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Metapopulation ecology in the sea: from Levins’ model to
marine ecology and fisheries science
Jacob P Kritzer & Peter F Sale
Department of Biological Sciences, University of Windsor, Windsor, Ontario, Canada N9B 3P4
Introduction 132
Over-emphasis on extinction? 133
Ecology versus evolution, fisheries versus farms 133
A matter of scales 134
Example of metapopulation analysis in fisheries 137
Spatial structure and spatial management 137
Conclusions 138
Acknowledgements 139
References 139
Abstract
Marine and fisheries scientists are increasingly using metapopulation concepts to
better understand and model their focal systems. Consequently, they are considering
what defines a metapopulation. One perspective on this question emphasizes the
importance of extinction probability in local populations. This view probably stems
from the focus on extinction in Levins’ original metapopulation model, but places
unnecessary emphasis on extinction–recolonization dynamics. Metapopulation mod-
els with more complex structure than Levins’ patch-occupancy model and its variants
allow a broader range of population phenomena to be examined, such as changes in
population size, age structure and genetic structure. Analyses along these lines are
critical in fisheries science, where presence–absence resolution is far too coarse to
understand stock dynamics in a meaningful way. These more detailed investigations
can, but need not, aim to assess extinction risk or deal with extinction-prone local
populations. Therefore, we emphasize the coupling of spatial scales as the defining
feature of metapopulations. It is the degree of demographic connectivity that
characterizes metapopulations, with the dynamics of local populations strongly
dependent upon local demographic processes, but also influenced by a nontrivial
element of external replenishment. Therefore, estimating rates of interpopulation
exchange must be a research priority. We contrast metapopulations with other
spatially structured populations that differ in the degree of local closure of their
component populations. We conclude with consideration of the implications of
metapopulation structure for spatially explicit management, particularly the design of
marine protected area networks.
Keywords demographic connectivity, extinction, marine protected areas, metapop-
ulation, spatial management, spatial structure
Correspondence:
Jacob P Kritzer,
Department of
Biological Sciences,
University of Windsor,
Windsor, Ontario,
Canada N9B 3P4
Tel.:
+519 253 3000/ext.
2723
Fax: +519 971 3609
E-mail: kritzer@
uwindsor.ca
Received 2 Dec 2002
Accepted 6 Jun 2003
Ó 2004 Blackwell Publishing Ltd 131
F I S H and F I S H E R I E S , 2004, 5, 131–140
Introduction
The prevalence of the metapopulation concept in
ecology has increased dramatically since it was
originally proposed by Levins (1969, 1970), especi-
ally during the 1990s (Hanski and Simberloff 1997).
Most of the early empirical and theoretical research in
metapopulation ecology focused on terrestrial sys-
tems. However, in the late 1980s and early 1990s,
papers began to appear that addressed marine
ecology and marine resource management using
metapopulation concepts (Iwasa and Roughgarden
1986; Roughgarden and Iwasa 1986; Shepherd and
Brown 1993). Starting in the mid-1990s and con-
tinuing to the present, the integration of metapopu-
lation ecology into marine ecology and fisheries
science has dramatically increased (Stephenson
1999; Smedbol et al. 2002; Grimm et al. 2003). In
response to the increasing importance of metapopu-
lation concepts within their discipline, marine ecol-
ogists are beginning to consider the defining
properties of metapopulations so that they may better
apply the theory to their focal systems (Forrester et al.
2002; Smedbol et al. 2002; Grimm et al. 2003).
Marine ecologists have not been alone in addres-
sing the definitions and characteristics of metapop-
ulations. Hastings and Harrison (1994) approached
this issue from the perspective of population genet-
ics, Hanski and Simberloff (1997) and Hanski
(1999) explored this issue for population ecologists
in general, and Eriksson (1996), Husband and
Barrett (1996) and Freckleton and Watkinson
(2002) have done so in the context of plant ecology.
To date, no consensus has emerged from this
literature. Freckleton and Watkinson (2002), Smed-
bol et al. (2002) and Grimm et al. (2003) argue that
high extinction risk of one or more local populations
is a necessary defining characteristic of a metapop-
ulation. This position stems from the focus on
extinction and recolonization in Levins’ original
model. Freckleton and Watkinson also outline a
series of other types of spatially structured popula-
tions that are distinct from metapopulations. How-
ever, nowhere in their scheme do Freckleton and
Watkinson describe a population structure defined
by local populations that inhabit discrete patches,
are interconnected by dispersal and therefore influ-
ence one another’s dynamics, but without regular
local extinctions. Yet, this may be a very common
arrangement in marine systems.
An alternative perspective on metapopulation
ecology (Hastings and Harrison 1994; Hanski and
Simberloff 1997; Hanski 1999) allows a population
with this structure to be considered a metapopula-
tion. We agree with these authors, and view a
metapopulation as a system of discrete local popu-
lations, each of which determines its own internal
dynamics to a large extent, but with a degree of
identifiable and nontrivial demographic influence
from other local populations through dispersal of
individuals. This perspective defines a metapopula-
tion on the basis of the arrangement of local
populations and their interrelationships, but does
not specify any particular form of dynamics (i.e.
extinction–recolonization events) that must arise.
Those systems that conform to the specific features
of the Levins’ model are typically identified as
‘classical’ metapopulations, but the concept is
allowed to extend more widely and describe a
broader array of population phenomena.
Interestingly, many of the other assumptions of
the original Levins’ model have been relaxed
through time. The number of habitat patches is
allowed to be finite and patches are allowed to differ
in size, quality and position (Hanski 1999; Grimm
et al. 2003). Yet, extinction risk remains a critical
element for many authors. We do not see the
advantage of this restriction, and support those who
define metapopulations according to spatial struc-
ture rather than resultant dynamics. We prefer this
perspective because it allows the theory to grow and
diversify, and therefore become more widely useful,
rather than being confined to the few special cases
that exhibit ‘classical’ metapopulation features. For
example, when less emphasis is placed upon extinc-
tion, one can begin to ask what role interpopulation
exchange plays in determining local population size
and stability (see, e.g. Gyllenberg et al. 1997),
regardless of whether the local populations are likely
to go extinct. The local presence or absence of
organisms is certainly not the only question of
interest to ecologists and resource managers.
In this paper, we take the position that while
extinction–recolonization analysis was important in
founding the metapopulation concept, and contin-
ues to play a role in metapopulation ecology,
extinction risk of local populations is not the critical
feature that defines metapopulations. We argue that
Levins’ focus on extinction and recolonization was a
necessary consequence of the resolution of his
model (and perhaps the computational limitations
at the time of his initial metapopulation work) and
was appropriate for the questions he addressed.
However, in contrast to Levins’ focus on pest control
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
132 Ó 2004 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 5, 131–140
(Levins 1969) and species persistence in evolution-
ary time (Levins 1970), extinction–recolonization
analysis is of very limited use to fisheries scientists
relative to higher resolution analyses of changes in
population size and structure. We suggest that
Levins’ most important contribution was in defining
an important population structure in which local-
and regional-scale processes are linked, and that
with this concept, a much wider range of population
processes and dynamics can be considered. We
contrast metapopulations with other spatial popu-
lation structures, and discuss the implications of
these for spatial management of marine systems.
Over-emphasis on extinction?
It is likely that local extinction risk is commonly
identified as a critical criterion defining metapopu-
lations because local extinctions were a fundamental
component of Levins’ original model (Levin 1969,
1970). However, Levins’ focus on extinction–recol-
onization was a necessary consequence of modelling
a system simply in terms of presence or absence in
particular habitat patches, which served the purpo-
ses of his focal questions (as we discuss in the next
section). The development of metapopulation ecol-
ogy in the three decades since Levins’ work has seen
systems modelled with increasing detail to examine
more complex population processes. Although the
coarsest descriptor of a population addresses simply
whether organisms are present or absent, more
detailed descriptors can account for overall abun-
dance or biomass, the ratio of males to females and
the age, size and genetic structure of the population.
We are not claiming that adopting a metapopula-
tion definition based upon extinction probabilities
necessarily precludes modelling a system with great-
er complexity than simply presence–absence resolu-
tion, nor does it require that only questions about
extinction and recolonization be asked. Indeed,
metapopulation models with higher resolution have
been constructed, but these still often aim to address
questions of extinction (e.g. Stacey et al. 1997). Nor
do we claim that local or global extinction is not a
critical issue. However, rarely are other aspects of
population dynamics the focus, even if models
incorporate greater complexity (but see ‘Example of
metapopulation analysis in fisheries’ below). It seems
that the focus on extinction risk in defining meta-
populations has unnecessarily channelled research-
ers’ perspectives exclusively towards extinction–
recolonization issues at the expense of other critical
aspects of population dynamics. We do not see the
advantage of the extinction-based definition respon-
sible for this narrowing of focus. Moreover, we do not
see the advantage of excluding from metapopulation
theory systems that are not prone to local extinctions,
but are affected by demographic processes operating
at local and regional scales.
Ecology versus evolution, fisheries versus
farms
The more substantive of Levins’ original papers
(Levins 1970) develops metapopulation concepts to
largely address evolutionary questions. Specifically,
the goal of the paper was to explain the persistence
or extinction of species when confronted with the
instability of populations in local habitat patches as
determined by movements among those constituent
populations. Presence–absence is a sufficient level of
resolution to address such a question because the
attribute of interest is simply whether organisms
exist in a given habitat patch or not. In evolutionary
time, the nuances of population size and structure
in any individual year are often of limited import-
ance in determining long-term trends.
In contrast to evolutionary questions, presence–
absence resolution is inadequate for many questions
addressed by ecologists, particularly applied ecolo-
gists such as those working in fisheries. In ecology,
systems are often examined over shorter temporal
scales (relative to evolutionary time) but in greater
detail. Processes that operate on longer temporal
scales and larger spatial scales establish the persist-
ence of species and the extent of their geographical
distribution. Within the limits set by biogeographical-
and evolutionary-scale processes, shorter-term and
finer-resolution processes operate that are of interest
in population ecology and population genetics. When
greater resolution is incorporated, the potential range
of questions that can be examined extends well
beyond extinction–recolonization dynamics.
This is not to say that an extinction–recoloniza-
tion perspective is never relevant within the scope of
ecology, nor that these questions cannot be
addressed with presence–absence resolution. In fact,
Levins’ first metapopulation paper (Levins 1969)
worked within an ecological context that was suited
to analysis using presence–absence resolution.
Levins developed his ideas to consider the dynamics,
and therefore control, of agricultural pest insects.
Often, the goal of agricultural pest control is
outright eradication of the pest, either locally or
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
Ó 2004 Blackwell Publishing Ltd, F I S H and F I SH E R I ES , 5, 131–140 133
globally, so modelling population dynamics in terms
of extinction meets the objective at hand. Further-
more, insect populations are inherently highly
volatile. Most insect species have incredibly high
rates of reproduction and population growth, yet
are also highly sensitive to environmental change
and are therefore susceptible to population crashes
(Schowalter 2000). The combined effect of these
characteristics is that insects can quickly establish
large populations after colonizing a habitat patch,
yet can also rapidly decline following perturbation
regardless of current population size. Adopting
presence–absence resolution in such instances has
tremendous advantages in terms of mathematical
tractability. Moreover, Levins lacked the benefit of
modern computing power, which might have lim-
ited model complexity.
In contrast to agricultural pest control, fisheries
science typically must work at finer levels of
resolution when modelling populations (see Hilborn
and Walters 1992; Quinn and Deriso 1999). The
ecological dynamics of marine organisms are con-
strained within the bounds set by evolutionary
processes, but the focus of fisheries analysis must
often go to finer resolution. Usefully, the metapop-
ulation concept has implications for population
dynamics beyond simply persistence (Hastings and
Harrison 1994; Gyllenberg et al. 1997). While pest
control may focus on eradication, presence–absence
will only be a concern of fisheries in dire circum-
stances (e.g. the potential extinction of white
abalone in California; Davis et al. 1998). More
often, the focus is on the size and structure of a
population, which determine overall yield, and the
size of harvested individuals (of special importance
in sport fisheries).
Many large and/or long-lived marine organisms
(e.g. groupers, abalone, pinnipeds) do not have the
extremely high reproductive rates characteristic of
pest insects that allow simplification to presence–
absence resolution. Hutchings (2001) demonstrates
that recovery rates among marine fishes are highly
dependent upon the starting population size, which
must therefore be accounted for when understand-
ing stock dynamics. Presence–absence resolution is
especially inadequate if Allee effects are operating.
When Allee effects operate, a population might not
increase when below a critical density, so population
behaviour is actually similar to that in an empty
patch (e.g. Frank and Brickman 2000). This would
not be accounted for by focusing solely on extinc-
tion–recoloniztion dynamics; patches with a popu-
lation of any size greater than zero would be treated
equally as occupied. Although presence–absence
resolution has been used in some initial fisheries-
orientated metapopulation analyses (Man et al.
1995; Smedbol and Wroblewski 2002), the use of
metapopulation concepts to model fisheries stock
dynamics must ultimately involve greater detail.
A matter of scales
If extinction probability and extinction events are
one possible focus of metapopulation science, but
are neither the topics of primary interest in fisheries
science nor the defining attributes of metapopula-
tions in general, what is the essence of a metapop-
ulation? We support the arguments of Hastings and
Harrison (1994), Hanski and Simberloff (1997) and
Hanski (1999) that the unique feature of a meta-
population is the need to adopt two spatial scales to
fully understand system dynamics: the local patch
scale and the regional patch network scale. If the
dynamics of each individual population can be
modelled in isolation without reference to external
influences, then metapopulation concepts are not
appropriate (Fig. 1A). If, however, the inner work-
ings of these local populations largely dictate their
fate, but there is also a degree of replenishment from
outside the population that affects population
size and structure to an extent that it cannot be
ignored, then metapopulation concepts are relevant
(Fig. 1B). Note that this conceptual model of a
metapopulation incorporates the importance of both
local and external supply in population replenish-
ment, but is not contingent upon extinction–recol-
onization events. Ultimately, it is the level of
demographic connectivity among local populations
set by exchange of individuals that determines
whether or not they form a metapopulation.
Therefore, estimating rates of interpopulation
exchange must be a priority for future research.
A system comprised of distinct local populations
that share reproductive propagules (unlike Fig. 1A)
will not necessarily be a metapopulation. If interpop-
ulation exchange is sufficiently high, all populations
equally affect all others and the system experiences
regionally correlated population fluctuations, despite
patchy distribution of individuals within the region.
Metapopulation concepts are not appropriate for
these ‘patchy populations’ (Fig. 1C). Grimm et al.
(2003) argue that the general ‘openness’ of marine
populations is not adequate justification for confer-
ring metapopulation structure upon a system,
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
134 Ó 2004 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 5, 131–140
because dispersal can be sufficiently widespread and
recruitment sufficiently homogenized to remove the
distinction between local- and regional-scale proces-
ses. An important component of metapopulation
dynamics is asynchrony in local population dynam-
ics because of partial closure of local populations that
counteracts homogenization of regional dynamics
(Hanski 1999). In contrast to metapopulations,
regional dynamics in patchy populations (Fig. 1C)
can be predicted by simply scaling up from the local
scale (Freckleton and Watkinson 2002).
It is possible that a metapopulation perspective is
useful for a given system in some contexts but not in
others. For example, Sinclair (1988) argues that
many marine fish stocks evolve towards near total
local retention of offspring, with only demograph-
ically insignificant interpopulation exchange that is
sufficient to preclude genetic divergence. Sinclair
dubbed this idea the ‘Member-Vagrant Hypothesis’
to capture both the ecologically meaningful mem-
bership in local populations and evolutionarily
meaningful vagrancy that prevents speciation.
Thus, in an ecological context, systems structured
according to Sinclair’s hypothesis should not be
considered as metapopulations, but rather as dis-
crete and generally unconnected closed populations
(Fig. 1A). In other words, dynamics on ecological
time scales can generally be understood without
reference to other populations because local popu-
lation size and structure are not significantly
affected by immigrants spawned at other popula-
tions. However, on longer time scales, the limited
connectivity among distinct populations becomes
significant, and metapopulation concepts are there-
fore useful (Fig. 1B) in terms of maintaining genetic
similarity, offsetting local extinctions and therefore
influencing evolution and biogeography. The con-
text-specific applicability of metapopulation theory
reinforces Hanski’s argument that the metapopula-
tion concept is more of an analytical approach to be
used when appropriate rather than a set of strict
criteria and definitions (Hanski 1999).
Figure 1 Three types of spatially structured populations, with generalized dispersal curves from each local population.
Small circles represent discrete local populations within the larger region bounded by the outer oval. Thick lines define the
spatial scale at which population fluctuations are correlated. Arrows connect the sources of offspring with their eventual
destination. (A) Closed local populations experience independent dynamics with no ecologically meaningful exchange of
individuals. Dispersal distances are highly localized. (B) A metapopulation can be seen as a network of partially closed
populations. There is some degree of self-replenishment and independent dynamics, but this is coupled with nontrivial
supply from other populations. Dispersal distances are predominantly localized, but with identifiable levels of export to other
local populations. (C) A patchy population is effectively a single closed population, within which individuals are distributed
among discrete groups. Dispersal distances are distributed more evenly, with local populations essentially drawing from a
common larval pool. Note that other types of spatially structured populations exist (see Freckleton and Watkinson 2002).
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
Ó 2004 Blackwell Publishing Ltd, F I S H and F I SH E R I ES , 5, 131–140 135
Some systems are comprised of distinct local
populations that experience unique demographic
rates and population fluctuations (akin to Fig. 1-
A,B), but with no identifiable link between repro-
ductive output and recruitment at either the local
population scale or the regional scale (Fig. 2A). For
example, Pfister (1998) studied the population
ecology of tidepool sculpins. She found that recruit-
ment, mortality and growth could differ markedly
among distinct tidepools. However, reproduction
among tidepool sculpins involves larvae transported
out to sea when the tide covers the pool and then
returning to pools again during the flooding tide
after the pelagic larval stage. The scale of habitat
patches relative to the scale of potential transport
and mixing during the pelagic larval stage decou-
ples tidepool-scale larval production and subsequent
recruitment. Gotelli (1991) coined the term ‘prop-
agule rain’ to describe this complete decoupling
between offspring production and replenishment.
The propagule rain is a useful concept when the
origins of new recruits cannot be identified, but
ultimately those recruits must originate from some-
where. In fact, Gotelli suggests that the propagule
rain perspective is most useful for plants with seed
banks or other organisms with a mechanism for
storage of dormant early-life stages. In such cases,
the decoupling of offspring production and recruit-
ment is actually illusionary and is simply a conse-
quence of a considerable lag (possibly many years).
This is not the case among marine organisms, for
which larval supply closely follows production
(weeks to months). Establishing the relationship
between offspring production by a standing stock
and recruitment is a central objective of fisheries
science, and has even been dubbed its most
important problem (Hilborn and Walters 1992,
p. 241). If so, the propagule rain concept is of limited
use because we cannot assume that new recruits
emerge from undetermined sources. Rather, we
must account for larval production–recruitment
relationships, even if operating over large scales
with a high degree of spatial complexity.
Forrester et al. (2002) examined a system com-
prised of groups of gobies inhabiting small patch
reefs within a larger reef system that is analogous to
Pfister’s tidepool sculpins. Groups of fish on the
distinct patches studied by Forrester et al. can
experience independent demographic rates, but
there is no reliance upon local reproduction in
determining local recruitment. Although this is
essentially a system experiencing Gotelli’s propagule
rain (Gotelli 1991), Forrester et al. describe their
system as a ‘mesopopulation’. They adopt this
alternative term to distinguish between systems
with some identifiable relationship between repro-
ductive output and recruitment within the system
(i.e. metapopulations) and systems where no such
link can be established (i.e. a propagule rain).
In practice, the distinction between most meta-
populations and propagule rain metapopulations
(mesopopulations) in the marine environment is
likely one of breadth of spatial perspective, with the
latter (Fig. 2A) simply being a component of the
former (Fig. 2B). With a broader spatial perspective,
Figure 2 Multiscalar complexity of population structure.
Spatial scope (delineated by thick lines) is important in
determining perceived population structure. (A) On a small
scale, there might not be any discernible relationship
between offspring production and recruitment. The system
should be considered a mesopopulation (Forrester et al.
2002) experiencing propagule rain from indeterminate
sources (Gotelli 1991). (B) However, spatial scope can be
increased and neighbouring groups of organisms can be
considered collectively as one local population, but with
patchy internal distribution. This can then be linked with
similar composite local populations, demographic connec-
tivity can be mapped and the system can be viewed as a
metapopulation.
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
136 Ó 2004 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 5, 131–140
the ‘local populations’ of Pfister and Forrester et al.
(Fig. 2A) become simply distinct aggregations of
organisms within larger ‘local populations’ with
patchy internal distribution of individuals. These
composite local populations exchange propagules
with other neighbouring local populations (Fig. 2B).
Recruitment would be unrelated to reproductive
output when the spatial scope is confined to a single
mesopopulation (Fig. 2A), but partitioning larval
supply among local and external sources may be
possible when that scope expands to the entire
metapopulation (Fig. 2B). There have been attempts
to link offspring production with recruitment among
coral reef fishes (Robertson et al. 1988, 1993;
Meekan et al. 1993), and these would likely have
benefited from an increase in spatial scope to
account for more potential source populations.
These studies would also have benefited from an
increased temporal scope because important features
of large-scale systems might not emerge over short
time scales (Hughes et al. 2000). The idea of patches
within patches and populations of one structure
nested within populations of another structure
highlights the tremendous multiscalar complexity
of most ecological systems through space and time,
and the difficulty of assigning any to a single
conceptual model (Sale 1998).
Example of metapopulation analysis in
fisheries
At present, relatively few marine systems have been
explicitly studied within the metapopulation con-
text. However, Botsford and coworkers (Botsford
et al. 1994, 1998; Botsford 1995; Wing et al. 1998)
have conducted empirical and modelling work on
Dungeness crab, Cancer magister, along the Califor-
nia coast within a metapopulation framework that
is expanded from the classical extinction–recoloni-
zation perspective. They describe how spatial and
temporal variation in spawning date, temperature,
salinity, current speed, current direction and den-
sity-dependence affect survival and interpopulation
transport of larvae, and therefore determine spatial
and temporal variation in population fluctuations.
For instance, release of larvae late in the breeding
season by any subpopulation will yield higher
recruitment at more northerly locations because of
temperature profiles and water movements that are
more conducive to successful survival and transport
to those locations (Botsford et al. 1998). An import-
ant result is that these complex interactions typic-
ally result in asynchrony in population fluctuations
and therefore in catch rates. Again, such asynchr-
ony is a common effect of metapopulation structure
(Hanski 1999). Clearly, this spatio-temporal vari-
ability in catch has implications for fleet behaviour
and the economics of the fishery.
Stacey et al. (1997) illustrate how immigration
dampens within-patch fluctuations of acorn wood-
peckers, thereby minimizing the risk of stochastic
declines to small population sizes. Their analysis was
ultimately addressing extinction risk, but by consid-
ering population size and not simply population
presence, they were able to describe the mechanism
(dampened fluctuations) by which extinction risk is
minimized. The work of Botsford et al. is analogous to
that of Stacey et al. in that they consider the
implications of demographic connectivity for chan-
ges in local population size. However, importantly,
Botsford et al. do so without assessment of extinction
risk as the end goal. Local populations of Dungeness
crab may or may not be highly susceptible to
extinction, independent of external supply, but,
regardless, population dynamics and yield to the
fishery are affected in important ways through
metapopulation structure. Other applications of
metapopulation concepts to address complex fisheries
dynamics include McQuinn’s analysis of Atlantic
herring ecology (McQuinn 1997) and Ware and
Schweigert’s model of British Columbia herring
(Ware and Schweigert 2001, 2002) .
Spatial structure and spatial management
The use of marine protected areas (MPAs) as tools
for marine fisheries and conservation management
has received considerable attention over the past
decade (see reviews by Carr and Reed 1993; Dugan
and Davis 1993; Guenette et al. 1998; Russ 2002,
among others). There are numerous potential
benefits of MPAs, and the most appropriate MPA
network design will be contingent upon the specific
objectives. From a conservation standpoint, one
goal of MPAs is to protect natural population size
and structure in some pockets of habitat, akin to
terrestrial nature reserves. From a fisheries stand-
point, one goal is to subsidize fished populations
through dispersal of the greater reproductive output
produced by the larger and more fecund populations
housed within MPAs. Empirical studies generally
suggest that conservation benefits are achieved:
populations of exploited species protected within
MPAs have higher densities and larger mean body
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
Ó 2004 Blackwell Publishing Ltd, F I S H and F I SH E R I ES , 5, 131–140 137
sizes because they are living longer (reviewed by
Cote
´
et al. 2001; Russ 2002, among others). In
contrast, there is presently no evidence of enhanced
larval subsidy to fished areas following MPA desig-
nation, although logic suggests it should occur.
Interestingly, the magnitude of differences be-
tween populations within and outside of MPAs is
poorly correlated with MPA size (Cote
´
et al. 2001).
This is likely because the absolute size of MPAs is
not important, but rather the size relative to the
structure of the population, including the scale of
dispersal and the size of discrete local populations
(Fig. 1) is important. An MPA enclosing a local
population will completely protect the full cycle of
offspring production, recruitment and post-settle-
ment life stages when the system is comprised of
closed local populations (Fig. 1A), thus fully meet-
ing conservation objectives. However, there will be
no flow-on benefits to the fishery because the
increased egg production is not shared. On the
other hand, protecting a local population within a
patchy population (Fig. 1C) should have some
fishery benefits because overall system-wide egg
production will increase as a consequence of
increasing survivorship and fecundity in the pro-
tected population. However, conservation benefits
will not be as great relative to a closed local
population because the protected population itself
will be replenished in part from harvested popula-
tions whose fecundity has diminished. There are
likely to be positive changes within the MPA, but
population size and structure comparable to those in
the absence of fishing will not be achieved as they
would be in a closed population.
Among metapopulations (Fig. 1B), the general
effects of MPA implementation will be similar to
those in patchy populations (Fig. 1C). Fishery
catch will be enhanced by increased and shared
reproductive output. There will be a conservation
benefit because of reduced mortality in the MPA,
but population size and structure would fall short
of natural (unexploited) conditions because of the
partial reliance upon unprotected external sources
of replenishment. However, there is a critical
difference in expected MPA efficacy between pat-
chy populations and metapopulations. In patchy
populations, the precise location of MPAs is
effectively irrelevant. Dispersal is so widespread
and recruitment is so uniform that all local
populations are essentially equivalent to smaller-
scale components of the larger system that
produce and receive recruits equally in the
absence of protection. In contrast, not all local
populations are necessarily equal within a metapop-
ulation. Of the population types we consider, meta-
populations have the most complex internal
structure (Figs 1 and 2). The effectiveness of protect-
ing a particular local population will depend upon
local demography and linkages with other local
populations, including the degree of self-recruitment
and export of larvae to other local populations.
Therefore, which local populations fall within MPAs
is a key determinant of the extent to which both
conservation and fisheries benefits will be achieved.
Crowder et al. (2000) illustrate how the effectiveness
of MPAs is strongly determined by the choice of which
local populations within the metapopulation are
protected as MPAs. At present, we know too little
about which population structures are exhibited by
which marine systems. Therefore, until we have
much better information on the extent and spatial
scale of connectivity of target populations, we are not
in a strong position to make informed decisions on
MPA network design.
Conclusions
We agree with the argument of Hanski and Gilpin
(1991), reiterated by Smedbol et al. (2002), that
clarifying terminology is not simply an exercise in
semantics, but rather helps avoid inappropriate use
of concepts. However, in contrast to Smedbol et al.
(2002), we argue that the definition of a metapop-
ulation should not hinge on the likelihood of
extinction. Instead, we suggest that the critical
feature of metapopulations is the coupling of spatial
scales, whereby local populations experience
partially independent dynamics but receive some
identifiable demographic influence from other pop-
ulations. This can happen regardless of whether
local populations are in imminent risk of extinction,
and establishes estimation of demographic connec-
tivity as a research priority.
Interestingly, during the various efforts to define
metapopulations, neither we nor any of the other
authors who have addressed the question propose
quantitative definitions (e.g. ‘local extinction prob-
ability of at least 5%’ or ‘proportional self-recruit-
ment of at least 80%’). Such definitions would be
arbitrary and therefore not terribly productive.
However, not proposing precise, quantitative defini-
tions leaves an element of ambiguity that allows the
concept to be more or less freely applied, despite the
attempts by us and others to control its use. Hanski
Metapopulation concepts in marine ecology and fisheries science Jacob P Kritzer & Peter F Sale
138 Ó 2004 Blackwell Publishing Ltd, F I S H and F I S H E R I E S , 5, 131–140
(1999) has addressed this difficulty by arguing that
precise, quantitative definitions are less important
than clear understanding of the general concept, the
types of systems for which it has relevance and the
questions that can be addressed. So, the debate over
definitions is useful at least in directing focus on the
most important system features. We argue that these
features have more to do with levels of demographic
connectivity than with local extinction risk.
The contemporary focus on extinction risk in
defining metapopulations may be a consequence of
Levins’ (Levins 1969, 1970) original focus and
model resolution, but it runs the risk of relegating
the metapopulation concept to explaining a small
range of phenomena for a few special cases exhib-
iting classical metapopulation features. A much
wider array of system dynamics can be considered
by shifting focus away from local extinctions while
increasing model resolution, allowing more to be
done with Levins’ important concept (Hastings and
Harrison 1994; Gyllenberg et al. 1997). This is
especially important in the fisheries context, in
which we must address stock size and structure and
not simply local presence or absence of organisms.
Smedbol et al. (2002) conclude their paper with a
call for scientists and managers to refrain from
using metapopulation concepts when making fish-
eries management decisions. We support this
recommendation in the short term given the pau-
city of data on metapopulation structure in the
marine environment. However, we feel that scien-
tific research must progress with metapopulation
concepts in mind, seeking whether metapopulation
structure exists and what form it takes (also see
Grimm et al. 2003). Managers, while avoiding
premature application of metapopulation concepts,
should have in mind the potential for scientific
discovery of metapopulation structure when plan-
ning for the long term and should think about how
to accommodate and take advantage of this struc-
ture in resource management.
Acknowledgements
We thank Tony Pitcher for the opportunity to
contribute this paper. The manuscript benefited
tremendously from comments by Ilkka Hanksi, Ron
Karlson, Jon Lovett-Doust, Helen Murphy and two
anonymous reviewers. During preparation of this
manuscript, JPK held a postdoctoral fellowship
funded jointly by the University of Windsor and
NSERC-CRO Grant #225965–00 to PFS and others.
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