existed in many research
institutes but were never compared and
synthesized to provide a picture for the entire
continent. MarBEF has been extremely
successful in this objective.
The MarBEF network of scientists addressed the
most topical questions in marine ecology,
biogeochemistry, fisheries biology, taxonomy
and socio-economics in Europe through a core
strategic programme which consisted of three
themes.
Theme 1: Patterns of
species diversity
Before we can answer the question of why
biodiversity varies, we need to know the basic
patterns of its distribution in space and time.
The most fundamental data on diversity are the
numbers of species in different places. It is a
fundamental problem for marine biodiversity
studies that this is largely unknown. There are
some exceptions, such as some animal groups
from the zooplankton, a number of plant and
10
animal species from intertidal and shallow
subtidal zones, and increasingly the microbial
flora and fauna from hydrothermal vents. But
we know next to nothing about the distribution
and the dynamics of the large majority of
species living in the sediments covering
millions of square kilometres of the deep-sea
floor.
Terrestrial ecologists have used geographic
distributions of species extensively and have
discovered relationships between these data
and latitude, climate, biological productivity,
habitat heterogeneity, habitat complexity,
disturbance, and the sizes of, and distances
between, islands. Several of these relationships
have suggested mechanisms that might
regulate diversity, but a general and
comprehensive theory of diversity accounting
for most or all of these relationships does not
exist.
Spatial scale is the overriding variable that
needs to be considered when discussing the
changes in diversity and what has caused these
changes. Definition of scales is not
straightforward, neither in terrestrial nor in
aquatic environments. Scales are often defined
from the perception of the human observer and
less as a function of the species or communities
considered. It is customary to distinguish
between local, regional and global spatial
scales. Locally, species diversity in any locality
is seen as a balance between two opposing
forces. On the one hand, local abiotic
processes, interactions between species and
chance tend to reduce diversity; on the other
hand, immigration from outside the locality
tends to increase diversity. Each local
population is seen as a sample from a larger
species pool. Theories on larger, mesoscale
patterns take migration and dispersion
explicitly into account. The metapopulation
concept and connectivity of land(sea)scapes are
central to this approach. Global patterns are, for
instance, latitudinal gradients. Within most
groups of terrestrial organisms the number of
species reaches its maximum in tropical
latitudes and decreases both northward and
southward toward the poles. In many cases the
latitudinal gradient in diversity is very steep.
Tropical forests, for example, may support ten
times as many species of trees as forests with
similar biomass in temperate regions (Latham
and Ricklefs, 1993).
Since many factors vary in parallel with latitude,
the causal mechanisms that explain such
patterns are difficult to distinguish and,
moreover, nearly all studies are from terrestrial
environments. In marine communities, the
existence of such patterns over large
geographical scales has only rarely been
studied (Rex
et al.,
1993). Whether they are as
widespread as in the terrestrial environment is
questionable, but even in terrestrial
environments the general trend in diversity is
sometimes reversed, as it is for shorebirds,
parasitoid wasps and freshwater zooplankton,
of which more species occur at high and
moderate latitudes than in the tropics. These
counter-examples may reflect the latitudinal
distribution of particular habitat types, the
history of the evolution of a taxon, or ecological
circumstances peculiar to a particular group.
Theme 2: What structures
species diversity?
The second main question that MarBEF
addressed was to understand why biodiversity
changes and what the consequences of these
changes are for ecosystem functioning.
Traditionally, species interactions are
considered to be important for structuring
biological communities, but this has not been
investigated in great detail and has not been
shown to be true also for the open ocean.
Experimental work in the marine environment
to test hypotheses is mostly known from
intertidal areas that are well accessible for
controlled experiments. Also, modelling of
11
marine systems has been part of this effort.
Furthermore, the importance of species
identities and species interactions for regulating
biogeochemical cycles, as supported mainly by
microorganisms, needs further study, which has
become extremely urgent in view of the rapid
changes in climate and biodiversity itself.
The composition of species assemblages
changes constantly. Species disappear and
appear all the time. But how does that impact
the ecosystem? One of the great challenges of
contemporary science has been the elucidation
of the link between biodiversity and ecosystem
functioning. Cycles in the biosphere have been
known to operate through biological agents for
at least two centuries. But the question of
whether the precise identity of these agents
matters is still looming large. In the oceans,
where most of the cycles are driven by
microbes, the question is even more pertinent
than on land: we now know that there are
endless numbers of ‘species’ and long tails in
the species abundance curves of relatively rare
species. Redundancy therefore seems to be
almost inevitable; if one species disappears
another will appear and take over its
functionality. Biodiversity then becomes a
buffering capacity factor of an ecosystem.
Theme 3: Socio-economic
consequences
Finally, MarBEF has looked at the socio-
economic consequences of biodiversity change.
Problems of valuation have been discussed,
including valuating the intrinsic biological
characteristics of certain communities and
areas. This is needed to bring the study of
biodiversity into the realm of socio-economic
sciences and is considered important for
policy-making, e.g., in spatial planning. With
the current economic crisis, which catalyses
new economic thinking, and an increased
awareness of the environmental constraints to
economic growth and development, the chances
that biodiversity will at last be taken seriously
by economists and politicians have increased,
but the intellectual framework and even the
paradigm shift that is required still needs
considerable input and support.
Epilogue
The legacy of MarBEF
When we started the MarBEF network of
excellence, biodiversity was hardly known by
the general public and not considered an
important feature, let alone a problem or an
asset of marine ecosystems. All this has
changed greatly in terms of what we know
about the oceans, in terms of understanding
how the oceans work, and in terms of how we
handle the problems of the oceans and its
inhabitants.
MarBEF has been something unique. It was the
first network of excellence, a new instrument in
EU Framework Programme 6 to support the
development of the European Research Area.
This volume, which summarizes the main
scientific results from MarBEF, hopefully reflects
the feeling of excitement that has stimulated
hundreds of the best European marine
scientists to devote five years of their attention
to helping it thrive. Not for the money –
although financial support has been substantial,
though it had to be shared by the original 53
partners – but out of enthusiasm and a sense of
responsibility and urgency. The planet is
changing, and the oceans as well. Over the five
years of MarBEF, we have witnessed society
becoming aware of the grave consequences of
overfishing, of acidification, of physical
disturbance and, above all, of the effects of
climate change. There is now a community of
European scientists who have the experience to
work together and the expertise to help adapt
human society to the coming changes. This is
the most important legacy of MarBEF.
12
With the advent of the European Marine and
Maritime Strategy and its requirements for good
ecological status of marine waters, the need to
understand marine biodiversity changes and
their consequences for stability and use of
marine ecosystems will only become more
urgent. Some of the priorities that we need for
the future are further efforts to map
biodiversity, including the genetic and habitat
components and especially the relationship
between them and species richness; data
integration and accessibility, and establishing a
network for observation and early warning of
biodiversity changes that covers most of
Europe’s coast. After all, more than half of the
EU is under water and this fraction is only likely
to increase.
The future
MarBEF will continue after EC funding has
ceased – because MarBEF members are of the
opinion that multidisciplinary marine
biodiversity research in Europe essentially
needs long-term concentration and integration
at large scale, and that the integrative bottom-
up approach within MarBEF is the proper
mechanism to accomplish this. MarBEF has
reached the critical mass to promote, unite and
represent marine biodiversity research at a
global scale, with 95 institutes as members, all
of which are active in marine biodiversity
research. Therefore, it is beneficial to all if the
network is kept alive and active. In preparation
for such a lasting infrastructure, MarBEF is
cooperating with MARS (the European Network
of Marine Research Institutes and Stations) and
Marine Genomics Europe to extend the network
of institutes involved in marine biodiversity
research in Europe and beyond.
References
Latham RE, Ricklefs RE (1993). Global patterns of tree
species richness in moist forests. Energy-diversity
theory does not account for variation in species
richness.
Oikos
67.
Rex MA, Stuart CL, Hessler RR, Allen JA, Sanders HL,
Wilson GDF (1993). Global-scale latitudinal
patterns of species diversity in the deep-sea
benthos.
Nature
365 636-639.
A glimpse at life within our oceans.
© Robert Hofrichter, ImagDOP
13
Exploring the unexplored
Treasure chest of information
Fishing for data
Scientific data on marine biodiversity is very
much fragmented and scattered over many
laboratories all over the world, where they are
often available only on paper or in old
electronic format, stored away and at risk of
getting lost. In the past, many research
expeditions have gathered biodiversity data
which has been funded by government bodies,
i.e. taxpayers’ money. The results of these
surveys produced enormous quantities of data
which could potentially be of huge importance
to the scientific community at large and yet they
sit gathering dust on a shelf – a crime to
society!
MarBEF scientists recognised this problem and
consequently built a framework and
infrastructure to increase the availability and
sharing of data which was previously at risk of
being lost. Now all this data has been quality
controlled and brought together in a single,
properly archived system where it will remain
available for future generations.
MarBEF’s work through the integration
of datasets is bringing new insights to
ecosystem processes and distribution
patterns of life in the oceans.
Key to the management of data was the
creation of the “Declaration of Mutual
Understanding for Data-sharing” (Annex 1).
This document provided a solid basis of trust
between MarBEF and non-MarBEF data
providers, and was instrumental in providing an
incentive for collective scientific work. It
resulted in the collection of 251 datasets
provided by more than 100 scientists from 94
institutions in 17 countries.
Databases
Large-scale marine environment datasets are
scarce, so there is a need to integrate and
manage local datasets in an alternative way, so
that they meet the requirements for data and
information on a global scale, and to support
decision-making. MarBEF has data records
ranging from the deep-sea to the coastal zone
and from the Arctic to the Antarctic; it has built
the world’s largest databases on
macrobenthos, meiobenthos and pelagic marine
species. Three scientific projects within MarBEF
alone have created thematic databases and
integrated 190 different datasets, containing
about 1,000,000 distribution records from
European seas.
MarBEF has captured 5.2 million
distribution records of 17,000 species
in all the European seas and many
of the world’s oceans.
Large temporal and spatial biological datasets
are essential for the study and understanding of
long-term distribution and abundance patterns
of marine life and how they have changed over
time. The analysis of this data allows
comparisons to be made between different
regions and habitats, to examine broad-scale
spatial and temporal patterns in biodiversity
and to explore implications from changes. The
data needed for this approach could never be
14 Sorting benthic fauna species during a sampling campaign.
© Karl Van Ginderdeuren
sampled by scientists or research groups due to
limitations in infrastructure, time and money.
The integrated database of MacroBen
(European MacroBenthic fauna)
is an important tool for studying
and understanding large-scale,
long-term distribution and abundance
patterns of marine benthic life.
As a consequence of the ever-growing
anthropogenic pressures on the sea floor, there
is an increased need for sustainable
management. Good management decisions
need to be based on sound scientific
information on the ecosystem function and the
diversity of the organisms present. Assessing
the biodiversity of large areas based on field
sampling is a long and expensive process.
Therefore, tools predicting and mapping
biodiversity are an important tool for managers
to underpin their decisions.
Scientists within the MarBEF project MANUELA
(Meiobenthic And Nematode biodiversity:
Unravelling Ecological and Latitudinal Aspects)
modelled the distribution of roundworms
(nematodes) and meiobenthos such as
copepods to develop techniques that allow for
mapping of biodiversity.
MarBEF is mapping diversity
to support ecosystem management
and decision-makers.
The MarBEF LargeNet (Large-scale and long-
term Networking on the observation of Global
Change and its impact on Marine Biodiversity)
database currently contains over 4,500
taxonomic names and more than 17,000
sampling locations, representing almost
542,000 distribution records.
Analysis of data collected by ArctEco
from the All Taxa Biodiversity Inventory
site at Hornsund (77°N, Svalbard) in the
Arctic shows that the marine benthic
biodiversity has increased by 50%
(>1,415 marine species) in recent years. 15
FFiigguurree 11::MarBEF data is available through EurOBIS, the largest online queryable public source of European marine biological
data. EurOBIS contains 5.2 million species distribution records from 210,832 localities and 32,225 taxa in all the European seas
and many of the world’s oceans.
© VLIZ
It is anticipated that, following the publication
of the LargeNet analyses, more datasets will be
attracted into the system. This huge enterprise
will be continued in the EMODNET (European
Marine Observation and Data Network) project
of FP7 that will support the European Marine
and Maritime Strategy.
Taxonomic information
Conservation and sustainable use of biological
resources are accepted as the way of achieving
healthy ecosystems. Biodiversity information,
whose basic tool is taxonomy, is the foundation
for conservation. Taxonomy has been defined
as “the scientific discipline of describing,
delimiting and naming organisms, both living
and fossil.” Taxonomy is of fundamental
importance for understanding the ways through
which biodiversity may be changing in the
context of climate change and the ways that
biodiversity may provide goods and services to
society.
MarBEF has spent considerable effort on
taxonomy through three main activities: the
Taxonomic Clearance System and the
PROPE-taxon and MANUELA projects. The
Taxonomic Clearance System scheme
successfully addressed the taxonomic
identification bottleneck and streamlined the
process of identification of specimens and the
description of new species. PROPE-taxon
provides European taxonomists with a
community-driven e-platform that acts as a
web-accessible depository for integrated
taxonomic knowledge systems (e.g. databases,
taxonomic keys, biogeographic data) based
upon existing software and technologies
(Scratchpads system developed by the Natural
History Museum in London). The MANUELA
project employed a second taxonomic
information system, NeMys (developed at Ghent
University), which contains available
taxonomical literature on free-living marine
nematodes, in addition to taxonomic keys.
The correct use of names and their
relationships is essential for biodiversity
management; therefore, the availability of
taxonomically-validated, standardised
nomenclatures are fundamental for biological
infrastructures. The European Register of
Marine Species (ERMS), originally funded by the
EU MAST research programme, has been
updated by MarBEF and is used as the
taxonomic reference for checking spelling and
harmonising synonymy, thereby improving
quality control and standardising species lists.
Now an impressive total of 31,455 names of
European species are stored within this new
database.
Over the last three years the
European Register of Marine Species
has increased its species numbers
by 1,371 species, of which
10% are from species recently
described.
LargeNET found that, after matching their
species data (1,600 species) with ERMS, 17% of
the names could be moved to the status of
invalid names. These invalid names were mostly
spelling variations, typing errors or synonyms.
Without quality control procedures these
16 Øjvind Moestrup with tiny microscope. Taxonomy is often about
looking at tiny details.
© Ward Appeltans
“erratic names” would have been regarded as
extremely rare taxa and could have led to
seriously flawed analyses.
ERMS now serves as a basis for the creation of a
World Register of Marine Species (WoRMS;
www.marinespecies.org). More than 140 world-
leading experts on marine species, from 26
countries (50% from EU), are building this world
register of marine species. It will be the first
expert-validated register of names of all marine
species known to science.
Many international biodiversity programmes,
among others CoML/OBIS, GBIF, EOL,
Species2000, ICZN/ZooBank and IODE of
UNESCO/IOC, need a register of valid names
and have agreed to use WoRMS for their
purposes.
WoRMs currently contains 140,000 valid
species or 60% of the estimated number
of described marine species
in the world.
Geographical information
Geographic Information Systems (GIS) have
become indispensable tools in managing and
displaying marine biodiversity data. Within
MarBEF, we have developed a standardised
register of place names, called the European
Marine Gazetteer.
The European Marine Gazetteer is the
first international, internet-accessible
gazetteer for the marine environment.
The ultimate goal is to have a hierarchical
standard list that includes all the marine
geographical names within Europe and
subsequently worldwide. Presently, the
gazetteer includes the names of 983 European
locations, seas, islands, sandbanks, ridges,
estuaries, bays, sea-mount chains and
submarine lava tubes.
The European Marine Gazetteer is hierarchical
and thus recognises that, for example, when a
species is reported from a bay in Italy, that bay
is part of Italy, the Adriatic Sea, the 17
FFiigguurree 22::Overview of the species coverage in EurOBIS. On a fine scale (1x1 degree) our knowledge of the diversity of life is still
very sketchy (or even non-existent: see grey areas on map).
© VLIZ
Number of taxa per grid
1-102
103-425
426-1140
1141-2009
2010-3592
Mediterranean and Europe. Therefore, users can
search for all datasets holding data on a
specific area and subsequently find the species
occurring in that area, or the people and
institutes that are involved in research in that
region. Other geographical regions in the
gazetteer include the major oceans and seas,
Exclusive Economic Zones (EEZs), Large Marine
Ecosystems, FAO Fishing Areas and Longhurst
Biogeographical Provinces.
Biogeographical information
MarBEF established the European node of the
international Ocean Biogeographic Information
System (EurOBIS). EurOBIS is a freely accessible
online atlas providing species distribution
records from 174 datasets. EurOBIS is the
largest data provider to the international OBIS.
EurOBIS contains 5.2 million species’
distribution records from 210,832 localities and
32,225 taxa in European marine waters.
By combining areas defined in the
Gazetteer and the species distribution
data in EurOBIS, national or regional
species checklists can easily
be created.
Meetings and publications
MarBEF has sponsored over 150 meetings,
which has resulted in new joint research and
strong partnerships between scientists across
Europe, which has led to numerous scientific
papers already published or in press in
international journals.
MarBEF has published 415 papers
of which 220 are in peer-reviewed
journals.
The MarBEF Open Archive (MOA) contains the
digital version of published works that are held
within the MarBEF Publication Series (i.e. any
class of publication where at least one author is
a network member and in which MarBEF is
acknowledged). In addition, those papers where
MarBEF has bought unrestricted ‘Open Access’
are automatically part of this archive. MOA can
only archive those publications for which the
publishers agree on the concept and principles
of open digital archives (http://www.marbef.
org/moa).
MarBEF has joined the Open Archives
Initiative (OAI) and, therefore, 82% (389)
of these scientific papers can now be
downloaded for free.
Permanent host
The Flanders Marine Institute (VLIZ) and its
oceanographic data centre led the data
integration activities in MarBEF. All the original
MarBEF data files have been described and
archived in the Marine Data Archive. Data
generated by MarBEF, with EU funding, are
available without restrictions. However,
following the MarBEF data policy, other datasets
that are owned by the participating institutes
and/or other agencies will not leave the
repository without the consent of the data
owners.
The MarBEF data system will continue
to be an important knowledge base for
future research and storage of marine
biodiversity data in Europe.
References
Vanden Berghe, E.
et al.
(2009). Description of an
integrated database on benthic invertebrates
of European continental shelves: a tool for
large-scale analysis across Europe.
Mar. Ecol.
Prog. Ser.
382 225-238.
Vandepitte L.,
et al.
(2009). The MANUELA database:
an integrated database on meiobenthos from
European marine waters.
Meiofauna Marina
17
35-60.
Vandepitte, L.
et al.
Data integration for European marine
biodiversity research: creating a database on
benthos and plankton to study large-scale
patterns and long-term changes.
Hydrobiologia
(submitted).
18
Discoveries
The discovery of new marine organisms
continues apace, with an average of about
1,400 new species described each year
worldwide. A surprising number of these are
from European waters, which one might have
assumed were so well studied that they
contained no surprises.
In fact, over the last three years a total
of 137 species new to science have
been added to the European Register
of Marine Species.
These novelties range from microbes such as
bacteria up to vertebrates, but the majority of
newly described species are invertebrates,
partly because the formal process of naming
new bacteria has lagged far behind the rate of
discovery of new microbes.
Species
New microbes
In the ocean, microbes – or organisms from 0.2
to 100m – are very abundant. It has been
calculated that they account for about half of
the biomass on planet Earth. In the ocean,
Bacteria
and
Archaea
account for billions of
tonnes of carbon (estimates range from 3 to 14
billion) while, in contrast, the entirety of
mankind on Earth only accounts for about 0.03
billion tonnes of carbon. In a drop (one
millilitre) of seawater, one can find 10 million
viruses, one million bacteria and about 1,000
small protozoans and algae (called “protists”).
In addition to their high abundance, microbes
play a crucial role in most biogeochemical
processes occurring in the marine environment:
FFiigguurree 11::A list of molecular methodologies used to measure richness and/or eveness of microbial communities. Also shown
is the resolution of the technique. Simplified from a table assembled by the students and professors of the MarBEF training
course Genetic Fingerprints in Biodiversity Research.
Result Richness Evenness Resolution
DGGE/TGGE bands <35 bands 5-100% >0.5%
SSCP bands <35 bands 5-100% >0.5%
T-RFLP bands <200 bands 0.1-100% >0.05%
ARISA bands <500 bands 0.1-100% >0.05%
Pryosequencing 100-250bp >10,000
(454 technology) sequences
Clone libraries sequence >100 no usually >200 clones
PFGE bands <50 bands 5-100% >0.5% (genome size)
Quantitative PCR no 0.01-100%
FISH / TSA-FISH / CARD-FISH no 0.1-100%
GENETIC FINGERPRINTS focusing on richness (number of operational units, absolute abundance)
GENETIC FINGERPRINTS focusing on evenness (relative abundance)
19
they account for almost half of global primary
production and form a major part of ecosystem
respiration and nutrient recycling.
Research in recent years has shown that
microbes are not only very abundant and
important ecologically but are also highly
diverse. This huge diversity is found in
organisms that, in most cases, are similar in
morphology, but we know they are very diverse
in the functions they perform and in the widely
different genetic material (DNA) that they
contain, which is a coding for a large variety of
proteins.
Different types of proteins can be compared to
different types of machines in a factory: they
allow for great metabolic and physiological
flexibility in the microbial world. However, as
scientists cannot identify most microbes from
their appearance alone, they have to rely on
molecular methodologies to describe their
diversity. In general, these methodologies rely
on the fact that microbes share a common gene
that is so important that it has changed
relatively little throughout the evolutionary
history of life on Earth. Reconstructing the
differences in the base sequences of that gene
enables organisms to be classified in a “natural”
way that reflects their evolutionary history.
There are a variety of techniques employed to
obtain microbial diversity data (Fig. 1).
Initial reports of microbial richness in aquatic
environments suggested that there were less
than 200 different microorganisms in a typical
sample. But recent advances in molecular
technologies, such as metagenomics [sampling
genes directly from the environment], have
shown that the diversity is much greater than
previously thought.
A single seawater sample may contain
up to 10,000 different types
of microorganisms.
This is a huge diversity, particularly when
compared with the number of formally
described species of bacteria, which is fewer
than 10,000 (Fig. 2).
To understand plankton distribution and
changes, MarPLAN first needed to know how
diverse it was. Using new techniques and
partnerships that MarPLAN developed have
allowed us to answer some fundamental
questions, such as: ‘Does limited dispersal
enable the evolution of local bacterium
species?’ or conversely, ‘Does a bacterium
inhabit all European waters?’
Figure 2: Adaptation by Thomas Pommier (CNRS) of a figure by Pedrós-Alió (2006).
Fingerprinting
(DGGE/TGGE)
~30 taxa
Individuals (N)
Comprehensive Clone Libraries
(Acinas et al., Pommier et al.)
~300 taxa observed
~1,500 taxa estimated
Curtis et al. (2002)
estimation
1,000,000 taxa
Dykhuizen (1998)
estimation
100,000,000 taxa
Pure culture
isolations
<20 taxa observed
Extension
Death
Active
growth
Predation,
viral lysis
Immigration
Global dispersion
Shotgun sequencing
(Venter et al., Rush et al.)
~4,000 taxa observed
PCR + 454 pyrosequencing
(Sogin et al.)
6,000 taxa observed
~20,00 taxa estimated
Abundant Taxon rank Rare
20
21
Rhodopirellula baltica,
an abundant red
bacterium that lives attached to marine
sediment grains (originally isolated from the
Baltic Sea, or more precisely, the Bay of Kiel)
was selected to investigate these questions.
MarBEF scientists from institutes all over Europe
provided 130 water and sediment samples for
analysis, from which we obtained 70 strains,
which revealed several new species within the
genus
Rhodopirellula.
The species
R. baltica
was restricted to the Baltic Sea, the Skagerrak
and the Eastern North Sea. A second species
was present in Iceland and Scotland,
representing the North-Atlantic habitat.
Another different species was obtained from the
Adriatic Sea, but the majority of the isolates
belonged to a species present in the English
Channel, on the French Atlantic coast and in the
Mediterranean.
The presence of several species of
Rhodopirellula
in European seas showed
evolutionary species diversification
within the genus.
Molecular techniques allow the detection of the
most abundant microbes, or those that actively
participate in growth. Therefore, it allows us to
attempt to identify the main microbes that
participate in biogeochemical cycling in
different marine habitats.
Molecular techniques which help to
identify the main microbes participating
in biogeochemical cycling enable us to
link biodiversity (or at least the
“identity” component of it) with
ecosystem functioning.
The trick is to use methodologies that tell us
“who is doing what,” and “who is the most
relevant” among those that perform a given
biogeochemical function and therefore what
effect global change will have on that particular
species or strain.
Members of the MarBEF project MarMicro have
researched the identity of the key microbial
organisms in different areas. For example:-
1) Central Baltic Sea
Anoxic and suboxic bottom waters are
characteristic features of marginal and enclosed
seas and many coastal environments (Black Sea,
Baltic Sea, fjords,
etc
) and are increasing in
extent worldwide. The oxic-anoxic transition
zones are sites of element transformations
which impact the overall biogeochemical cycles
and are important on an ecosystem scale.
Furthermore, these environments can be
considered as model systems for ancient
oceans which were dominated by anoxia
throughout much of the Earth’s history. Oxic-
anoxic interfaces (chemoclines) are ideal sites
to study the link between microbial community
structure and biogeochemical transformations
(and thus between biodiversity and ecosystem
function), because distinct and measurable
processes can be related to the activity of key
bacterial or archaean species.
Studies of the central Baltic Sea redoxclines
(here defined as transition zones several metres
thick between suboxic and sulfidic water layers)
revealed the exceptional importance of
chemoautotrophic prokaryotes, which dominate
microbial abundance (20-40 % of total cell
numbers) and production. By applying
techniques that link structure with function of
prokaryotes (e.g., MICRO-CARD-FISH, SIP-RNA),
Epsilonproteobacteria
were identified as the
major organisms responsible for
chemoautotrophic production. A more detailed
study of this group in the central Baltic revealed
that
Epsilonproteobacteria
were nearly entirely
represented by one phylogenetic cluster
belonging to the genus
Sulfurimonas
. This
organism can be called a “key player” in this
habitat, mediating, for example,
chemoautotrophic denitrification. A strain of
this cluster demonstrated the exceptional
metabolic versatility which includes the capacity
22
to utilise different inorganic redox reactions as
well as to make use of different organic
substrates. This is likely to be an adaptation for
survival in pelagic redoxclines that are
characterized by steep physico-chemical
gradients but also by frequent disturbances due
to inflow and small-scale mixing events.
The study of redoxcline communities
offers many new possibilities to
examine and understand the link
between diversity and ecosystem
functioning in microbial communities.
In future, this will be done in combination with
newly-developed tools from metagenomic,
transcriptomics and proteomics.
2) Coastal NW Mediterranean Sea
On an annual basis, alphaproteobacteria are the
dominant group [29% of total counts and 70% of
bacterial clones]. The SAR11 clade is the most
abundant during spring and summer, and it
uses a variety of organic compounds that we
can use as tracers of organic matter. On
average, <10% of the SAR11 cells are active in
the uptake of aminoacids, glucose or ATP. The
Roseobacter
clade (also from the
alphaproteobacteria) is less abundant and can
be detected only in winter and spring. In
contrast
Roseobacter
cells, which constitute
only 5-10% of the community, are much more
active in the incorporation of these substrates
(Fig. 3).
The phylum
Bacteroidetes
constitutes the
second most important group and is equally
abundant throughout the year.
Gammaproteo-
bacteria
showed a small peak during summer,
but was only very abundant on one particular
day. The
Alteromonadas
subgroup of
Gammaproteobacteria
constituted a population
of highly active cells that were all actively
taking up organic matter. However, they were
quickly eliminated from the water by grazers.
This indicates that some groups of bacteria in
the NW Mediterranean act as r-strategists [fast-
growing opportunists]. They have high rates of
growth and they dominate incorporation of
FFiigguurree 33::Contribution of different bacterial groups to community structure and to the pool of really active cells. Yearly average.
Alteromonas is a subgroup of Gammaproteobacteria, and SAR11 and Roseobacter are subgroups of Alphaproteobacteria. Redrawn
from Alonso-Sáez et al. (2006) and Gasol et al. (submitted).
Contribution to community structure (%)
50
40
Alteromonas
Roseobacter
Gammaprot Alphaprot
SAR11
Bacteroidetes
30
20
10
0
0 10 20 30 40 50
Contribution to the pool of active cells (%)
23
substrates when they are present, but they are
seldom abundant. These groups would be the
Roseobacter
and the
Alteromonadacea.
Other
groups, such as the
Alphaproteobacteriaceae,
SAR11 and the
Bacteroidetes,
follow more the
alternative k-strategy, with slow growth and
relative dominance.
3) Deep North Atlantic
The bacterial and archaeal community
composition of the major deep-water masses of
the North Atlantic was followed from 65°N to
5°S, following the flow of North Atlantic Deep
Water east of the Mid-Atlantic Ridge. Using a
T-RFLP fingerprinting approach, we found that
each of the main deep-water masses is
characterized by a specific bacterial community.
In general, the diversity of bacterial
communities was about three times higher than
that of the archaeal community throughout the
water column (down to a depth of 4,500m).
Studies reveal that neither bacterial nor archaeal
diversity decreased with depth, although the
total number of prokaryotes decreased from
106 at the surface to 104 ml-1 at 4,500m.
A pronounced latitudinal gradient was detected
for ammonia-oxidizing
Crenarchaeota.
The only
two enrichment cultures of mesophilic marine
Crenarchaeota
currently available,
Cenarchaeum
symbiosum
and
Nitrosopumilus maritimus,
use
ammonia as an energy source and take up
carbon dioxide as a carbon source. Hence, it
has been generally assumed that all the Marine
Crenarchaeota Group I (MCGI) are nitrifiers. We
found that, while MCGI are putatively oxidizing
ammonia throughout the water column in the
northern latitudes, in the deep waters around
the equator only a small fraction of the MCGI
utilize ammonia as an energy source. We also
found evidence that the MCGI in the deep
temperate and (sub)tropical waters are utilizing
organic matter as substrate and hence exhibit a
heterotrophic life mode. The shift from
autotrophic, ammonia-oxidizing northern
deep-water MCGI communities to hetero-
trophic, deep-water MCGI in equatorial regions
is apparently related to the age of the deep-
water masses. Deep-water formation in the
northern latitudes transfers large amounts of
surface-water ammonia into the deep ocean
which is then oxidized to nitrate as these deep
waters age in the meridional ocean circulation.
MarBEF has identified the dominant
bacterioplankton groups in the NW
Mediterranean, the Central Baltic and
deep North Atlantic Sea in terms of
their contribution to bacterial
biogeochemical function in the
carbon and nitrogen cycles.
Invertebrates
Copepods are small crustaceans, diminutive
relatives of the crabs and lobsters, but
abundant and diverse in the oceans. There are
about 3,000 species of copepods in European
waters, and they comprise almost 10% of all
species contained in the European Register of
Marine Species. Free-living copepods are
typically the dominant group of multicellular
animals in the plankton, but they are also found
on and in marine sediments, where they are
usually second in abundance only to the
nematodes.
A new genus of benthic harpacticoid
copepod has been named
Marbefia
to
honour the outstanding contributions
of MarBEF to our knowledge
of marine biodiversity.
Marbefia
is a small, slender copepod, with a
female body length of about 0.7mm, and is
highly ornamented, with a dense covering of
fine hairs (Figs. 4 & 5).
Marbefia
is currently
known from the Southern North Sea and the
Isles of Scilly.
Copepods are also parasites on almost every
phylum of marine animals, from sponges to
chordates, including whales. For example,
sixteen copepod families are parasitic on
polychaete worms. These parasites are typically
rare and our knowledge of their biology and
distribution is extremely limited. Such parasites
are usually found by researchers studying the
hosts, so the sheer volume of sampling and
analysis that took place within MarBEF provided
an exciting opportunity to collect these very
rare animals. The diversity of new forms found
was astonishing:
In a large series of samples taken from
around the Norwegian Sea and White
Sea, a total of 11 species new to
science and three new genera of
parasitic copepods were identified.
The numerous new host and geographical
records have greatly improved our knowledge
of the host-specificity of the parasites, their
abundance and their distribution in European
waters.
24
As well as numerous new copepods parasitic on
worms, MarBEF researchers, with the support of
the Taxonomic Clearing System, also discovered
new worm species from European seas. Among
these,
Osedax mucrofloris
is perhaps one of the
most remarkable. It burrows into the decaying
bones of whale carcasses – an extremely widely
dispersed habitat – and derives nutrients from
the abundant sulphur compounds in the
carcass.
The roundworms or nematodes (phylum
Nematoda
) are one of the most species-rich
phyla of ecdysozoans (animals with cuticles),
and one of the most speciose of all animal
groups. Nematodes have successfully adapted
to nearly every ecological niche, from marine to
freshwater and from polar to tropical regions.
They are ubiquitous in freshwater, marine and
terrestrial environments, where they often
outnumber other animals both in individual
abundance and in species counts, and are
found in locations as extreme as Antarctica and
oceanic trenches.
35% (333 species) of nematode species
identified in the MarBEF project
MANUELA were new records for Europe.
Habitats
Shallow-water marine caves
Marine caves located in the littoral zone offer a
permanently dark, stable, quiescent
environment with limited food resources that
resembles, at least to some extent, the deep
sea. Because they can be visited by SCUBA
divers, these caves have tremendous potential
as accessible analogues of deep-sea habitats.
One important difference is that the water
temperature in shallow-water marine caves is
usually much higher than near the ocean floor.
Parts of the Mediterranean, where the
temperature of the deep water (~13°C) is similar
to that of the surface waters during the winter
FFiigguurree 44::Two females and a male (right) of the new genus
Marbefia. The male copepod is slightly shorter and has
modified antennules which are used to clasp onto the
female during mating.
© Geoff Boxhall
25
FFiigguurree 55::Scanning electron micrograph of a parasitic copepod,
Herpyllobius polynoes, attached to the head of its host, a
polynoid worm. Herpyllobius is an extremely modified copepod,
having lost limbs and segmentation. It feeds via an embedded
rootlet system that penetrates the skin of the host and directly
absorbs nutrients.
© Geoff Boxhall
in the northernmost part of the basin, provide
an important exception to this generalisation.
Most of the well-studied caves are located in
the NW Mediterranean and have a profile that
ascends from the outside in, trapping warm
summer waters in the upper parts. However,
one particular cave, the 3PP cave near Marseille,
has a descending profile that traps cold (~13-
15°C) water year round. Similar caves of this
type have now been discovered.
The inner parts of the 3PP marine cave
studied by DEEPSETS exhibit strong
faunal and ecological parallels to the
deep sea.
Partly within the DEEPSETS project framework, a
detailed study of the 3PP cave fauna was made.
The most striking and best-studied examples
were the carnivorous sponge
Asbestopluma
hypogea
and the hexactinellid sponge
Oopsacas
minuta,
both now also found in the bathyal
Mediterranean. Similar examples exist for less
conspicuous taxa such as bryozoans and
brachiopods. It appears that caves, particularly
descending cold-water caves, are home to an
interesting combination of marine cave fauna,
successfully-established true deep-sea species,
and an additional consortium of mobile
shallow-water taxa using caves as a shelter
from predators.
Recent research within the DEEPSETS framework
investigated the sediment-dwelling
Foraminifera
and metazoan meiobenthos,
mainly harpacticoid copepods, nematodes and
annelids. This effort, primarily concentrated on
the 3PP cave, was intended to provide
background data on cave sediment-dwelling
taxa as a basis for a temporal survey that could
be compared with deep-sea time series.
Preliminary results showed a strong gradient in
meiofaunal composition from the cave’s
entrance to the darkest parts, with a prevalence
of deep-sea components in the inner regions.
Little is known about the temporal stability of
marine caves. Seasonality is marked in the
littoral zone, and naturally affects the cave
entrance. However, seasonal fluctuations also
penetrate into the darkest parts of caves, where
allochthonous organic matter or indices such as
chlorophyll may display considerable intra-
annual variations. In addition to the slow
advection of material from outside, the
circadian movements of some cave residents
(fish, mysids) in and out of caves may transport
organic matter and thereby transmit a temporal
signal. Longer temporal trends are largely
unknown, but some marine caves have been
affected by current warming trends. A
Mediterranean-cave mysid species has been
replaced by a congener in the majority of caves
of the NW Mediterranean following a series of
unusually hot summers.
Cold-water marine caves act as a refuge
during episodes of warming such as
unusually hot summers.
There are also indications that some deep-sea
taxa (particularly sponges), which are probably
living near their thermal limit in the ‘cold-
water’ marine caves, are showing signs of
mortality during milder than average winters.
Other Mediterranean caves, such as the
26
Assemblage 1
Assemblage 2a
Assemblage 2b
Assemblage 3
Assemblage 4a
Assemblage 4b
Substratum 1a
Substratum 1b
Substratum 2
Black smoker
Flange (active)
Diffusion zone
Estimated width (m)
Immersion/depth (m)
1,681
1,682
1,683
1,684
1,685
1,686
1,687
1,688
1,689
0123456789
anchialine caves on Mallorca in the Balearic
Islands, are home to new planktonic species of
copepods, such as
Stephos vivesi,
which have
been described with the support of MarBEF’s
Taxonomic Clearing System.
Vents
Analyses of high-definition photographs and
video records conducted revealed detailed
information about the spatial distribution of
biotic assemblages on the Eiffel Tower
hydrothermal edifice (Fig. 8). This edifice is a
part of the Lucky Strike vent field and is
situated on the Mid-Atlantic Ridge, south of the
Azores. The faunal assemblages comprise
bivalves, decapods and other smaller associated
fauna ranging from polychaetes and gastropods
to bacteria.
The distribution of the assemblages
on the surface of the Eiffel Tower
hydrothermal edifice is very patchy
and is related to the position
of fluid venting and resulting
temperature gradients.
In contrast to the rapid dynamics observed on
edifices from the Pacific, the rate of change in
the Atlantic Eiffel Tower communities is clearly
lower and remained rather constant between
the years during which it was observed (1994,
1998, 2001, 2002, 2005, 2006 and 2008).
Genetics
Ecological information on most marine keystone
and foundational species is readily available,
while information about their changing
FFiigguurree 66::The east side of the Eiffel Tower hydrothermal construct in the Lucky Strike vent field (Mid-Atlantic Ridge). The map
shows the distribution of different faunal assemblages and substrates during 2006. The assemblages are characterised by different
animals species and the presence or absence of bacterial mats. The main attached animals present are the mussel Bathymodiolus
azoricus (Assemblages 1, 2a, 2b) and the alvinocarid shrimps Mirocaris fortunata and Chorocaris chacei (Assemblage 3). Substratum
1b is a bare surface with visible bacterial mats; Substratum 2 is a bare surface with whitish or greyish mineral precipitation and
possible bacteria. (Adapted from Cuvelier et al., in press: “Distribution and spatial variation of faunal assemblages on a hydrothermal
edifice at Lucky Strike vent field (Mid-Atlantic Ridge) revealed by high-resolution video image analysis.” Deep-Sea Research I.)
27
geographic distributions through space and in
time is seldom available. Temperature is a key
structuring feature of biogeographic
distribution for most organisms. Therefore, in
the context of climate change, many species
have already begun to shift their ranges. Using
genetic data, it is possible to track both past
and present changes, identify past refugia and
present-day hotspots of high genetic diversity,
and determine particular boundary edges,
which may influence dispersal abilities.
Modern approaches to molecular genetics and
advances in understanding of fish genetics have
improved our knowledge of the structure of fish
populations and their adaptation to
environmental gradients and local
environmental conditions. This knowledge
helps us to analyse the environmental basis for
spatial structure in fish populations and
examine how the spatial distribution of local
populations changes over time (e.g., whether
they expand, relocate or shrink), depending on
their physiological response to changes in
abiotic conditions, and on their genetic capacity
for adaptation. New genetic methodologies
were applied to several marine species (cod,
herring, flounder and sprat) throughout the
salinity gradient in the North Sea-Baltic Sea
area. These analyses showed that the steepest
gradient in genetic variation overlapped
spatially with the steepest gradient in salinity –
that is, in the western Baltic-Belt Sea area – and
that populations in the Baltic were genetically
distinguishable from those in the North Sea.
The advances in knowledge of fish
genetics and the new genetic
technologies can be used to help
improve the way fisheries are
managed and inspected.
For example, genetic methods can be used to
identify and trace the geographical origin of fish
sold on markets and, therefore, to identify
whether fish sold have been caught from
populations which are protected by quotas or
other conservation measures. There are now
cases in which such technologies have been
used in court proceedings, resulting in
convictions of fishermen for illegal fishing
activities.
The GBIRM (Genetic Biodiversity) project has
helped to resolve the phylogeographic structure
of a set of species at a level of detail that
enables predictions to be made about how
global and local perturbations will influence
large-scale structure and distribution in the
coming decades.
EPIC (Exon Primed Intron Crossing) is filling a
gap in the toolbox for studying animal
biodiversity. The EPIC project has helped us
identify universal genetic markers in the nuclear
genome of metazoans. Genetic (molecular)
markers provide extremely informative data to
study intraspecific biodiversity.
Despite the enormous growth of sequence
databases, nuclear markers which are
sufficiently polymorphic for population genetics
and phylogeography studies, and yet still
potentially applicable across various phyla, are
crucially needed. Numerous introns (a region of
DNA) have invariant positions, even between
kingdoms, thus providing a potential source for
such markers.
MarBEF has developed a new
bioinformatics approach to extract
promising loci from genomic sequence
databases that are applicable
to all living kingdoms,
not only animals.
Chemical ecology
Chemical ecology, as an integrative science, has
been instrumental in understanding the
function of terrestrial ecosystems. Pollination of
flowers by bees, homing behaviour of birds and
human attractiveness to a partner are some of
the many examples of chemically mediated
interactions. It is not difficult to imagine the
catastrophic consequences of the absence of
such crucial relationships. Imagine a similar
scenario without chemical interactions in the
marine environment. Many key life processes
would be compromised, such as food source
identification and selection, prey location and
capture, mate recognition and location,
chemical defence, behaviour, and population
synchronisation.
Chemical diversity in the marine realm
is an integral part of taxonomic
diversity and therefore contributes
to overall biodiversity.
Species-specific chemicals can shape
community processes such as seasonal
succession, niche structure, selective feeding
and population dynamics. Similarly, chemical
interactions mediate functional diversity,
affecting, for example, meroplanktonic larval
settlement, signalling within populations,
differential production of allelopathic
compounds and bloom dynamics.
The MarBEF ROSEMEB (Role of Secondary
Metabolites in Ecosystem Biodiversity) project
has provided a better understanding of the
roles of these chemicals in maintaining marine
biodiversity and driving ecosystem
functionality.
Microbes
Microbes sense their environment via cell-
associated and diffusible molecules such as
AHL (N-acylhomoserine lactones) that are
constantly produced by many bacteria and
diffuse through membranes into the
surrounding environment. Beyond a certain cell
density of the bacterial population and
corresponding concentrations of AHLs, a
threshold or quorum is reached, and expression
of target genes is initiated, e.g., the proteins for
light emission in luminous bacteria or
pathogenic factors that cause disease.
Quorum-sensing typically controls processes
such as swarming (coordinated movement),
virulence (coordinated attack) or conjugation
(gene transfer between cells) that require high
cell densities for success and that are essential
for the survival of the producing organisms
(Fig. 6a).
The discovery that bacteria
communicate with each other using
signal molecules has changed our
perceptions of single-cell organisms
and interspecies communication
and information transfer.
Phytoplankton
Within the plankton community, many prey
organisms use chemical defence against their
predators, either through toxin production or
feeding deterrence. Diatoms are key players at
the base of the marine food web and have
always been assumed to represent a good food
source for herbivores, but some species use
chemical defence against being grazed. The
discovery that these unicellular algae produced
chemicals such as polyunsaturated aldehydes
(PUAs) and other oxidised products of fatty acid
metabolism (collectively termed oxylipins) that
induced abortions, birth defects, poor
development and high offspring mortality in
their grazers has changed our view of plant-
animal interactions in the plankton (Fig. 6c).
Researchers in ROSEMEB have
discovered that some diatom species
produce chemicals that induce
abortions, birth defects,
poor development and high
offspring mortality on their
copepod grazers.
28
29
Although the effects of such toxins are less
catastrophic than those inducing poisoning and
death, they have insidious effects. Such
compounds may discourage herbivory by
sabotaging future generations of grazers,
thereby allowing diatom blooms to persist when
grazing pressure would normally have caused
them to crash. This defence mechanism is a
new model for the marine environment because
most of the known negative plant–animal
interactions are generally related to poisoning,
repellence or feeding deterrence, not to
reproductive failure. In fact, the production of
PUAs acts mainly as a post-ingestion signal
impacting future generations of grazers, with
lesser effects on the direct adult grazers. PUAs
have also been shown to negatively impact
other phytoplankton cells and possibly function
as a diffusible bloom-termination signal that
triggers active cell-death (Fig. 6b). So, these
compounds may have multiple functions within
plankton communities, acting as defence
molecules against predators and competitors as
well as signal molecules driving diatom bloom
dynamics and species succession patterns.
Other phytoplankton groups such as the
dinoflagellates produce potent neurotoxins that
can be transferred up the marine food chain
and have been responsible for mass fish-kills,
both wild and farmed, as well as for the deaths
of aquatic birds and mammals, including whales
and sea lions.
Dinoflagellates produce potent
neurotoxins that can be transferred
up the marine food chain.
In humans, consumption of shellfish containing
high levels of toxins can induce paralytic,
neurotoxic, diarrhetic and amnesic shellfish
poisoning. Records of human poisoning by at
least two of these syndromes date back
hundreds of years, yet the discovery and
characterisation of the molecules responsible
for this biological activity are quite recent.
Many benthic invertebrates are capable of
sequestering compounds from the food they
consume and using them as defensive
molecules against predators, and the same may
also occur in the plankton. Studies on chemical
interactions in the plankton are still in their
infancy, but there remains great scope for
research into the effects of toxins on gamete,
embryonic and larval development of
herbivorous grazers, and understanding why
zooplankton avoid consuming certain
metabolites and what happens when they do.
Seaweeds
Seaweeds have been shown to produce a large
variety of secondary metabolites with highly
variable chemical structures such as terpenoids,
acetogenins, amino-acid derivates and
polyphenols (Fig. 6??). Many of these
compounds probably have multiple
simultaneous functions for the seaweeds and
can act as allelopathic, antimicrobial and
antifouling or ultraviolet-screening agents, as
well as herbivore deterrents.
Most marine herbivores are generalist grazers
that consume many different seaweeds,
although some herbivore species can be
specialised on one or a few algal species.
Grazing pressure is highly dependent on the
specific seaweed and herbivore involved in the
interaction, but is generally considered to be
higher in tropical coral reefs than in temperate
habitats. Large mobile grazers, such as fish,
crabs and sea urchins, can have a more drastic
negative effect on seaweed production and
fitness than smaller ones. Due to their ability to
rapidly consume large amounts of algal tissues,
they are thought to select for constitutive
defences (i.e., defences that are produced and
present continuously within the plants). Smaller
grazers use plants both as food and habitat,
and they consume individual algae over a more
extended period of time. It has been
hypothesised that smaller grazers may select
for inducible rather than constitutive defences
(i.e., defences that are produced in response to
specific environmental cue).
The hypothesis that sessile or slow-moving
organisms, without obvious escape mechanisms
and physical protection, are likely to be
chemically defended has recently been explored
with greater frequency in the marine
environment. Of these organisms,
opisthobranch molluscs appear to be
particularly well endowed with secondary
metabolites. In these gastropods, the reduction
of the protection offered by the shell is
compensated by the development of complex
strategies of defence that include use of
chemicals. In sea slugs
(Nudibranchia),
the shell
is lost, and these species tend to show high
specialised behaviour. Opisthobranchs can feed
30
upon sponges, algae, hydroids, bryozoans,
tunicates and soft corals. In some cases they
are not only capable of accumulating dietary
molecules but also transform or even produce
chemical mediators
de novo
(Fig. 6d).
Oxynoe olivacea,
a green sea snail that
lives camouflaged upon algae
(Caulerpa),
is able to transform the
major algal metabolite, caulerpenyne,
to oxytoxins, increasing the toxicity of
the algal metabolite 100 times (Fig. 6e).
Despite its emphasis on the integration of
researchers, MarBEF has also served as a
catalyst in a remarkable range of new
discoveries. New species were found and
characterised from across the range of marine
life from bacteria to crustaceans, polychaetes
FFiigguurree 77::Xxxx.
31
and echinoderms. In addition, the application of
new tools, which we recognise as one of the
fundamental drivers of scientific progress over
the last millennium, has generated insight into
the astonishing functional diversity of microbial
life in the oceans. Molecular tools have allowed
MarBEF scientists to probe the functioning of
marine microbial communities in novel ways –
and their results have reinforced the emerging
view that improved understanding of the
dynamics of marine life at all scales is the key
to developing a predictive model of the Earth
Systems. This understanding will be built by
integrating knowledge of which organisms are
involved (taxonomy), how they are involved in
ecosystem processes (ecology, chemical
ecology and functional genomics) and their
history of involvement (phylogeny and co-
evolutionary history). The discoveries we have
made in MarBEF are vital steps in this process.
Global questions require
comprehensive datasets
Many current topics in marine biodiversity
research are taking place on very large spatial
scales and over long-term periods. These topics
include baseline assessments in the marine
realm, for assessing impacts of climate change
on marine biodiversity, and studying the
mechanisms by which alien species are
introduced. Therefore, MarBEF recognised that
its scientists would require analyses on an all-
encompassing scale and it funded the LargeNET
project.
LargeNET collected and integrated a large
amount of appropriate data, comprising
pelagic, rocky-shore and soft-bottom benthos
data from across Europe. The data were
collected not only from MarBEF partners but
also from external contributors, and this
established a baseline for current biodiversity
analyses and future investigations within a
changing world. This scale of data collection is
essential to provide the necessary
understanding for anticipating the
consequences of environmental variations on
biodiversity, such as the changing distribution
patterns of macroalagal species.
For example, the database has been employed
to assess the current biodiversity status and
future changes in marine communities through
the evaluation of techniques for the
measurement of species richness.
Twelve different species richness estimators
were tested. The Ugland TS method clearly
performed best and was the only estimator
producing a <10% error. Sample heterogeneity
was found to be one of the most important
factors in determining the performance of
different species richness estimators and
particularly while employing the Total Species
method.
References
Alonso-Sáez, L, Gasol, JM (2006). Seasonal variations
in the contributions of different bacterial groups
to the uptake of low-molecular-weight
compounds in Northwestern Mediterranean
coastal waters.
Appl. Environ. Microbiol.
73
3528-3535.
Beaugrand G, Reid PC, Ibanez F, Lindley JA, Edwards M
(2002). Reorganization of North Atlantic marine
copepod biodiversity and climate.
Science
296
1692-1694.
Cuvelier
et al.
(in press). Distribution and spatial
variation of faunal assemblages on a
hydrothermal edifice at Lucky Strike vent field
(Mid-Atlantic Ridge) revealed by high-
resolution video image analysis.
Deep-Sea
Research
.
Gasol
et al.
(submitted).
Appl. Environ. Microbiol.
Pedrós-Alió, C (2006). Marine microbial diversity: Can
it be determined?
Trends in Microbiology
14(6)
257-63.
Climate change
Changes from the Arctic
to the Mediterranean
Climate change is expected to be one of the
major environmental challenges of the 21st
century, and its impacts are starting to be seen
in the marine environment. MarBEF scientists
have measured rising temperatures in European
waters and have observed how the warmer
temperatures are affecting marine biodiversity.
In waters from the Arctic south to the
Mediterranean, the project has recorded shifts
in species distribution to northern and deeper
waters, changes in the seasonal timing
(phenology) of life-history events such as
migration, reproduction, metamorphosis and
settlement, and how interactions among species
(e.g., predation and competition) are changing.
However, climate change will not only affect the
thermal environment of marine ecosystems;
rises in temperature will be accompanied by
changes in other abiotic conditions of seawater,
including acidity (pH), oxygen concentration
and, in some areas, even the salt concentration
itself (salinity). Moreover, the strength and
direction of some ocean currents, on which
nearly all marine species depend at some stage
in their lives, could change due to climate
change. MarBEF has been finding that some of
these climate-related changes are already
happening and has seen how these changes are
affecting, and will continue to affect, marine
biodiversity in this century.
The Arctic
Warming in the European Arctic has caused not
only sea ice to melt and temperature to increase
but also an increasing advance of Atlantic
waters to high latitudes by way of the prevailing
North Atlantic Current. In MarBEF, the ArctEco 1
project showed how Atlantic water stemming
from a biologically diverse marine region
(Norwegian Sea, Norwegian and British shelf) is
introducing additional species to the relatively
species-poor Arctic (Fig. 1). The pelagic
herbivores (e.g., krill) from the relatively warm
Atlantic water are typically smaller than the
cold-water Arctic herbivore species. Naturally,
top predators of the Arctic (seabirds, seals,
whales) feed efficiently on these relatively large
herbivores, often without any intermediate
small predators between the herbivores and the
top predators. The process of warming is
causing a substantial shift in the food web,
from large Arctic herbivores to smaller Atlantic
species, thus reducing the food resources
available to the top predators (Fig. 2). In the
warming Arctic, primary production is utilised
by smaller, faster-growing species.
Additionally, small carnivores are becoming
more diversified and numerous, which is
dissipating the energy flow considerably. In this
way,
Warming effects lead to higher
biodiversity in the Arctic and
simultaneous food shortages for
the top predators.
North Sea and Baltic Sea
Climate models predict a 2-4ºC rise in water
temperature along with a rise in sea levels in
the current century. This will have major
implications for species, ecosystems and food
webs: spatial distributions, life-histories,
phenologies and biotic interactions among
species will be altered.
In MarBEF, the MarFISH project examined
archaeological evidence from the waters around
Denmark (the Kattegat, Skagerrak, the Belt Sea
and Bornholm) during a warm period from
7000-3900BC and showed that there were
several warm-water fish species then present.
These species were: smoothhound
(Mustelus
sp.),
common stingray
(Dasyatis pastinaca),
anchovy
(Engraulis encrasicolus),
European sea
bass
(Dicentrarchus labrax),
black sea bream
(Spondyliosoma cantharus)
and swordfish
(Xiphias gladius).
These species currently have a
32
more southerly distribution and their presence
near Denmark in the past was presumably due
in part to the warmer temperatures at the time.
Some of these same species are now being
captured regularly by fishermen in the area, in
commercially important quantities: catches have
been reaching tens and thousands of tons
annually during the past decade.
Warming temperatures have been
contributing to an overall increase
in fish species diversity in the
North Sea since the mid-1970s.
This is mainly the case for small-sized southern
species while large, northern species have
shifted their distributions to northern and
deeper waters. These changes have been seen
in scientific fisheries surveys which annually
monitor the species composition of the North
Sea fish community.
Historical evidence shows that
climate may cause substantial
changes in fish phenology.
During the times of substantially colder climate
and severe winters in the 17th century, the
herring
Clupea harengus membras
fishery in
the NE Baltic Sea (Gulf of Riga) mostly took
place during the summer months (June-July).
This was probably due to the later migration of
herring to the spawning areas close to the coast
where the fish were caught. In contrast,
nowadays, in much warmer climate conditions,
the coastal trapnet herring fishery takes place
in spawning grounds a few months earlier than
the historical colder times.
Climate change will also have many non-
thermal impacts on fish populations. These will
include, for example, changes in the strength,
direction and location of ocean currents which,
for example, will affect the likelihood that fish 33
Figure 1: Energy flow scheme showing the typical short-and-efficient food chain of the Arctic (top) compared to the situation in the
warmed Sub-Arctic (bottom).
0.01 0.12 1.2 12 120 g C/m2/yr
eggs and larvae can survive and grow.
Moreover, as temperatures rise, the ability of
the ocean to retain oxygen will decrease. In
many coastal areas in Europe (e.g., bays, straits,
estuaries) the combination of rising
temperature and decreasing oxygen,
particularly in areas which already also receive
high levels of nutrients (eutrophication), will
reduce the size of habitats for, especially,
bottom-living fish species such as cod and
flatfishes. These species will become less
abundant and widespread if coastal areas
experience longer and more frequent anoxic
periods.
In some areas, climate change could even
influence the salinity of the seawater. This could
happen because precipitation and the discharge
of freshwater from rivers and lakes in, for
example, northeastern Europe, could change.
For example, in the Baltic Sea, some climate
oceanographic models predict that the salinity –
which is already so low that some fish species
have adapted physiologically to living there, and
it prevents many other marine fish species from
living there – will fall even further because
climate change in this area will increase
precipitation. If climate change leads to a fall in
Baltic Sea salinity, this will reduce the number
of marine fish species, even though one might
otherwise predict that the increasing
temperature should allow warmwater-adapted
species to immigrate. The Baltic Sea example
shows that it will be important to consider
multiple aspects of climate change, especially in
coastal areas, if we are to estimate how marine
biodiversity will change in future.
Another impact of climate change will be the
rise in sea level due to melting of land-based
glaciers and the expansion of seawater as it
warms up – as warm water occupies more space
than cold water. Both factors will cause flooding
of existing coastal lowlands. The newly flooded
34
Figure 2: Scheme of the use of resources and energy loss as a consequence of increasing biodiversity.
Number of species on the same trophic level, increasing resources use
0.0001
0.001
0.01
0.1
0
10
Number of trophic levels, increasing energy loss
coastal areas will provide more fish habitat,
especially for benthic juveniles stages which are
common in coastal areas.
North Atlantic benthos
In the North Atlantic, temporal changes in
deep-sea communities at the Porcupine Abyssal
Plain (PAP), at 4,850m water depth, have been
studied since 1989, most recently within the
DEEPSETS project.
Shifts in different elements of the
benthic biota of the deep-sea
communities at the Porcupine Abyssal
Plain over decadal as well as shorter
(seasonal) time-scales have been
recorded and attributed to the North
Atlantic Oscillation (a climatic
phenomenon).
While intra-annual changes reflect seasonal
productivity cycles, the decadal-scale changes
at the PAP are believed to be linked to the North
Atlantic Oscillation, a climatic phenomenon that
affects winds, precipitation and storm intensity
and frequency. These oscillations lead to
changes in upper ocean biology and the export
of particulate organic carbon (POC) from the
euphotic zone (i.e., the export flux) and to the
sea floor, as well as in the quality (biochemistry)
of the material that reaches the sea floor. These
changes in food quantity and quality (for
example, the content of pigments necessary for
reproduction) probably underlie the ‘boom-
bust’ cycles observed in the holothurians
Amperima rosea
and
Ellipinion molle.
Vastly
increased populations of these small surface-
feeding organisms may, in turn, have affected
foraminiferal and meiofaunal populations
through depletion of food resources and
sediment disturbance. A similar relationship
between climate, sea-surface processes and
deep-sea benthos appears to exist in the NE
Pacific Ocean.
The most obvious changes at the PAP were seen
among the megafauna (animals visible in sea-
bottom photographs and trawls), notably the
holothurians
Amperima rosea
and
Ellipinion
molle.
These relatively small species both
exhibited ‘boom-bust’ cycles - rapid
abundance increases followed by declines –
during the period from 1996 to 2005. The rise
to dominance of
A. rosea
during 1996 has been
termed the ‘Amperima event.’ Two larger
holothurian species,
Psychropotes longicauda
and
Pseudostichopus aemulatus,
exhibited
more modest increases while a third,
Oneirophanta mutabilis,
underwent a significant
decrease over the entire time-series. Increases
in holothurian densities led to a dramatic
increase in the extent to which surface
sediments, and particularly deposits of
phytodetritus (organic detritus derived from
surface primary production), were reworked.
Probably as a result of these activities, there
was little sign of phytodetritus on the seafloor
between 1997 and 1999.
Among smaller organisms, densities of
foraminifera were significantly higher in 1996-
2002 (post-Amperima event) compared to
1989-1994 (pre-Amperima event). The
species-level composition of the assemblages
changed over this period, reflecting fluctuations
in the densities of higher taxa and species. In
1996, following a phytodetritus pulse, the
miliolid
Quinquiloculina sp.
migrated to the
sediment surface, grew and reproduced before
migrating back into deeper layers as the
phytodetrital food became exhausted. A
substantial increase in the abundance of
trochamminaceans, notably one small,
undescribed species, may have reflected
qualitative change in the phytodetrital food,
repackaging of food by megafauna, increased
megafaunal disturbance of the surficial
sediment, or a combination of these factors.
Thus, the PAP time-series suggests that
decadal-scale changes have occurred among
shallow-infaunal foraminifera at this site, more 35
or less coincident with changes in the
megafauna, as well as indications of shorter-
term events related to seasonally-pulsed
phytodetrital inputs.
Densities of metazoan meiofauna increased
significantly between 1989 and 1999, driven
mainly by the dominant taxon, the nematodes,
and to a lesser extent the polychaetes.
Ostracods showed a significant decrease while
most other taxa, including the second-ranked
group, the copepods (harpacticoids and
nauplii), did not exhibit significant temporal
changes in abundance. MDS ordination of
higher taxon composition showed a significant
shift from the earlier (pre-Amperima, 1989-
1994) to the later (1996-1999, post-Amperima)
periods. There were also significant increases
over time in the proportion of total meiofauna,
nematodes and copepods (but not polychaetes)
inhabiting the 0-1cm layer. In addition,
seasonal changes in the vertical distribution
patterns of total meiofauna and nematodes
within the sediment were apparent during the
intensively sampled period, 1996-97.
36
Figure 3: Multiple correspondence analysis results of Ceratium spp. in phytoplankton samples from Monaco, Genoa (a century ago)
and Naples (at present).
AFCM stations (horizontal surface sampling)
Axis 2 – coordinates
3
2
1
0
-1
-2
-3
-2
-1.5 -1 -0.5 0 0.5 1 1.5 2 2.5
-1 0123
Monaco (1908-1914)
Genoa (1915)
Naples (1984, 1988, 2002, 2005)
Old data (Monaco) Recent data (Naples)
C. trichoceros
C. teres
C. arietinum
C. horridum
C. fusus
C. falcatum
C. macroceros
C. pentagonum
C. extensum
C. declinatum
C. symmetricum
C. furca
C. tripos
C. massiliense
C. concilians
C. limulus
C. candelabrum
C. carriense
C. hexacanthum
C. gibberum
Coordinates of species presence on AFCM axis 2 (surface sampling)
Macrofaunal polychaetes exhibited a more
muted response to changes at the Porcupine
Abyssal Plain. Although the abundance of the
whole assemblage increased significantly before
and during the Amperima event, the increase
was not on the same scale as that observed in
the megafauna, and only certain taxa and trophic
groups responded. The same dominant species
occurred throughout the study period, with the
exception of the
Paraonidae,
where the dominant
species declined prior to the Amperima event
and was replaced by two other species. Only six
of the 12 most abundant species showed a
significant response (abundance increase) during
the Amperima event. The fact that only some
polychaete species responded may be related to
efficient foraging by megafaunal deposit feeders
that sequestered and repackaged organic matter,
leaving less available for smaller organisms. Yet
there did not appear to be an impact from
physical disturbance caused by megafaunal
feeding activities. For example, surface deposit
feeders increased during the Amperima event at
the same time as disturbance of the surficial
sediment by holothurians and ophiuroids was
also increasing. The polychaetes indicate that
changes in the upper ocean which affect the
ocean floor may operate in a complex way and
that high taxonomic resolution is needed to
establish how the fauna responds.
Temporal changes in the deep sea are
not confined to the deep Abyssal Plains;
changes have also been recorded in the
Arctic and the Mediterranean.
In the Arctic, work by the Alfred-Wegener
Institute in Bremerhaven demonstrated a small
but important temperature increase between
2000 and 2008 at 2,500m depth in the Fram
Strait between Svalbard and Greenland. Within
DEEPSETS, a five-year (2000-2004) time-series
study of nematodes at this site revealed shifts
in nematode abundance and community
composition, reflecting changes in food
availability. 37
Although depth-related changes were more
prominent than shifts relating to sampling year,
interannual variability in nematode community
structure was clearly apparent, particularly at
the 4,000m station. Parallel observations at
several water depths indicated that most of the
variation over the time-series was the result of
real temporal changes, driven by shifts in food
availability as measured by sediment-bound
phaeopigment and chlorophyll
a
concentrations. For the larger organisms, a
towed camera system revealed a significant
decrease in megafauna densities at 2,500m
water depth.
The Mediterranean
Global change and
microplankton
Plankton is a collective term for all organisms
living in the water column that lack their own
means of active movement or whose range of
movements are more or less negligible in
comparison to the movement of the water mass
as a whole. Plankton organisms can range in
size from a few metres for large jellyfish and
salp colonies to less than a micrometre for
bacteria. Within the MarPLAN
project the biodiversity of
eukaryotic marine single-celled
plankton organisms was
studied in order to answer
the question “In what ways
can global change affect
microplankton?”
To understand plankton
distribution and changes
therein, we first need
to know how diverse
it is. Cryptic diversity
can be found in easily
identifiable
morphologically
defined species,
Ceratium sp.
and while the morpho-species may be
considered cosmopolitan, the cryptic diversity
therein shows more restricted patterns.
Investigations by MarPLAN uncovered
many cases of remarkable species
diversity within what was originally
perceived as single, widely-distributed
species.
For example, MarPLAN discovered that the
cosmopolitan species
Fibrocapsa japonica
in
fact consists of two cryptic species. The second
one was discovered in the Adriatic Sea.
Another research project has focused on the
diatom genus
Skeletonema.
In this genus,
several new species were discovered and a
biogeographic study showed that some of the
newly discovered species had a restricted
38
distribution pattern. For instance,
Skeletonema
gretae
is found only along the Atlantic coasts of
the US but nowhere else, despite massive
efforts to detect it in similar environments
along the coasts of Europe, China, Japan, South
America and Australia.
In the temperate zones, many phytoplankton
species form blooms during restricted periods
of the year. Under influence of global warming,
some species show a propensity to bloom
earlier in some places. In addition, the
distribution of these blooms tends to shift
polewards. New species may appear in regions,
partly through introduction (for example, via
ballast water dumping) and partly through
polewards range expansion of warm-water
species. Several MarPLAN research partners
collaborated on assessing these trends in the
dinoflagellate genus
Ceratium.
Figure 4: Schematic diagram illustrating forcing factors that influence temporal processes in ’normal’ sedimented parts of the
deep-sea and in chemosynthetic systems. In the first case, temporal changes are forced ultimately by climatic oscillations. In the
second case, they are forced by geological processes that affect fluid flow.
Over the last century, several species of
the genus
Ceratium
have disappeared
from study sites in Villefranche sur Mer
and Naples, or have become far less
common, while new dinoflagellate
species have recently appeared.
The appearance of zooplankton (copepods,
planktonic larvae of meiobethos) may be
triggered by different factors; increased
temperatures may affect the timing of
appearance of certain species differently. If
grazers such as planktonic larvae find
themselves out of phase with their food source
they will be short of food and not make it into
adulthood. Subsequently, populations of
benthic species which rely on them for nutrients
may also dwindle. These temporal changes,
documented by DEEPSETS, have occurred within
our lifetime.
Many phytoplankton species produce toxins or
otherwise constitute a nuisance to other
species, including humans. Such species (for
example,
Fibrocapsa japonica)
are considered
harmful and, when appearing in large numbers,
form harmful algal blooms (HABs)
.
In the
current scenario of global change, coastal
regions may suddenly find themselves
confronted with increasing numbers of HABs.
Another driver of global change is the increased
concentration of CO2in the atmosphere, which
results in a higher CO2concentration in the
upper layers of the ocean. This might seem a
good thing for phytoplankton. However, there is
a less favourable side-effect: with increasing
CO2in the seawater, the acidity increases (the
pH drops).
As the acidity of seawater increases,
several phytoplankton species that
utilise calcium carbonate as
construction material for their cell walls
will have difficulty sequestering it from
seawater and will thus retain it. 39
The coccolithophorid
Emiliania huxleyi
is one
such species: it forms discs of calcium
carbonate called coccoliths, which appear to
provide protection to the cell.
DEEPSETS research has shown that the eastern
Mediterranean is periodically subject to
stochastic flux events that deliver large
amounts of food to the sea floor, abruptly
turning the ‘desert’ into an ‘oasis.’ This event-
driven character of the eastern Mediterranean
was illustrated by the very high phytopigment
concentrations in the Ierapetra Basin during
1993. These were linked to significant changes
in the hydrography of the Cretan Sea after
1992, involving an increasing outflow of
nutrient-rich water masses into the Levantine
Basin, resulting in enhanced biological
productivity and OM flux to the seabed. In
1993, this enhanced flux caused significant
changes in the abundance and composition of
the meiobenthic assemblages as well as of the
planktonic and macrobenthic communities.
Species detection tools
Reliable tools have been developed for
detecting declining species, cryptic populations
and non-indigenous species. Despite the
growing evidence of range shifts of marine fish
species, local extirpations and even extinctions
are predicted, but not yet observed, as a
consequence of climate change. Small pelagic
fish species, in particular, are characterised by
Emiliania huxleyi.
© SZN
large effective population sizes and a high
potential for gene flow, and they may respond
rapidly to changes in physical oceanographic
conditions and have shown large population
fluctuations and extirpations over glacial
time-scales.
MarBEF presented a range-wide phylo-
geographic survey of European sprat
(Sprattus
sprattus),
based on a 530-base-pair sequence
from the mitochondrial control region, that
demonstrates the existence of genetically
isolated populations in northern Mediterranean
basins. We concluded that these populations -
characterised by significantly reduced genetic
diversity - remain isolated because of their
inability to maintain gene flow under the
present physical oceanographic regime. The
results demonstrate the effect of glacially-
induced changes in physical oceanographic
conditions on a cold-adapted small pelagic fish
species trapped in a geographically confined
area at its southernmost distribution limit.
MarBEF, for the first time, identified
distinct and potentially vulnerable
populations on the climate-change-
induced edge of survival.
The genetic analysis of marine organisms has
revealed various examples of cryptic species -
populations that we previously thought
belonged to the same species because they
shared the same morphological diagnostic
characters. Genetic comparisons of distant
populations demonstrated genetic differences
at the same level as we typically find between
well separated species. Such studies have
generated important new insights into the
process of speciation in the marine
environment, as, for example, in the case of the
Heart Urchin,
Echinocardium cordatum,
which
splits into five distinct branches (clades). Such
clear-cut genetic distinctions between
populations provide strong evidence of
reproductive isolation, from which we can infer
40
that speciation has occurred. So now we have a
complex of species masquerading under a
single name!
This phenomenon suggests that genetic and
morphological change may take place at
different rates in evolution, and such cryptic
species are a product of slow molecular
evolution combined with morphological stasis.
They provide good models to help us
understand the speciation processes which lie
at the heart of modern evolutionary theory.
Edges, centres and hotspots
The large, brown fucoid seaweeds are dominant
intertidal, foundational species occurring along
rocky shores throughout Europe (Fig. 10),
whereas in subtidal, soft-sediment habitats,
this dominant role is played by seagrasses.
Members of the genus
Fucus
and the seagrass,
Zostera marina
were extensively sampled
throughout their entire North Atlantic ranges.
For most seaweeds and corresponding
invertebrates, refugia during the last glacial
maximum (ca. 18,000 years Before Present)
existed in parts of SW Ireland, Brittany and NW
Iberia (Fig. 9).
Today, the Brittany peninsula is a
hotspot of accumulated diversity for
many taxa, whereas NW Iberia is
quickly becoming a ‘trailing edge’ as
increased sea surface temperatures
push the boundaries northward.
This type of retrospective-prospective analysis
aids in understanding changes in biodiversity
that will be unavoidable as the natural world
responds to climate change. As well as
providing detailed information about large-
scale connectivity along coasts, such
information can help in establishing guidelines
for the design of marine protected areas and, in
the near future, addressing the genetic
potential for adaptation under climate change.
Impacts and disturbance
Human activities
In an era of advancing globalisation,
environmental degradation is a major inter-
national concern. Human impacts propagate
across terrestrial and aquatic environments and
throughout the atmosphere because of the
inherent connection between these components
of the biosphere. A direct consequence of this
connectivity is that human impacts can
accumulate their effects in space and time,
challenging the ability of living organisms to
absorb environmental shocks. This is
particularly true for marine environments, which
are the final recipient of many terrestrial wastes
and are simultaneously exposed to human
impacts occurring directly in the sea.
Marine ecologists and biologists are engaged in
a collaborative effort to understand how
escalating trends in human impacts are
affecting marine biodiversity and, in turn, how
changes in biodiversity affect the functioning of
marine systems and their ability to produce the
key resources that are necessary for our own
well-being. This is not a simple task. Different
kinds of environmental degradation affect
different species in different ways, and impacts
can vary depending on characteristics of the
habitat in which the species occur and the
locality. Combined effects of numerous sources
of impact can propagate throughout
ecosystems in extremely complex ways, making
it difficult to predict how a given ecosystem will
respond to future disturbances and
environmental changes.
MARBEF researchers have used a number of
different approaches to address some of these
challenges, bringing together individuals with a
range of different skills and areas of expertise.
We have worked with information accumulated
over decades of past research as well as
collecting new information by undertaking
experiments and sampling programmes in a
range of marine ecosystems. Below, we
summarise some of the key findings and
emphasise their implications for management
and future research.
Effects of fishing
The consequences for
ecosystem structure and
functioning
Fishing affects fish populations in many ways –
reducing numbers, changing the age and size
composition of populations, and changing life
history patterns (including evolutionary changes
in maturation). Many fish populations have been
reduced to low numbers due to long-term
impacts of fishing (e.g., cod in Baltic Sea) and
some populations may be approaching collapse
(e.g., bluefin tuna in NE Atlantic and
Mediterranean).
Historical studies have shown that cod
in the eastern Baltic Sea were more
abundant 400 years ago than in
the late 20th century.
This result, highlighted by MarFISH, is
surprising, because the Baltic Sea 400 years ago
was not very “cod-friendly” and was much less
productive than today (i.e., before the increase
in nutrients and primary production in the mid-
to-late 20th century) and marine mammal
predators of cod (seals) were more abundant.
Cod were probably more abundant despite the
lower productivity because of the overall lower
level of exploitation in the 1500s.
Bluefin tuna were abundant in northern
European waters such as the North and
Norwegian Seas until the late 1960s and into
the 1970s, when they disappeared; they have
not yet returned. The reasons for their
disappearance are not clear. However, since the
1970s, the overall biomass in the entire NE
Atlantic and Mediterranean has declined and
landings have been too high for too many years 41
to allow recovery of the population. Legitimate
fishing quotas are exceeded by illegal landings
and catches of undersized fish. As a result, the
population is at risk of collapse and has been
disappearing from other areas of its range
including the Black Sea and parts of the
Mediterranean.
Heavy exploitation of fish populations
can also have consequences for the
other species in the ecosystem.
These consequences include effects on
abundances of prey species, and how predators
and prey interact (e.g., the structure and
functioning of ecosystems). The effects can
include “cascading” effects in which abundances
of prey species increase in response to
decreases in abundances of predators; the
increase in the prey species then has a
controlling effect on prey in the next lowest
trophic level in the food web, and so on.
An early example of this ecological cascade
occurred in the Limfjord, Denmark, in the early
1800s, when heavy fishing pressure contributed
to the collapse of a local herring population and
the subsequent dominance by jellyfish,
including
Aurelia aurata.
The ecosystem became
so dominated by jellyfish that fishermen were
complaining that they could not haul their nets,
and the issue was discussed in the Danish
parliament. This example seems to have been
repeated in other areas around the world where
fishing has removed large quantities of
zooplanktivorous fish, such as herring, sardines
or anchovy, and jellyfish subsequently became
abundant.
Evolutionary effects
of fishing on fish biodiversity
Fishing is by nature a selective process: some
individuals are more likely to avoid capture,
survive and reproduce than others due to
individual differences in size, morphology or
behaviour. Fishing may therefore act selectively
on reproductive age- and size-groups. If these
differences are heritable, then fishing will have
evolutionary effects on the population over
time. In addition,
Different populations of the same
species may differ in their sensitivity
to exploitation;
this could lead to a decline of less
resilient populations while other
populations of the same species are
less affected.
Fishing can, therefore, have evolutionary effects
on fish populations, and this topic has been
receiving increasing attention in the last 10-15
years. One of the most interesting and striking
results is that:
Fishing, by increasing the mortality
of reproductive age- and size-groups
of fish, favours evolution towards
earlier maturation.
This pattern has been predicted from
theoretical models employed by MarFISH, and
has been observed in nature in several wild fish
populations. These observations strongly
support the hypothesis that fisheries-induced
evolution towards earlier maturation at smaller
size is commonplace. Remarkably, we see that
the pace of fisheries-induced evolution can be
very high, leading to detectable changes, even
over just a few generations. Present fishing
practices typically favour fish on the “fast track”
of maturation and development, as opposed to
unexploited situations where there is also room
for fish in the “slow lane.” These findings of
evolutionary effects of fishing are controversial
and still being debated in the scientific
literature. Whatever is the nature of the change
– genetic change, plasticity, or community
change – phenotypic diversity of fish life-
histories is on the decline. As a consequence,
42
43
Fish populations may be becoming
more vulnerable (and less resilient) to
perturbations such as fishing, climate
change and invasive alien species.
Effects of an increase in
freshwater to coastal
regions
Climate models predict increasing variance in
rainfall regimes, with increased frequency of
droughts parallelled by unusual amounts of
rainfall and floods. In anticipation of this, the
Mediterranean region is now being subjected to
extensive river damming, which can have far-
reaching impacts on coastal food webs. For
instance, the diets of the five most abundant
flatfish species of the Gulf of Lions and their
prey depend on river inputs. Two trophic
networks occur off the River Rhône, one based
on the consumption of carbon of marine origin,
the other on carbon of terrestrial origin. The
transfers of the latter are most significant
between 30 and 50m depth, where river
particulate organic matter sedimentation and its
uptake by the benthos are highest. The
common sole largely profits from the
contributions from terrestrial organic matter,
via their main prey: deposit-feeding polychaete
worms. The increase in abundance of these
polychaetes stabilizes the whole life-cycle of
the species and consequently the associated
fisheries. That means that climate changes
inland may affect coastal marine food webs,
particularly through variation in river flow.
Increased river inputs to coastal
systems may alter food webs
and fisheries
Combined impacts: loss
of species and disturbance
Coastal ecosystems are extremely productive
and provide a range of economic and social
benefits, such as fisheries and coastal
protection. They are subjected to a wide range
of disturbances and, under forecasted climate
change scenarios, including increased
storminess, many will experience increased
physical stress and organic enrichment. At the
same time, a range of local activities are
causing the loss of some of the key species in
the ecosystems such as large seaweeds,
seagrasses and burrowing worms. It is not yet
known how these different impacts might
Oceans and seas make up the most widespread habitat type on the planet. Industrial fisheries, habitat destruction and pollution
are increasingly diminishing fish resources at a global level.
© Ferdinando Boero, Alberto Gennari, Fabio Tresca
44
combine to affect ecosystem processes. This
information is essential for the implementation
of environmental legislation such as the new EU
Marine Framework Strategy Directive. Such
legislation also requires that specific
management strategies are developed for
different regions in Europe.
MARBEF workers on the BIOFUSE project used
simple experiments to compare effects of loss
of biodiversity (specifically, a key species) on a
number of marine ecosystems (rocky shores,
seagrass beds and sedimentary shores) also
subjected to experimental disturbance (physical
impacts or organic enrichment) at a number of
locations in Europe to answer the question ‘Are
the effects of biodiversity loss consistent across
different habitats and locations?’
The loss of key species affected structure and
functioning in many, but not all, ecosystems.
The influence of loss of species and disturbance
on structure varied among habitats and
locations. In only a few cases were there
complex combined effects of these two
impacts. An influence on functioning was rare,
suggesting widespread capacity of ecosystems
to compensate for loss of single species, even
‘key’ species. This is good news with respect to
these habitats, but the results showed variation
between locations, something which is reflected
in the EU Marine Strategy Framework Directive
where there is emphasis on regional focus.
There is considerable variation in
impacts as a result of biodiversity loss
among locations within regions,
which requires different
management strategies.
Additional field-based experimental research is
needed to predict combined effects of loss of
‘key’ species and disturbance. This research
need not be complex, but it does need to be
extensive and carefully designed. This
information is of direct use to managers to
avoid being misled by assuming that impacts of
disturbance and species loss are consistent
across systems.
Do changes in species
abundance have impact?
Many species are being reduced in abundance
or driven to local extinction by human activities.
Although there are clearly consequences of
Seagrass meadows are a priority habitat under the EC Habitats Directive.
© Ferdinando Boero, Alberto Gennari, Fabio Tresca
45
changing biodiversity for the functioning of
ecosystems, the relative importance of different
kinds of changes are not clear. MarBEF
scientists on the BIOFUSE project used intertidal
communities of algae and invertebrates as an
experimental system to assess the separate and
combined effects of changes in the number and
type of key species on the functioning of the
selected ecosystem. The results showed that
changes in the abundance of species were more
important than changes in the variety of
species.
The key result was that while effects of changes
in diversity vary according to the habitat and
location, the effects of changes in species
abundance are much more consistent. Current
environmental policies focus on conservation of
species diversity and habitats, placing less
emphasis on preservation of species
abundances. MarBEF data shows that:
Alteration of key species abundances
affects ecosystem functioning more
than changes in species diversity.
This outcome emphasises the importance of
preserving not only particular species but also
the relative abundances with which species
populate our marine coastal environments.
Potential impacts of
biodiversity change on
ecosystem stability
Biodiversity loss is being observed in many
ecosystems and raises concerns about the
potential effect of this loss on the functioning
of ecosystems and their provision of services to
society. A key consideration is the extent to
which biodiversity can improve the stability of
ecosystems through time, both in terms of their
structure and functioning. More stable
ecosystems are more reliable providers of
ecosystem services such as fish catches and
stabilisation of coastal habitats.
In this study, the relationship between
biodiversity and stability (as temporal
variability) of marine benthos was investigated
using two approaches: (a) meta-analysis to
assess whether consistent patterns could be
found in existing datasets, and (b) new
sampling at fifty rocky shores throughout
Europe.
The overall outcome of the meta-analysis
indicated a negative (although weak)
relationship between diversity and stability in
some aspects of ecosystem structure for each
of three habitats (rock pools, emergent rock
and sedimentary shores). These relationships
were observed at small and large scales, but
there was variation in the outcome depending
on which habitats and locations were being
considered.
In many cases, there was no clear
relationship between diversity and
stability; research revealed that the
relationship varied among regions,
depending on habitat, scale
and location.
In the sampling programme employed by
BIOFUSE scientists, which was focused on
emergent rock on rocky shores, there were
generally no relationships observed. However,
at small scales (areas of less than a metre), we
observed a positive relationship between
diversity and stability of the suite of species
present. The relationships varied among
regions, which again helps to support the
regional focus of the new EU Marine Strategy
Framework Directive. Outcomes from both
approaches led to similar results for rocky
shores. Therefore, where sufficient datasets
exist, meta-analysis of those datasets can
provide a cost-effective alternative to collecting
new data on diversity:stability relationships.
However, more empirical research is required to
characterise the link between diversity and
stability in many habitats.
Human disturbance and the
stability of rocky shore
assemblages
The structure and functioning of marine
ecosystems is threatened by a range of human
activities, including degradation and destruction
of habitat, organic and inorganic pollution,
enhanced inputs of terrestrial sediments, over-
fishing and invasion by alien species. It is not
clear, however, how different activities vary in
the way in which they influence stability of
ecosystem structure. In this study, the BIOFUSE
project combined and reanalysed the results of
a large number of experimental studies on
impacts of disturbances on stability of
assemblages of animals and seaweeds on rocky
shores.
Only some types of human disturbance
have strong effects on the stability
of rocky shore assemblages.
Overall, the results of this study indicated that
some types of disturbance, such as loss of large
46
seaweeds and nutrient enrichment, did not
influence stability. Other sources of
disturbance, including removal of organisms
caused by mechanical forces or the dominance
by exotic species, can reduce, although through
different mechanisms, the stability of intertidal
assemblages. It is interesting to note that an
increase in the severity of mechanical
disturbance is predicted in intertidal habitats as
a consequence of increased frequency of
extreme meteorological events (i.e. sea-storms
and hurricanes). Similarly, the introduction of
exotic species is increasing rapidly with the
intensification of global trading.
Some evidence suggests that
management initiatives should focus
their attention on responses to climate
change and on reducing the impact of
invasive species on rocky shore
assemblages.
Impacts of disturbance
on nematodes
Sediment movement, erosion and deposition
are natural processes, and benthic organisms
have adapted to such disturbances. Man-made
physical disturbances (e.g., beam trawling,
Rocky shores are dynamic and fascinating habitats which are influenced by the tides. They are biologically rich in terms of the
number and variety of species they support.
© Ferdinando Boero, Alberto Gennari, Fabio Tresca
47
dredged material disposal, coastal
development) occur at a much larger scale, rate
and magnitude which may exceed the adaptive
capacity of sediment-inhabiting organisms.
MarBEF researchers on the MANUELA project
compiled and analysed an extensive database of
experimental and observational studies
investigating the effects of physical
disturbances in sediments. Some measures of
diversity decreased with increasing level of
disturbance regardless of the disturbance type.
Others, however, were more variable and
depended on the nature and origin of the
disturbance. Hence, there is no consistent effect
of physical disturbances on nematode
assemblages. In addition, it was shown that
man-induced changes are intrinsically different
from those of natural origin. Nematode
assemblages were more similar after being
subjected to high-intensity disturbances, even
if they originated from geographically distinct
areas.
Nematode assemblages do not show
a similar response to different types
of physical disturbance.
However, it is largely unknown whether
nematodes respond in a similar way to the
same disturbance, independently from the
geographical location. In this experiment,
MANUELA researchers mimicked the effect of an
increased amount and frequency of rainfall on
sandy beaches from four different locations in
Europe. Experimental beaches were located in
Poland (Baltic Sea), Belgium (North Sea),
Portugal (NE Atlantic Ocean) and Crete
(Mediterranean Sea). Beaches covered a range of
tidal regimes (microtidal to macrotidal), salinity
brackish to marine) and temperature (north-
south gradient) environments. The frequent
addition of fresh water to the Baltic beach did
not affect salinity in the sand, due to the low
natural salinity. All other beaches showed
modified salinity profiles. All nematode
assemblages changed significantly as a
consequence of the experimental treatment, but
the underlying mechanisms were different.
Nematodes do not show a universal
response to disturbances associated
with climate change.
This shows that there is no universal response
of nematode assemblages to disturbances and
that changes occurring at a global scale will
have different impacts in different localities.
The adaptation of the receiving community to
the frequently-changing environment largely
determines the effect of the increase in rainfall.
Conclusion
MARBEF has examined impacts of disturbance
at a truly European scale - collating, generating
and comparing evidence from a wide range of
disturbance types, habitats, taxa, places and
times. Its researchers have worked to improve
methodologies for data collection, archiving
and analysis and have completed a substantial
body of original research. New evidence has
shown that the impacts of key disturbances can
vary substantially depending on the
environmental context in which they act and are
not necessarily predictable based on existing
knowledge. The specific and general findings of
the work can be applied directly to the
implementation of the existing Water
Framework Directive and the new Marine
Strategy Framework Directive. Effective
decision-support tools must incorporate
empirically derived insight into the impacts of
key disturbances in specific regions and
localities. The databases generated during
MARBEF will provide a lasting legacy and can be
built upon and interrogated repeatedly in future
with great potential to improve our
understanding of variation in impacts of
disturbance on marine ecosystems and our
approaches to managing marine environments.
Valuation and marine planning
Integrating natural and
social science
Initially, MarBEF spent time on integrating
activities to discover common ground and
common language between the disciplines;
developing methodologies for valuation that
could be applied in the marine environment and
to marine biodiversity issues, and developing
the research potential of this heterogeneous
group of people. MarBEF recognised that there
was barely any existing data on the socio-
economic importance of marine biodiversity
and, previous to MarBEF, almost no
development of methodology to collect such
data.
MarBEF developed an ambitious research
project (MarDSS) to begin to fill some of the
gaps in available data and to test the
methodologies it had developed. Such data
collection required substantial effort, beyond
what was available within MarBEF. MarBEF,
therefore, decided to make a substantial
contribution to this area by capacity-building
and training PhD and MSc students to provide
them with appropriate interdisciplinary skills.
Goods and services
Marine biodiversity provides goods and services
that yield direct and indirect benefits to people.
Understanding these goods and services can
indicate the socio-economic importance of
marine biodiversity. Within the framework of
the Millennium Ecosystem Assessment, MarBEF
economists and cultural anthropologists, in
collaboration with marine ecologists, have come
together and identified and defined specific
ecosystem goods and services provided by
marine biodiversity.
MarBEF scientists have identified and
defined specific ecosystem goods and
services provided by marine
biodiversity.
Case-studies were used to provide examples of
marine ecosystem goods and services and
hence an insight into the practical issues
associated with their assessment. This validated
the definitions of marine goods and services,
providing a theoretical framework for their
assessment, and identified knowledge gaps and
likely difficulties of quantifying the goods and
services. The research will enable future
assessments of marine ecosystem goods and
services.
A ‘goods and services’ approach has
the capacity to play a fundamental
role in the ecosystem approach
to environmental management
Utilisation of this goods and services approach
has the capacity to play a fundamental role in
the ecosystem approach, by enabling the
pressures and demands of society, the economy
and the environment to be integrated into</