Marine and terrestrial ecology: unifying concepts

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Marine and terrestrial ecology: unifying concepts
Opinion
Marine and terrestrial ecology: unifying
concepts, revealing differences
Thomas J. Webb
Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
The extent to which similar ecological processes operate
on land and in the sea has been much debated, with
apparently ‘fundamental’ differences often disappearing
when appropriate comparisons are made. However, marine and terrestrial ecology have developed as largely
separate intellectual endeavours, which has hampered
the search for general patterns and mechanisms. Here, I
argue that marine–terrestrial comparative studies can be
extremely useful at uncovering mechanisms when they
explicitly consider those facets of the environment that
are important to a particular hypothesis. Furthermore,
the binary ‘marine–terrestrial’ division misses many
opportunities for more interesting comparisons, several
of which I highlight here. Increasing the flow of concepts,
hypotheses, and data between marine and terrestrial
ecologists is essential to reveal those differences that
really are important.
A tale of two ecologies
Surveying the quest for generality in ecology, Lawton [1]
noted that ‘environments are different, organisms are
wonderfully different, and the laws, rules and mechanisms
we end up with... are contingent’ on the particular system
one happens to study. This suggests that untangling the
dynamics of any specific community will require a good
deal of specialist ecological knowledge. However, the risk is
that this knowledge is gained at the expense of a more
general view of pattern and process: ecologists specialising
in a particular type of system tend to favour particular
methods and hypotheses [2], if only through ignorance of
those developed in other systems [3]. Thus, although important ecological insights tend eventually to be applied
across systems, the search for general patterns in Lawton’s
contingencies will typically be restricted to a subset of
available case studies, and bounded by system-specific
understanding. Forest ecologists will draw on a different
empirical and theoretical corpus than will students of
grasslands, mangroves, or the deep sea.
A formative decision faced by any ecologist in this
respect concerns whether to specialise in marine ecology.
Marine ecologists remain, as a rule, largely separate from
the ecological mainstream (see Box 1 for a discussion of
terminology), working in separate departments or institutes, publishing in (and reading) different journals, and
participating in different workshops and meetings [3,4].
The clearest consequences of this separation may be in the
policy arena, where marine systems have a much lower
Corresponding author: Webb, T.J. ([email protected]).
profile than do terrestrial systems in discussions of biodiversity and biological responses to climate change [5]. But
equally important, these barriers can also reduce the
transfer of theory, hypotheses, and methods [3], effectively
limiting ‘meme flow’ [6] and leading to unwitting reinvention, duplication of effort, repetition of mistakes, and an
overall loss of conceptual coherence (Box 2).
Two decades ago, Steele [7] recognised these problems
and championed the idea that communication between
marine and terrestrial ecologists could both provide critical
tests of theory and lead to more general conclusions. My
aim here is to highlight various (still regrettably rare)
attempts to meet Steele’s challenge in the fields of community ecology and macroecology, and to suggest areas with
high potential for future cross-domain collaborations. My
goal is to show that the exchange of concepts, models, and
empirical approaches between marine and terrestrial ecologists is usually worth the effort, and is often both enlightening and productive [6,8].
Differences between marine and terrestrial ecosystems:
fundamental or incidental?
Before examining where cross-domain collaboration can be
most fruitful, it is worth considering why it has not been
more common. The physical differences between air and
water (summarised in [9,10]), and their consequences for
organisms living in these different environments, have led
to claims of ‘fundamental’ differences between marine and
terrestrial ecology. Certainly, the raw materials upon
which biotic and abiotic forces can act are rather different
in the two domains. The seas are immensely diverse in
terms of higher taxa (most animal phyla have marine
members, many exclusively so [11]), yet species-level diversity has been higher on land for some 100 million years
(my) [10] and, today, marine species constitute only approximately 15% of all described species and 25% of predicted global species numbers [12]. However, it is not clear
whether these stark differences in diversity reflect fundamentally different ecological processes, or whether they
are instead an incidental consequence of rather few chance
evolutionary events.
In an insightful review [9], Dawson and Hamner argue
that to address such questions, one has to acknowledge
that reality is far more nuanced than a binary ‘marine–
terrestrial’ division allows. Each domain includes its own
contrasts, and there is little justification for elevating
marine–terrestrial contrasts over and above those between, for example, marine pelagic and marine benthic
habitats or between the forest canopy and the rhizosphere.
0169-5347/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2012.06.002 Trends in Ecology and Evolution, October 2012, Vol. 27, No. 10
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Trends in Ecology and Evolution October 2012, Vol. 27, No. 10
In this article, I contrast ‘marine’ and ‘terrestrial’ ecological research.
This leaves the position of ‘freshwater’ ecology somewhat ambiguous. Some authors contrast ‘terrestrial’ and ‘aquatic’ systems
regardless of salinity [2,24]; others focus only on the two major
domains (marine and terrestrial) for simplicity [7,9], or explicitly
include freshwater systems as a separate domain [3]; and some
divide instead ‘marine’ and ‘mainstream’ ecology [4], with the latter
taken to include the kinds of ecologist who typically dominate
general ecology conferences, societies, and journals. I have tended
towards this latter sense, and my use of ‘terrestrial’ typically implies
‘mainstream’ (i.e., including freshwater ecology), with the division
based more on the sociology of ecological research than on the
physical characteristics of the medium. All of this simply serves to
reinforce the point that there are many more interesting comparisons to be made than simply between generic ‘marine’ and
‘terrestrial’ ecology [9].
precisely because the physics of the medium is under explicit
consideration. Introducing a recent special issue of the
Journal of Experimental Biology on ‘Biophysics, bioenergetics and mechanistic approaches to ecology’, Denny [17]
boasts: ‘Bacteria, phytoplankton and seaweeds; salmon
and jellyfish; vultures, dragonflies, mussels and lizards;
we have them all’; and although the umbrella term ‘ecomechanics’ [18] retains a largely marine flavour to date, it has
great potential to unite workers based on a common methodological approach rather than a specific habitat. However,
in this article, I focus on levels of ecological complexity at
larger spatial scales: the disciplines of community ecology
and macroecology, where comparisons must consider the
interactions between multiple individuals of many species
and, thus, may be more complicated.
More specific contrasts are likely to be most revealing, such
as comparing invertebrate communities in soil and in
marine sediments [13,14], or terrestrial and marine members of a single taxonomic class [15]. Sensible comparisons
will depend on the specific question (Figure 1). For example, a food-web ecologist would have little to gain from
comparing trees and whales, yet such a comparison makes
sense in terms of the carbon cycle [16].
Comparative analyses will also vary in their focal levels of
ecological complexity. At the scale of individual organisms
interacting with the environment, physical differences between air and water (e.g., in terms of flow regime) are not as
pronounced as one’s intuition might suggest [9], and individual-level allometries may vary predictably across environments [14]. More generally, mechanistic approaches to
ecology may suffer less from the marine–terrestrial divide
Community ecology: the messy middle
‘The middle ground’, warned Lawton when speaking of the
complex interacting communities which sit between singlespecies population dynamics and regional-scale macroecology, ‘is a mess. . .do not expect universal rules, even simple
contingent general rules, to emerge’ [1]. Nonetheless, it is
at the community scale that some of the richest and most
revealing comparisons between marine and terrestrial
systems can be made, and where new approaches offer
the potential to test fundamental hypotheses concerning
the structure and diversity of assemblages. As discussed
above, marine and terrestrial systems clearly differ in
diversity, so any general theory of coexistence ought to
be able to explain patterns for both species-rich terrestrial
and phylum-rich marine systems, and to predict the conditions under which exceptions occur.
Box 1. Terminology
Box 2. Parallel evolution of diversity measures
The choice of methods, software, and even research questions is
governed as much by sociological factors to do with ease of use and
tradition within a specific discipline as by any scientific criteria. For
example, consider measures of evolutionary diversity. Faith [50]
defined phylogenetic diversity (PD) based on the evolutionary history
represented by a community of species. Conceptually, this is similar to
the measures of taxonomic diversity and distinctness (which I group as
TD) later defined by Clarke and Warwick [51]. Although the measures
differ in important ways, and each has its advantages and problems,
both involve summing (or averaging) the length of the branches on a
phylogenetic (or taxonomic) tree linking pairs of species. The important
point is that, although both papers were published in similar general
applied ecological journals, TD was developed by marine biologists,
working in a marine biological institution, and communicating
primarily with other marine biologists, whereas PD was developed
within the ecological ‘mainstream’ (Box 1). Therefore, although both
papers have been well cited (PD: 460 cites, TD: 291 cites, ISI Web of
Knowledge, March 2012), their citation patterns differ.
On the basis of their title or abstract, I was able to categorise
unambiguously all the papers citing [51] and 432 papers citing [50]
according to the focal realm of the study: terrestrial, freshwater,
marine, cross-realm, or conceptual (theoretical, methodological, or
conceptual discussions of diversity without reference to a specific
study system). I found that the measure used to quantify evolutionary
diversity was strongly contingent on the system in which the work
was done (Figure I). PD has been widely adopted in empirical studies
of terrestrial systems, whereas TD has predominantly been used in
marine systems. Equally striking is the contrast in conceptual studies,
with only 26 (9%) of citations to TD being conceptual, compared with
142 (31%) for PD. Whether this represents a terrestrial slant to most
conceptual studies is unknown.
536
Study system
Source
C
X
T
FW
M
TD
PD
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Figure I. Citation patterns for key taxonomic diversity (TD) and phylogenetic
diversity (PD) papers across different study systems: marine (M), freshwater
(FW), terrestrial (T), multiple systems (X), or conceptual studies (C). The width of
a bar reflects the overall number of citations within a given study system; the
height of the bars reflects the apportionment of these citations between to the
two sources. The interaction between approach (TD or PD) and system is highly
significant (deviance test between additive and saturated loglinear models,
P <0.00001).
Opinion
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Same taxon, different environments (e.g, gastropod molluscs [15])
Same function, different taxa (e.g, carbon storage in whales and trees [16])
Antipredator behaviour (e.g, wolves and elk, sharks and dugongs [30])
Trophic interactions (e.g, size-structured pelagic vs taxonomic terrestrial [2,14,24])
Macroecology of comparable assemblages (e.g, birds and fish [25])
Diversity in stable habitats (e.g, coral reefs and tropical forests [20,23])
Community structure in similar environments (e.g, soil and marine sediment [9,13,14])
TRENDS in Ecology & Evolution
Figure 1. Some potentially informative comparisons that can be made between marine and terrestrial systems. Comparisons can consider similar systems, taxonomic
groups, or ecological functions in the different habitats. Such targeted comparative studies are likely to be more revealing of key ecological commonalities and differences
than is a simple binary comparison between all ‘marine’ and all ‘terrestrial’ habitats and communities [9].
Explaining diversity
Explaining coexistence in diverse communities has taxed
ecologists for decades. One hypothesis, the Janzen–Connell (JC) effect, proposes that aggregations of conspecifics
are selected against by the actions of specialised natural
enemies, which limit recruitment of offspring in the immediate vicinity of reproductive adults [19]. Generally considered only in the context of tropical forests, there is
nothing so specific in the formulation of the JC effect;
indeed, one of the studies on which it is founded [20] gave
as much space to marine case studies (the action of predatory snails on intertidal barnacles) as it did to rainforest
trees. Of particular interest, in positing that, on land, the
conditions necessary for natural enemies to promote diversity are most likely to occur in the wet tropics, compared
with high latitudes where opportunities for specialisation
among predators are limited, Connell [20] notes: ‘. . .the
terrestrial high arctic resembles the high intertidal zone
where there is too short a time for the predators to feed
effectively. At the lower edge of the intertidal zone, the
predators can feed almost continuously, as they can in
those parts of the terrestrial wet tropics with little seasonal
change.’ In other words, not only is the theory explicitly
applied to both marine and terrestrial systems, but Connell also suggests that an extensive terrestrial latitudinal
gradient is replicated within a few tens of metres on a
single seashore. Indeed, Whittaker [21] considered this
intertidal gradient to be one of five major global ecosystem
gradients (ecoclines), and the suite of opportunities it offers
as a tractable analogue to larger-scale gradients is well
recognised [22] (although its vastly reduced scale relative
to the dispersal distances of the component organisms
cautions against pushing the analogy too far).
Connell [20] also identifies coral reefs as being similar
to tropical forests, where rarity and wide dispersion of
conspecific individuals is favoured by the presence of natural enemies, making an analogy between plants and
sessile animals that he further developed in a later influential article [23]. More generally, the environmental conditions (as measured by the typical spatial and temporal
scales of environmental variation) that are likely to select
for or against the evolution of specialisation are not restricted to either marine or terrestrial systems [6,9,10],
suggesting fruitful grounds for testing the role of natural
enemies in maintaining diversity within marine communities. Yet, to date, the JC effect has received effectively no
attention from marine ecologists: none of the 212 studies
that include the term ‘Janzen–Connell’ in their ‘topic’ field,
and only 12 (2%) of the 792 studies citing Connell’s original
paper [20] are of marine systems (data from ISI Web of
Knowledge, April 2012).
Interacting individuals
Framing marine–terrestrial comparisons in terms of the
nature of interactions between individuals, rather than
simply numbers of species, is useful because it introduces
ecological processes (e.g., competition and predation) that
are common to all environments. In terms of trophic interactions, there has been debate about whether food webs of
fundamentally different character result from differences
between aquatic and terrestrial systems in the degree to
which feeding is size structured, and in the relative roles of
top-down versus bottom-up control (reviewed in [2,24]). A
recent promising approach uses body size as a common
currency with which to compare interactions from an
individual to a network level across ecosystems [14]. The
focus on individual size as a structuring property of ecosystems derives primarily from studies of marine communities [4], where size structuring is most obvious and
taxonomy is least effective at capturing ecological roles
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Opinion
[25]; in general, size-based analyses have been less common in terrestrial ecology [4]. However, by quantifying
statistical variation between communities in the strength
of indices of size structure (e.g., various cross-species allometric relationships), one moves from a dichotomy (a
community is either size structured or it is not) to a
continuum [14], allowing more nuanced comparative analyses and lessening the temptation to enforce a rigid aquatic–terrestrial separation. Another important concept first
developed by marine ecologists before being profitably
applied more generally concerns the role of large-scale
patterns of climate variability on multitrophic ecological
interactions and the timing of reproduction and growth
[26,27]; climatic indices, such as the North Atlantic Oscillation, are now routinely used by terrestrial ecologists [8].
Common behaviours
One inevitable difference in the study of marine and
terrestrial systems concerns the amenability of the two
systems to direct observation. As Underwood [28] puts it,
terrestrial ecologists usually ‘. . .can actually see (or hear)
[their study] organisms in nature, in groups, in real time
and space. That is rarely true for ecologists studying fish or
benthic marine invertebrates because of the opacity of the
medium. Even when they can be seen, it is usually for very
short periods over very small spatial scales.’ Thus, what
marine ecologists gain in the ability to sample destructively across entire communities, and so measure, dissect and
chemically analyse multiple individuals, they may lose in
terms of deep natural historical understanding; a contention supported by the lack of basic biological information
for most marine species [29]. Nonetheless, when extensive
behavioural observations have been made, commonalities
between marine and terrestrial systems emerge [30]. For
example, dugongs Dugong dugon respond to the threat of
tiger sharks Galeocerdo cuvier across multiple spatial
scales, in a fashion surprisingly similar to the responses
of elk Cervus elaphus to wolves Canis lupus [30]. Such
comparative studies should lead to a more general understanding of how behaviour shapes the dynamics of ecological communities.
Community phylogenetics
A final example of the potential of cross-system collaboration in community ecology concerns the emerging field of
community phylogenetics [31,32], analysing together the
evolutionary history, biological characteristics, and patterns of occurrence of species. Empirical community phylogenetics has to date focused almost exclusively on
terrestrial systems [32]. Given that most terrestrial studies tend to be ‘taxocoenic’ (i.e., they focus on specific taxonomic groups, such as birds or butterflies, in isolation to
other organisms using the same resources [28]), this means
that the phylogenetic diversity encompassed in community
phylogenetic studies has tended to be rather low. Contrast
this with the tradition (indeed necessity) of considering
transphyletic interactions in marine studies [28] and it
becomes clear that applying community phylogenetic
methods to marine systems may allow for more direct tests
of specific hypotheses. For example, the prediction that
phylogenetic community structure will depend on the
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Trends in Ecology and Evolution October 2012, Vol. 27, No. 10
relative importance of physiological tolerances versus competition [32] could be tested using the gradient in the
intertidal zone from the highly competitive lower shore
to the physiologically stressful upper shore. In addition,
there appear to be no a priori predictions about whether
high phylum or species richness would lead to greater
competition [28]; thus, testing whether competition intensity varies with average relatedness within a community
would be of great interest.
A frequently cited obstacle to the application of phylogenetic ecology to marine systems is the lack of comprehensive phylogenies for marine taxa. One possibility is to
use taxonomy as a surrogate for phylogeny [33,34]; however, more exciting is the potential of new methods directly
to address the phylogeny gap. For example, although DNA
barcodes were originally devised as an identification tool,
they can also provide a bridge between taxonomy and
phylogenetics [35]. The major animal barcode (cytochrome
c oxidase subunit I; COI) contains at least some phylogenetic signal [36] and, when paired with other initiatives to
resolve deeper nodes in the animal tree [37], could provide
a route to resolving evolutionary relationships across entire communities (see [38] for an example of what has
already been achieved in a plant community). This is
important because DNA barcoding does not have the traditional bias towards large-bodied, charismatic groups: of
approximately 170 000 barcoded animal species, from 23
phyla, >90% are invertebrates and approximately 10–15%
are marine (T.J.W., unpublished analysis of data obtained
from the Barcode of Life Data System [39], April 2012), a
figure rather similar to the 18% of recorded animal species
that are marine [12]. Such advances mean that we may
soon enter a new era in the availability of comprehensive
phylogenies for marine assemblages.
Macroecology: statistical order from the scrum
Lawton [1] felt that the best chance of finding simple
ecological rules lay in stepping back from the ‘mind-boggling details’ of community ecology to see the bigger picture; that statistical order and manageable contingency
emerge from the scrum at large spatial scales. Likewise, it
is at such macroecological scales that the broadest similarities (and possibly the most revealing differences) between
marine and terrestrial systems may lie [4,9] (see [6] for a
trans-realm discussion of the related discipline of biogeography). In particular, the statistical tools of macroecology
offer a means to test some of the hypotheses outlined
above.
Although most macroecology to date has concerned
terrestrial systems [4], sufficient evidence now exists to
state that general macroecological patterns and relationships also appear to hold in the sea. For instance, most
marine species are rare, whether one measures numbers of
individuals (species–abundance distributions, SADs [40])
or spatial distribution (species–range size distributions
[41]), and the relationship between local abundance and
regional distribution (the abundance–occupancy relationship, AOR) is typically positive [25]. Likewise, both the
latitudinal gradient in species richness and the species–
area relationship (SAR) appear to have general support
across marine and terrestrial systems [42,43].
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Trends in Ecology and Evolution October 2012, Vol. 27, No. 10
From pattern to process: the role of environmental
variation
Such generality is encouraging, but common patterns need
not imply common mechanisms and comparative studies of
marine and terrestrial ecosystems are likely to be revealing as macroecology seeks to become more mechanistic in
its approach. For instance, the physiological characteristics of a group of species must surely influence how extensively they are distributed. Thus, the finding that
latitudinal trends in thermal tolerance and niche filling
differ predictably between marine and terrestrial systems
[44,45] has important implications when using macroecological ‘rules’ to predict the responses of species in different
systems to a changing climate. If the pace and scale of
human activities leads to a convergence of marine and
terrestrial environmental dynamics [7], then studying the
macroecology of a variety of systems offers the best chance
of predicting responses to environmental change.
Differences in environmental variability present a major
opportunity for theoretical advances in macroecology. For
instance, seasonal variation in temperature, already dampened at the sea surface compared with on land [44,46],
almost disappears in the deep sea whether one considers
a single site [47] or an entire ocean (Figure 2). Of course, even
at depth, there is considerable spatial variation in temperature and other environmental variables (such as energy
availability), which are important in structuring deep-sea
30°C
communities [34]. However, the key point is that, by studying the considerable variation in biological diversity in the
deep sea, it may be possible to isolate the effects of differences in mean environmental conditions from differences in
environmental variability in a way that is seldom achievable
on land. Other widely distributed deep-sea habitats, for
instance chemosynthetic ecosystems [48,49], offer similar
comparative opportunities.
The role of biology: towards a trait-based macroecology
Another opportunity for the marine macroecologist derives
from the tendency for marine sampling programmes to
target entire multi-phylum communities, such that comparable data on the key macroecological variables of abundance and distribution are often available across taxa
varying considerably in their biological traits [33]. Again,
this opens up novel comparative possibilities, for instance
comparing the distributions of related species with differing dispersal modes (e.g., sessile benthic species with or
without a planktonic larval phase, or holo- and meroplanktonic species [9,33]). Clearly, the availability of biological
trait data will be a limiting factor here [29]; however,
where suitable data are available, interesting comparisons
between purely taxonomic and purely trait-based macroecology are possible; for instance, the contrast between
species-based and size-structured AORs in marine
fish [25].
30°C
Temperature
Sea surface
4000–5500 m
25°C
25°C
20°C
20°C
15°C
15°C
10°C
10°C
5°C
5°C
0°C
0°C
66°S
23°S
0°
Latitude
23°N
66°N
66°S
23°S
0°
23°N
66°N
Latitude
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Figure 2. Latitudinal variation in sea-water temperature in the Atlantic Ocean at the sea surface and in the deep sea. Data are from The World Ocean Atlas 2009 [52], for
longitudes between 08 and 308W, and for both ‘winter’ (January–March) and ‘summer’ (July–September) to reflect annual variation in both hemispheres. The World
Ocean Atlas uses all available observations to derive temperatures at standard depths, and presents them as means of five decadal periods at a 18 resolution. Full details
of the quality control and interpolation algorithms used are given in [52], as are limitations of the data (e.g., a general decline in the number of observations with depth).
The general pattern shown here, of far less latitudinal and seasonal variation in temperature in the deep sea compared with at the sea surface, is robust to such
limitations.
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Opinion
Concluding remarks
The physical differences between marine and terrestrial
systems clearly impact the way in which organisms interact with each other and their environment. However,
rather than assuming that these differences have
resulted in fundamentally different ecological processes
in the two domains, carefully construed cross-system
comparisons in which physical differences are either
eliminated as much as possible (e.g., by comparing marine and terrestrial sediment communities [13]) or are
explicitly accounted for in the analysis (e.g., relating
biological attributes such as body size or range size to
metrics of the biophysical environment [9]) offer an effective route to understanding how the environment determines ecological process. The fact that structural barriers
exist to such cross-system collaboration, in terms of the
institutional and intellectual separation of marine from
‘mainstream’ ecology [3,4,7], perhaps explains why such
efforts have historically been rather thin on the ground.
However, exploring when ecological theory can cross the
land–sea boundary and, equally importantly, when it
cannot, can be revealing. As Underwood [28] puts it,
‘Reflecting on differences – even if they are not real, or
if real, intractable – at least gives one pause for thought
about what might actually matter.’ If one embraces the
variability within and among ecosystems, is it possible to
tease out generalities in the way that putative ecological
‘rules’ are contingent on specific biotic and abiotic settings? We must hope so, because predicting how communities will respond to environmental change will depend
on it.
Acknowledgements
T.J.W. is a Royal Society University Research Fellow. Thanks to Dave
Raffaelli, Nick Dulvy, Rob Freckleton, Al McGowan, Simon Jennings,
Paul Somerfield, Andy Clarke, Remi Vergnon, and Alison Holt for past
discussion of these issues or for suggestions and comments on this work,
to Paul Craze for encouraging me to write it, and to Mike Dawson and an
anonymous reviewer for helping to improve it.
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