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This article has been published in published been This has article or collective redistirbution other or collective or means this reposting, of machine, is by photocopy article only anypermitted of with portion the approval The O of M a r i n e P o p u l at i o n C o nn e c t i v i t y

Population Connectivity and , Volume 3, a quarterly 20, Number The O journal of Conservation of Marine

B Y G e o FF r e y P. J O N E S, ceanography Society. Copyright 2007 by The O M AYA S r i N I VA S A N , A ND G l e N N R . a l M A N Y

An understanding of the extent to which marine populations are ceanography Society. A ceanography Society. Send all correspondence to:ceanography Society. Send [email protected] Th e O or connected by larval dispersal is vital, both to comprehend past impacts and future prospects for ll rights reserved. Permission is reserved. ll rights granted to in teaching copy this and research. for use article R sustaining biodiversity. Marine popu- lations and their supporting are now subject to a multitude of threats, most notably overharvesting, pollution, and (Hixon et al., 2001; Jackson et al., 2001; Hutchings and Reynolds, 2004; Kappel, 2005; Lotze et al., 2006). The intensity and scale of anthropogenic impacts in the world’s have increased dramatically during the industrial age (Jackson et al., 2001; Lotze et al., 2006), and these impacts are combining to acceler- ate the loss and fragmentation of important coastal , including man- groves (Ellison and Farnsworth, 1996; Alongi, 2002), (Duarte, 2002; Orth ceanography Society, P et al., 2006), (Dayton et al., 1998; Steneck et al., 2002), and coral reefs (McClanahan, 2002; Gardiner et al., 2003; Hughes, et al., 2003; Aronson and Precht, 2006). The increasing risk of in the is widely acknowledged (Roberts and Hawkins, 1999; Powles et al., 2000; Dulvy et al., 2003; Kappel, 2005; Reynolds et Box 1931, R O Box al., 2005), and the conservation of marine biodiversity has become a high priority for researchers and managers alike. ockville, MD 20849-1931, U ockville, epublication, systemmatic reproduction, S A .

100 Oceanography Vol. 20, No. 3 The increasing diversity, intensity, recent advances in our understanding of be of limited benefit where habitat loss and scale of human impacts on marine larval retention and connectivity, and to and fragmentation, pollution, and cli- systems will likely reduce potential con- explore their implications for evaluating mate change are contributing to declines nectivity among remnant populations, threats to marine biodiversity as well as in marine biodiversity (Allison et al., due to declining numbers and increas- different management options for mini- 1998; Jameson et al., 2002; Jones et al., ing fragmentation. It follows that the mizing these threats. 2004; Aronson and Precht, 2006). Also, resilience of a species to these impacts if MPAs simply result in a displacement will depend to a large degree on its dis- marine reserves and of effort (Hilborn et al., 2004, persal capability. Marine larvae exhibit biodiversity protection 2006), potential benefits of biodiversity extremes of larval dispersal, from those Marine reserves or no-take marine pro- protection inside MPAs may be offset by that travel just a few meters to others tected areas (MPAs) are now routinely an increase in the detrimental effects of with the potential to disperse thousands established both as management fishing outside reserves. of kilometers (Kinlan and Gaines, 2003; tools and for biodiversity protection. In some situations, the design of MPA Shanks et al., 2003). Species with wide However, while there is ample evidence networks for and dispersal capabilities may be less sus- that MPAs can provide a host of benefits biodiversity protection may have con- ceptible to global extinction because of to exploited populations within their flicting goals or outcomes. The optimal their large ranges, multiple populations, boundaries (Roberts and Polunin, 1991; sizes of MPAs for biodiversity conser- and potential for local recovery through Jones et al., 1993; Halpern and Warner, vation are likely to be larger than those larval transport. On the other hand, 2002; Halpern, 2003), the effectiveness of designed for protecting stocks and and disease vectors with MPA networks in biodiversity protection enhancing recruitment to adjacent fished high dispersal potential pose greater has received much less attention. Ideally, areas (Hastings and Botsford, 2003). global threats to marine biodiversity. The marine reserves should encompass rep- Large MPAs may be ideal for biodiversity problem we face is that the actual larval resentative regions/habitats so as to pro- conservation because they encompass dispersal distances of highly overfished, tect as much of the regional biodiversity more species, but they may limit the threatened, or invasive species are sel- dom known. While new technologies are leading to major discoveries concerning the scales of dispersal (Thorrold et al., ...a much greater knowledge of connectivity 2002; Palumbi et al., 2003; Levin, 2006), as yet, this knowledge is too incomplete is required in order to optimize strategies to be comprehensively incorporated into for conserving marine biodiversity. management strategies (Sale et al., 2005). Most approaches to the manage- ment of marine species and ecosystems are based on untested assumptions as possible (e.g., Airame et al., 2003; exploitation of to well below about typical larval dispersal distances. Beger et al., 2003; Fernandes et al., 2005). sustainable levels. Small MPAs may pro- Understanding connectivity is critical However, the degree to which reserves vide a protective umbrella for the bio- both for the design of achieve the goal of “protecting” species diversity of sedentary species but are networks to protect biodiversity and for is uncertain. Given that the majority of unlikely to provide an effective refuge for the development of conservation strate- marine species are not eaten (at least not highly mobile exploited species (Hilborn gies to protect species associated with yet), closing areas to fishing or collect- et al., 2004; Nardi et al., 2004). Increases degrading and fragmenting seascapes. ing does not necessarily address the pri- in the abundance and of large The aims of this essay are to highlight mary threats to most species. MPAs may exploited predators or space occupiers

Oceanography September 2007 101 in reserves may result in the decline of al., 2005; Purcell et al., 2006; Gerlach duration (PLD) of 10 days (Figure 1b). prey or inferior competitors, and thus et al., 2007), biophysical and hydrody- Almany et al. (2007) marked larvae of an overall decline in biodiversity (Jones namic models (Cowen et al., 2000, 2006; another clownfish (A. percula) with et al., 1993; Micheli et al., 2004). Getting James et al., 2002), metapopulation an 11-day PLD and a butterflyfish the right balance between reserve design models (Armsworth, 2002; Hastings and (Chaetodon vagabundus) with a 38-day for both exploitation and conservation Botsford, 2006), and fish otolith chem- PLD at Kimbe Island using maternally requires a detailed understanding of lar- istry (Swearer et al., 1999) have all indi- transmitted barium isotopes (Figure 1c). val dispersal patterns for the widest pos- cated both significant local retention and They found that 60% of the juveniles (a) sible range of marine species. the potential for long-distance dispersal. of both species were locallyCape Heussner spawned, 20 km Many larvae may settle much closer returning to a reef of only 0.3 km2. In New discoveries on to home than once thought possible. both studies, the other immigrant juveKimbe- Island variation in dispersal: For example, larval marking studies at niles must have traveled 10–20 km from Kimbe Bay implications for two small islands in Kimbe Bay, Papua

management New Guinea, (Figure 1a) show that a Geoffrey P. JoneSchumanns (geoffrey.jones@jcu. Island Directly tracking the movements of large proportion of juveniles of three fish edu.au) is Professor, School of Marine and marine organisms through their pelagic species are locally spawned. Jones et al. Tropical Biology, and Chief Investigator, larval stages is seldom possible. However, (2005) used both direct larval mark- Australian Research Council Centre of recent advances in technology are pro- ing (embryo immersion in tetracycline) Excellence for Studies, James (a) (b) viding new insights into the extent of and genetic parentageCape Heussner analysis to exam20 km- Cook University, Townsville, Queensland, marine larval dispersal, indicating more ine retention of clownfish (Amphiprion Australia. Maya Srinivasan and

local retention and a greater variation polymnus) larvae at SchumannKimbe Island. Island Glenn R. Almany are Postdoctoral in dispersal distances than once appre- They showed that a significant propor- Researchers, Australian Research Council Kimbe Bay ciated. Direct larval marking (Jones et tion (~ 30%) of larvae settling at the Centre of ExcellenceSchumann for Coral Reef Studies, Island al., 1999, 2005; Almany et al., 2007), island wereSchumann within aIsland few hundred meters James Cook University, Townsville, advanced genetic techniques (Jones et of their parents, despite a pelagic larval Queensland, Australia.

200 m Amphiprion polymnus

(a) (b) Cape Heussner 20 km (c)

Kimbe Island Amphiprion percula Kimbe Bay Schumann Kimbe Island Island Schumann Island

200 m 200 m Amphiprion polymnus Chaetodon vagabundus

(b) Figure 1. (a) Kimbe Bay, Papua New Guinea. Direct larval marking studies at two islands (Schumann and Kimbe)(c) show that many larvae settle much closer to home than previously thought. (b) Schumann Island. Larval marking via tetracycline immersion of embryos and genetic parentage analysis dem- onstrated ~ 30% self-recruitment in a population of the panda clownfish Amphiprion( polymnus), which have a 10-day pelagic larval duration. (c) Kimbe Island. Larval marking via maternal transmission of stable barium isotopes demonstrated ~ 60% self-recruitment in both the orange clownfish A.( percula; 11-day Amphiprion percula pelagic larval duration) and the vagabond butterflyfishChaetodon ( vaganbundus; 38-day pelagic larval duration). Percent of self-recruitment was defined as the proportionSchumann of the recruitment to a population that was a product of that population. Kimbe Island Island

102 Oceanography Vol. 20, No. 3

200 m 200 m Amphiprion polymnus Chaetodon vagabundus

(c)

Amphiprion percula

Kimbe Island

200 m Chaetodon vagabundus the nearest adjacent populations. Hence, relate closely to larval dispersal potential of suitable habitat (Figure 2d,e). A wide reef from semi-isolated subpopu- (Figure 2a–c). The higher the variance variance in dispersal kernels, including lations with a range of PLDs can exhibit in dispersal, the greater the realized con- significant levels of self-recruitment, will a wide variance and multimodal patterns nectivity within a species’ population result in multimodal patterns of realized in dispersal distances. range (Figure 2c). More often than not, dispersal that will maximize the persis- Realized dispersal distances may suitable habitat is discontinuous, and tence of the metapopulation (Figure 1f) be explained by a combination of the marine (meta) populations are made up (Hastings and Botsford, 2006). actual dispersal potential (a dispersal of many subpopulations that are linked Realized dispersal patterns have kernel based on how far larvae have the to an unknown degree and distance by important strategy implications for bio- intrinsic ability to disperse) and the dis- larval dispersal (Figure 2d–f) (Kritzer diversity conservation, such as optimal tribution of suitable habitat (Figure 2). and Sale, 2004). Greater dispersal abili- reserve size and spacing. As a general Where suitable habitat is continuous ties do not necessarily increase realized rule, an increasing range of effective and not saturated, the observed connec- dispersal unless they are sufficient to dispersal will require larger MPAs to tivity through much of the range may bridge the gaps between isolated patches achieve recruitment benefits within

C O N T I N U O U S H A B I T A T (a) Low (b) Medium (c) High R1 R2 R1 R2 R1 R2

dispersal potential realized dispersal R1 = reserve 1 R2 = reserve 2

P r o p o r t i o n P

F R A G M E N T E D H A B I T A T (d) Low (e) Medium (f) High R1 R2 R1 R2 R1 R2

P r o p o r t i o n P

Distance Distance Distance

Figure 2. Schematic representation of the influence of dispersal potential and habitat fragmentation on realized dispersal and optimal reserve size and spacing. Where habitat (orange horizontal bars) is continuous, realized dispersal reflects dispersal poten- tial, and optimal reserve (blue vertical bars) size and spacing increase with variance in realized dispersal (a–c). Where habitat is discontinuous, realized dispersal reflects a combination of dispersal potential and habitat fragment size and spacing (d–f). Realized dispersal only occurs if dispersal potential is sufficient to bridge gaps between patches of habitat. Optimal reserve size and spacing will be constrained by the size and spacing of habitat fragments.

Oceanography September 2007 103 boundaries and will allow a greater spac- representation of species inside reserves persal distances may under-represent ing of MPAs to achieve recruitment ben- (e.g., Diamond, 1975; Simberloff, 1988; the potential spread of larvae from efits beyond boundaries or connectivity Margules et al., 1982; Pressey et al., source populations. among MPAs (Figure 2a–c). Where habi- 1993). These approaches are increasingly If we explicitly incorporate larval tat is discontinuous, the optimal reserve being applied to MPA design, particu- retention and connectivity into the design of MPA networks for biodiversity conservation, then optimal outcomes depend on whether the goal is to maxi- Critical questions, such as how population mize benefits within MPAs, beyond their boundaries, or a balance between these connectivity will be influenced by the objectives (Figure 3). Individual, isolated increasing loss and fragmentation of marine MPAs cannot function as sanctuaries for within their boundar- habitats, are only beginning to be answered. ies unless the populations are big enough and there is sufficient self-recruitment to ensure persistence. Also, they cannot function as sources to repopulate locally size and spacing to ensure retention larly in relation to site selection (Turpie extinct populations beyond their bound- and connectivity may be constrained by et al., 2000; Roberts et al., 2002, 2003; aries unless there is sufficient longer- the size and spacing of habitat patches. Beger et al., 2003; Fox and Beckley, 2005; distance dispersal to do so. Given the Subpopulations that are not connected Fernandes et al., 2005). likely variance in dispersal (based on the because of limited dispersal capabil- There are relatively few analyses that information gathered so far), it is highly ity, geographic isolation, or increasing explicitly incorporate larval connectiv- probable that reserve size and spacing habitat fragmentation (Figure 1d,e), will ity and population persistence in reserve can be adjusted to achieve both of these take high conservation priority because design, and those that do primarily focus goals (Halpern and Warner, 2002; Jones of their reduced ability to recover from on reserves for fisheries management et al., 2005; Almany et al., 2007). local depletion or habitat degradation (Roberts, 1997; Botsford et al., 2001; (Roberts et al., 2006). Lockwood et al., 2002; but see Hastings 1. Reserve Size: Large Versus Small and Botsford, 2003). These models set The pros and cons of small versus large connectivity and the out to predict the optimal size, spacing, marine reserves have received increased design of marine reserve or cumulative area under different lev- attention (Halpern, 2003; Roberts et networks to protect els of dispersal. However, until realized al., 2003; Palumbi, 2004; Sale et al., biodiversity dispersal distances are confirmed for a 2005). There is substantial variation in The design of MPA networks, includ- wide variety of species, application of the size of existing no-take MPAs, from ing the size of individual reserves, the these models is limited. Typical larval < 1 km2 to > 1000 km2 (Halpern 2003), number of reserves, cumulative total dispersal distances, often inferred from but which is best? Even the smallest reserve area, the trade-off between a few indirect information such as PLD or reserves monitored appear to have local large or several small reserves, and the measures of genetic distance, have been benefits in terms of increases in fished spacing and locations of reserves, can be used to argue for the optimal size and species (e.g., Roberts and Hawkins, 1997; varied to achieve different conservation spacing of marine reserves for particu- Francour et al., 2001). However, in MPA goals. Most recommendations for the lar marine taxa (e.g., Sala et al., 2002; networks, larger reserves have advan- design of MPA networks are based on Shanks et al., 2003; Palumbi, 2004; Mora tages in terms of protecting significantly theory and practices that maximize the et al., 2006). However, “typical” dis- larger populations (Halpern, 2003) and

104 Oceanography Vol. 20, No. 3 enforcing compliance (Kritzer, 2004; recruitment benefits either inside or dramatically with reserve size. However, Little et al., 2005). beyond their boundaries (Figure 3a). little benefit may be achieved by increas- In terms of connectivity, extremely With significant local self-recruitment, ing reserve size above the level at which small reserves will provide minimal the benefit inside reserves should rise persistent populations can be achieved. Lockwood et al. (2002) calculated that to have a persistent population in an isolated reserve, reserve size should be about two times the mean dispersal dis- (a) Reserve size (b) Reserve number tance to ensure that it is substantially Inside Inside

Better self-recruiting. Recruitment subsidies beyond boundaries will increase in pro- Outside Outside portion to the perimeter of the reserve, so a bigger reserve will always be better. Few have attempted to put actual dimensions on optimal reserve size

Worse based on mean larval dispersal estimates. Small Large One Many Shanks et al. (2003) argue that marine reserves should be 4–6 km in diameter (c) Total reserve area (d) Single large or several small to be large enough to contain the larvae Inside Inside of short-distance dispersers. However,

Better Palumbi (2004) argues that greater Outside Outside variation in reserve sizes (1–100 km in diameter) is necessary due to the large variance in dispersal distances across taxa. Laurel and Bradbury (2006) sug-

Worse gest larval dispersal distances in fishes 0% 100% Several Single increase substantially with latitude, Percent total area small large suggesting marine reserves in temper- (e) Reserve spacing (f) Reserve location ate climes should be larger than those

R e s e r v e N e t w o r k D e s i g n Q u a l i t y in the tropics.

Better

Inside Inside 2. Reserve Number Outside Outside Assuming reserve sizes are the same, for conservation purposes, it should also be better to have as many MPAs as possible

Worse (Figure 3b). However, self-sustaining Near Far Source Sink populations inside reserves may be Isolated Not isolated R e s e r v e P a r a m e t e r achieved by a relatively small number of reserves, while recruitment subsi- Figure 3. Design guidelines for marine networks based on connectivity and achiev- ing optimal outcomes for recruitment benefits inside (green line) and outside (blue line) boundar- dies outside reserves and connectivity ies. (a) Individual reserve size. (b) Number of reserves. (c) Total reserve area (as percentage of total among reserves should increase in pro- habitat). (d) Single large versus several small. (e) Reserve spacing. (f) Reserve location (source versus portion to reserve number (Figure 3b) sink, isolated versus clustered). These guidelines are based on an assumption of a wide variance in dispersal ranges, including a significant level of localized recruitment. (Roberts et al., 2006).

Oceanography September 2007 105 ...total area protected is probably best adjusted to maximize recruitment subsidies beyond boundaries.

3. Total Reserve Area of exchange may be unnecessary for 4. Single Large or Several Small: The conservation benefits of MPAs inside persistence inside reserves. Hence, total The SLOSS Debate and outside reserves vary in relation to area protected is probably best adjusted The decision over whether a fixed pro- the proportion of the total area to be pro- to maximize recruitment subsidies portion of the total reserve area should tected (Hastings and Botsford, 2003). At beyond boundaries. be divided into either a few large or the lower extreme, with 0% of the habitat Few workers have put a figure on many small reserves is an important inside MPAs, obviously there can be no the proportion of the total habitat practical decision faced by managers. benefits either within or beyond bound- area inside reserves that is required for There has been conflicting opinion over aries. However, if 100% of the available biodiversity conservation, although which strategy maximizes the number habitat were protected, this would maxi- recommendations ranging between of species inside reserves, the so-called mize the benefits within boundaries but 20 and 50% have been published (e.g., SLOSS debate (Single Large or Several provide no benefits beyond boundaries Botsford et al., 2001, > 35%; Sala et Small) (Diamond, 1975; Simberloff, (Figure 3c). While this could be seen as al., 2002, 40%; Airame et al., 2003, 1988). Whether or not one of these alter- a fundamental conflict between design- 30–50%; Gell and Roberts, 2003, natives is better than the other depends ing MPAs for biodiversity protection and 10–20%; Halpern et al., 2004, < 50%). on the degree to which small reserves for sustainable fishing, increasing evi- Theoretically, the total area needed will represent nested subsamples of species dence for localized recruitment suggests increase with decreasing connectivity from larger reserves (Lomolino, 1994; that a relatively small total area will sup- (Roberts et al., 2006). Small, unique hab- Worthen, 1996). The few published port self-sustaining populations. While itats or endangered species will require comparisons of small and large marine inter-reserve connectivity will increase protection of 100% of the habitat or the reserves suggest that it may not make with the total proportion protected area supporting the population. much difference to the number of spe- (Roberts et al., 2006), such high levels cies protected (McNeill and Fairweather,

106 Oceanography Vol. 20, No. 3 1993; Stockhausen and Lipcius, 2001). There are a few specific recommen- outside reserves. Sinks (places that rely In terms of larval dispersal and bio- dations about MPA spacing based on solely on larvae imported from upstream diversity protection, whether a single generalizations about dispersal distances. for their persistence) will receive little large or several small is better again Shanks et al. (2003) recommend a spac- benefit from protection and should be depends on the goal. A single large MPA ing of 10–20 km for species with typi- resilient to “recruitment” may maximize population persistence cal pelagic larval durations to promote (Roberts, 1997). through self-recruitment, but several connectivity among adjacent reserves. It has been suggested further that smaller MPAs will maximize recruit- However, Palumbi (2004) argues for potential source reefs that are resistant ment beyond boundaries (Hastings and more variation in spacing (10–200 km) to perturbations should have the high- Botsford, 2003) (Figure 3d). However, if to reflect the likely variation in the dis- est MPA value, as they alone can source there is a high level of local retention, it persal abilities of fish and invertebrates. the recovery of damaged habitats (Salm is unlikely that it would make any differ- Kaplan and Botsford (2005) show that et al., 2006). However, while protecting ence over a broad range of reserve size/ variable spacing is better than fixed spac- source populations is critical, locating number combinations. Several medium- ing when there are several small reserves them is a difficult matter. Populations sized reserves, appropriately spaced, are rather than few large reserves. are usually classified as sources on the likely to maximize recruitment subsidies basis of hydrodynamic models (Roberts, from MPAs, simply because the mag- 6. Reserve Location 1997; Bode et al., 2006). For example, nitude of recruitment subsidies should Discussions about reserve location in Bode et al. (2006) predicted that popula- increase as a function of the sum of the relation to connectivity center on three tions on the northern Great Barrier Reef circumferences of all reserves (Figure 3d). main issues: (1) protecting source popu- in Australia are self-sustaining source lations, (2) protecting isolated popu- reefs, while those in the south may be 5. Reserve Spacing lations, and (3) protecting spawning reliant on the north for their persistence. As long as individual reserves are suf- aggregation sites. Larval “sources,” if they However, models that incorporate larval ficiently large to be substantially self- can be identified, make better reserves behavior and demography suggest that sustaining, the spacing of reserves may have little effect on reserve population persistence (Figure 3e). Persistence of populations inside reserves may be ...the increasing evidence for local retention marginally better if reserves are close together, because of increased recruit- of larvae argues that biophysical models must ment subsidies from other reserves be able to predict patterns of dispersal (Roberts et al., 2006). However, spac- ing will be much more critical to maxi- and connectivity at fine spatial scales. mizing recruitment subsidies outside reserves. Again, there is likely to be an optimal spacing, because if they are too close, this effectively restricts the area in than “sink” populations (Roberts, 1997), the scale at which marine populations between, and if they are too far apart, regardless of whether the priority is bio- act as sources may be more limited than they will not receive recruits from other diversity conservation or fisheries man- once thought (Cowen et al., 2006). reserves. As a general rule, the lower the agement. Sources must be prioritized Isolated islands or habitats have a high effective dispersal, the closer MPAs will because they (a) must be self-recruiting conservation priority because they often have to be to provide benefits to unpro- to persist, and (b) will provide an above- have unique assemblages and popula- tected areas (see Figure 2a-c). average recruitment subsidy to areas tions that are disconnected from all

Oceanography September 2007 107 others (Jones et al., 2002; Roberts et al., Why marine reserves are within their boundaries without restrict- 2006; Perez-Ruzafa et al., 2006). Sources insufficient to conserve ing access to an unreasonably large total of replenishment for populations along marine biodiversity reserve area. Hence, such species will coastlines or archipelagos may be greater, It is increasingly appreciated that marine always require a safety net of manage- affording them greater resilience. Given reserves “are necessary, but not suf- ment actions outside MPAs (Jones et al., that isolated islands rely on self-recruit- ficient” to manage exploited species or 2002). Overfished species may also need ment for their persistence, protecting a protect marine biodiversity (Allison et to be managed outside protected areas, relatively high proportion of the repro- al., 1998; Jameson et al., 2002; Aronson both to control overall fishing effort ductive population may be necessary to and Precht, 2006). A comprehensive (Hilborn et al., 2004, 2006) and to ensure avoid potential extinction. management plan must involve mini- an adequate source of larvae for all Many large marine organisms gather mizing human impacts both inside and unprotected areas (Almany et al., 2007). at widely separated, but spatially predict- outside MPAs. Individual populations able, spawning aggregation or breed- and local biodiversity inside MPAs can CONCLUSIONS ing sites (Vincent and Sadovy, 1998; be threatened by the buildup of large Clearly, a much greater knowledge of Claydon, 2005). As these areas encom- predators (Jones et al., 1993; Micheli et connectivity is required in order to opti- pass the main sources of larvae for local al., 2004) and extrinsic sources of envi- mize strategies for conserving marine or regional replenishment of popula- ronmental degradation, such as sedi- biodiversity. To our knowledge, empiri- tions, their protection is of paramount mentation and global climate change cal estimates of connectivity have never importance (Roberts et al., 2006). (Allison et al., 1998; Rogers and Beets, been incorporated into the design and However, where and how far larvae go 2001; Jones et al., 2004). Although some implementation of an MPA network. from particular aggregation sites remains exploited populations in degraded MPAs While improved estimates of connec- a mystery. On coral reefs, populations can benefit from protection (Hawkins tivity may not bring about changes to returning to well-known aggregation et al., 2006), the majority of unexploited existing MPA networks, it will help us sites are generally in decline, and recov- species may not. An idealized MPA to understand how they operate and to identify any deficiencies. Hopefully, future MPA designs will explicitly take into account larval sources, optimal MPA The increasing risk of extinction in the sea is sizes for animal sanctuaries, and optimal spacing to maximize recruitment sub- widely acknowledged..., and the conservation sidies in non-MPA areas. While there is of marine biodiversity has become a high increasing direct evidence that MPAs can provide benefits within and beyond their priority for researchers and managers alike. boundaries, such evidence is limited. There is also information to suggest that extrinsic disturbances from beyond their boundaries can negate these benefits. ery at locally extinct aggregation sites is network based on reliable estimates of Critical questions, such as how popula- limited (Sadovy, 1993; Sala et al., 2001). dispersal may change if ocean warming tion connectivity will be influenced by Local management of individual - and climatic conditions alter patterns the increasing loss and fragmentation ing aggregation sites may be critical of circulation and larval development of marine habitats, are only beginning if particular sites are not replenished (Munday et al., 2007). MPA networks to be answered. from other sources. cannot be designed to encompass all It is impractical to suggest that we rare and potentially threatened species will ever have detailed empirical data on

108 Oceanography Vol. 20, No. 3 larval dispersal for all marine species. national cooperation, especially among the world’s forests. Environmental Conservation 29:331–349. Ultimately, we must rely on biophysical small countries. Armsworth, P.R. 2002. Recruitment limitation, popu- models or other proxies of dispersal that The large range in dispersal distances lation regulation, and larval connectivity in reef fish metapopulations. 83:1,092–1,104. can be applied across a range of species that has been observed, even within spe- Aronson, R.B., and W.F. Precht. 2006. Conservation, with similar history characteristics. cies, is probably no accident. Populations precaution, and Caribbean reefs. Coral Reefs However, the increasing evidence for that are capable of persisting through 25:441–450. Beger, M., G.P. Jones, and P.L. Munday. 2003. local retention of larvae argues that bio- either mechanisms of self-recruitment Conservation of coral reef biodiversity: A compari- physical models must be able to predict or from larval supply from upstream son of reserve selection procedures for corals and fishes. Biological Conservation 111:53–62. patterns of dispersal and connectivity populations will be resilient to the widest Bode, M., L. Bode, and P.R. Armsworth. 2006. Larval at fine spatial scales. Cross-validation of range of disturbances. This variance may dispersal reveals regional sources and sinks in the different techniques for estimating dis- be sufficient to ensure populations can Great Barrier Reef. Marine Ecology Progress Series 308:17–25. persal and testing predictions using lar- benefit from a wide range of MPA sizes Botsford, L.W., A. Hastings, and S.D. Gaines. 2001. val marking studies will be necessary to and configurations, and indeed that may Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. increase the reliability of these models. be the best strategy. While it is unlikely Ecology Letters 4:144–150. To a large extent, managing marine that we can hope to get the manage- Claydon, J. 2005. Spawning aggregations of coral reef fishes: Characteristics, hypotheses, threats and biodiversity on the basis of information ment of all marine species completely management. Oceanography and : on connectivity will be a balancing act, right, we can take comfort in the fact An Annual Review 42:265–301. exploiting the advantages and minimiz- that it would also be impossible to get Cowen, R.K., K.M.M. Lwiza, S. Sponaugle, C.B. Paris, and D.B Olson. 2000. Connectivity of marine pop- ing the disadvantages of the extremes it completely wrong. ulations: Open or closed? Science 287:857–859. of dispersal. For species or habitats Cowen, R.K., C.B. Paris, and A. Srinivasan. 2006. Scaling of connectivity in marine populations. with low connectivity, local protection Acknowledgements Science 311:522–527. of populations will be enhanced, small This manuscript has benefited from Dayton, P.K., M.J. Tegner, P.B. Edwards, and K.L. Riser. 1998. Sliding baselines, ghosts, and reduced reserves will be effective, and there will discussions with members of the ARC expectations in kelp communities. Ecological be demonstrable benefits for local fisher- Centre of Excellence for Coral Reef Applications 8:309–322. ies and less need for international coop- Studies Connectivity Program, and Diamond, J.M. 1975. The island dilemma: Lessons of modern biogeographic studies for the design of eration in management. Low-dispersal members of the Coral Reef Targeted nature reserves. Biological Conservation 7:129–146. regions may also be more impervious to Research and Capacity Building (CRTR) Duarte, C.M. 2002. The future of meadows. Environmental Conservation 29:192–206. invasive species and pests. However, with Program, Connectivity Working Group Dulvy N.K., Y. Sadovy, and J.D. Reynolds. 2003. low connectivity comes the greater threat (CWG). Special thanks to S. Thorrold Extinction vulnerability in marine populations. Fish and Fisheries 4:25–64. of local and global extinction, and low and an anonymous reviewer for their Ellison, A.M., and E.J. Farnsworth. 2006. recruitment subsidies from MPAs or ref- contributions to the final draft. Anthropogenic disturbance of Caribbean man- uge populations. The total reserve area grove ecosystems: Past impacts, present trends, and future predictions. Biotropica 28:549–565. may have to be large and reserves closely REFERENCES Fernandes, L., J. Day, A. Lewis, S. Slegers, B. Kerrigan, spaced to maximize their benefits. Airame, S., J.E. Dugan, K.D. Lafferty, H. Leslie, D.A. D. Breen, D. Cameron, B. Jago, J. Hall, D. Lowe, and McArdle, and R.R. Warner. 2003. Applying ecologi- others. 2005. Establishing representative no-take On the other hand, with high larval cal criteria to marine reserve design: A case study areas in the Great Barrier Reef: Large-scale imple- dispersal and connectivity, subpopula- from the California Channel Islands. Ecological mentation of theory on marine protected areas. Applications 13:S170–S184. 19:1,733–1,744. tions will be resilient to local Allison, G.W., J. Lubchenco, and M.H. Carr. 1998. Fox, N.J., and L.E. Beckley. 2005. Priority areas for and recruitment subsidies from MPAs, Marine reserves are necessary but not sufficient conservation of Western Australian coastal fishes: A and remnant populations will be greater. for marine conservation. Ecological Applications comparison of hotspot, biogeographical and com- 8:S79–S92. plementarity approaches. Biological Conservation However, total protection of a popula- Almany, G.R., M.L. Berumen, S.R. Thorrold, S. Planes, 125:399–410. tion or species may be impossible, the and G.P. Jones. 2007. Local replenishment of coral Francour, P., J.G. Harmelin, D. Pollard, and S. reef fish populations in a marine reserve. Science Sartoretto. 2001. A review of marine protected value of small reserves may be limited, 316:742–744. areas in the northwestern Mediterranean region: and there will be a premium on inter- Alongi, D.M. 2002. Present state and future of Siting, usage, zonation and management. Aquatic

Oceanography September 2007 109 Conservation: Marine and Freshwater Ecosystems and others. 2001. Historical overfishing and the 2005. Effects of size and fragmentation of marine 11:155–188. recent collapse of coastal ecosystems. Science reserves and fisher infringement on the catch Gardiner, T.A., I.M. Cote, J.A. Gill, A. Grant, and A.R. 293:629–638. and biomass of coral trout, Plectropomus leopar- Watkinson. 2003. Long-term region-wide declines James, M.K., P.R. Armsworth, L.B. Mason, and L. Bode. dus, on the Great Barrier Reef, Australia. Fisheries in Caribbean corals. Science 301:958–960. 2002. The structure of reef fish metapopulations: Management and Ecology 12:177–188. Gell, F.R., and C.M. Roberts. 2003. Benefits beyond Modelling larval dispersal and retention patterns. Lockwood, D.R., A. Hastings, Botsford, L.W. 2002. The boundaries: The effects of marine reserves. Proceedings of the Royal Society of London, Series B effects of dispersal patterns on marine reserves: Trends in Ecology and Evolution 18:448–455. 269: 2,079–2,086. Does the tail wag the dog? Theoretical Population Gerlach, G., J. Atema, M.J. Kingsford, K.P. Black, and V. Jameson, S.C., M.H. Tupper, and J.M. Ridley. 2002. Biology 61:297–309. Miller-Sims. 2007. Smelling home can prevent dis- The three screen doors: Can marine “protected” Lomolino, M.V. 1994. An evaluation of alternative persal of reef fish larvae.Proceedings of the National areas be effective? Bulletin strategies for building networks of nature reserves. Academy of Sciences of the of America 44:1,177–1,183. Biological Conservation 69:243–249. 104:858–863. Jones, G.P., R. Cole, and C.N. Battershill. 1993. Lotze, H.K., H.S. Lenihan, B.J. Bourque, R.H. Halpern, B.S. 2003. The impact of marine reserves: Marine reserves: Do they work? Pp. 29–45 in Bradbury, R.G. Cooke, M.C. Kay, S.M. Kidwell, Do reserves work and does reserve size matter? The Ecology of Temperate Reefs: Proceedings of the M.X. Kirby, C.H. Peterson, and J.B.C. Jackson. Ecological Applications 13:S117–S137. Second International Temperate Reef Symposium, 2006. Depletion, degradation, and recovery Halpern, B.S., S.D. Gaines, and R.R. Warner. 2004. Auckland. NIWA Publications, Wellington. ISBN potential of and coastal . Science Confounding effects of the export of production 0-478-08327-0. 312:1,806–1,809. and the displacement of fishing effort from marine Jones, G.P., M.I. McCormick, M. Srinivasan, and J.V. Margules, C., A.J. Higgs, and R.W. Rafe. 1982. Modern reserves. Ecological Applications 14:1,248–1,256. Eagle. 2004. Coral decline threatens fish biodiver- biogeographic theory: Are there any lessons for Halpern, B.S., and R.R. Warner. 2002. Marine reserves sity in marine reserves. Proceedings of the National design? Biological Conservation have rapid and lasting effects Ecology Letters Academy of Sciences of the United States of America 24:115–128. 5:361–366. 101:8,251–8,253. McClanahan, T.R. 2002. The near future of coral reefs. Hastings, A., and L.W. Botsford. 2003. Comparing Jones, G.P., M.J. Milicich, M.J. Emslie, and C. Lunow. Environmental Conservation 29:460–483. designs of marine reserves for fisheries and for bio- 1999. Self-recruitment in a coral reef fish popula- McNeill, S.E., and Fairweather, P.G. 1993. Single diversity. Ecological Applications 13:S65–S70. tion. Nature 402:802–804. large or several small marine reserves? An experi- Hastings, A., and L.W. Botsford. 2006. Persistence of Jones, G.P., P.L. Munday, and M.J. Caley. 2002. Rarity mental approach with seagrass fauna. Journal of spatial populations depends on returning home. in coral reef fish communities. Pp. 81–101, in Coral Biogeography 20:429–440. Proceedings of the National Academy of Sciences of Reef Fishes: Dynamics and diversity in a complex Micheli, F., B.S. Halpern, L.W. Botsford, and R.R. the United States of America 103:6,067–6,072. . P.F. Sale, ed., Academic Press, San Diego. Warner. 2004. Trajectories and correlates of Hawkins, J.P., C.M. Roberts, C. Dytham, C. Schelten, Jones, G.P., S. Planes, and S.R. Thorrold. 2005. Coral community change in no-take marine reserves. and M.M. Nugues. 2006. Effects of habitat char- reef fish larvae settle close to home. Current Biology Ecological Applications 14:1,709–1,723. acteristics and sedimentation on performance of 15:1,314–1,318. Mora, C., S.Andréfouët, M.J. Costello, C. Kranenburg, marine reserves in St. Lucia. Biological Conservation Kaplan, D.M., and L.W. Botsford. 2005. Effects of A. Rollo, J. Veron, K.J. Gaston, and R.A. Myers. 127:487–499. variability in spacing of coastal marine reserves on 2006. Coral reefs and the global network of marine Hilborn. R., F. Micheli, and G.A. De Leo. 2006. fisheries yield and sustainability. Canadian Journal protected areas. Science 312:1,750–1,751. Integrating marine protected areas with catch reg- of Fisheries and Aquatic Sciences 62:905–912. Munday, P.L., G.P. Jones, M. Sheaves, A.J. Williams, ulation. Canadian Journal of Fisheries and Aquatic Kappel, C.V. 2005. Losing pieces of the puzzle: Threats and G. Goby. 2007. Vulnerability of fishes of the Sciences 63:642–649. to marine, estuarine and diadromous species. Great Barrier Reef to climate change. Pp. 357–391 Hilborn, R., K. Stokes, J.J. Maguire, T. Smith, L.W. Frontiers in Ecology and Environment 3:275–282. in Climate Change and the Great Barrier Reef. P. Botsford, M. Mangel, J. Orensanz, A. Parma, J. Rice, Kinlan, B.P., and S.D. Gaines. 2003. Propagule dispersal Marshall and J. Johnson, eds, Great Barrier Reef J. Bell, and others. 2004. When can marine reserves in marine and terrestrial environments: A commu- Marine Park Authority. improve fisheries management? Ocean & Coastal nity perspective. Ecology 84:2,007–2,020. Nardi, K., G.P. Jones, M.J. Moran, and Y.W. Cheng. Management 47:197–205. Kritzer, J.P. 2004. Effects of noncompliance on the suc- 2004. Contrasting effects of marine protected areas Hixon, M.A., P.D. Boersma, M.L. Hunter Jr., F. Micheli, cess of alternative designs of on the abundances of two exploited reef fishes E.A. Norse, H.P. Possingham, and P.V.R. Snelgrove. networks for conservation and fisheries manage- at the sub-tropical Houtman Abrolhos Islands, 2001. at risk. Pp. 125–154 in Conservation ment. Conservation Biology 18:1,021–1,031. Western Australia. Environmental Conservation Biology: Research Priorities for the Next Decade. M. Kritzer, J.P., and P.F. Sale. 2004. Metapopulation ecol- 31:160–169. Soulé and G. Orians eds, , Washington, ogy in the sea: From Levins’ model to marine Orth, R.J., T.J.B. Carruthers, W.C. Dennison, C.M. DC. ecology and .Fish and Fisheries Duarte, J.W. Fourqurean, W. James, H.K. Heck Jr, Hughes, T.P., A.H. Baird, D.R. Bellwood, M. Card, 5:131–140. A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, and S.R. Connolly, C. Folke, R. Grosberg, O. Hoegh- Laurel, B.J., and I.R. Bradbury. 2006. “Big” concerns others. 2006. A global crisis for seagrass ecosys- Guldberg, J.B.C. Jackson, J. Kleypas, and others. with high latitude marine protected areas (MPAs): tems. Bioscience 56:987–996. 2003. Climate change, human impacts and the Trends in connectivity and MPA size. Canadian Palumbi, S.R. 2004. Marine reserves and ocean neigh- resilience of coral reefs. Science 301:929–933. Journal of Fisheries and 63: borhoods: The spatial scale of marine popula- Hutchings, J.A., and J.D. Reynolds. 2004. Marine fish 2,603–2,607. tions and their management. Annual Review of population collapses: Consequences for recovery Levin, L.A. 2006. Recent progress in understanding Environment and 29:31–68. and extinction risk. Bioscience 54:297–309. larval dispersal: New directions and digressions. Palumbi, S.R., S.D. Gaines, H. Leslie, and R.R. Jackson, J.B.C., M.X. Kirby, W.H. Berger, K.A. Integrative and Comparative Biology 46:282–297. Warner. 2003. New wave: High-tech tools to help Bjorndal, L.W. Botsford, B.J. Bourque, R.H. Little, L.R., A.D.M. Smith, A.D. McDonald, A.E. marine reserve research. Frontiers in Ecology and Bradbury, R. Cooke, J. Erlandson, J.A. Estes, Punt, B.D. Mapstone, F. Pantus and C.R. Davies. Environment 1:73–79.

110 Oceanography Vol. 20, No. 3 Perez-Ruzafa A., M. Gonzalez-Wanguemert, P. Sala, E., E. Ballesteros, and R.M. Starr. 2001. Rapid Lenfant, C. Marcos, and J.A. Garcia-Charton. 2006. decline of Nassau grouper spawning aggregations Effects of fishing protection on the genetic struc- in Belize: Fishery management and conservation ture of fish populations. Biological Conservation needs. Fisheries 26:23–30. 129:244–255. Sale, P.F., R.K. Cowen, B.S. Danilowicz, G.P. Jones, J.P. Powles, H., M.J. Bradford, R.G. Bradford, W.G. Kritzer, K.C. Lindeman, S. Planes, N.V.C. Polunin, Doubleday, S. Innes, and C.D. Levings. 2000. G.R. Russ, Y.J. Sadovy, and R.S. Steneck. 2005. Assessing and protecting endangered marine spe- Critical science gaps impede use of no-take fishery cies. Journal of Marine Sciences 57:669–676. reserves. Trends in Ecology and Evolution 20:74–80. Pressey, R.L., C.J. Humphries, C.R. Margules, R.I. Salm, R.V., T. Done, and E. McLeod. 2006. Marine Vane-Wright, and P.H. Williams. 1993. Beyond protected area planning in a changing climate. Pp. opportunism: Key principles for systematic 207–221 in Coral Reefs and Climate Change: Science reserve selection. Trends in Ecology and Evolution and Management. Coastal and Estuarine Studies 8:124–128. 61, American Geophysical Union. Purcell, J.F.H., R.K. Cowen, C.R. Hughes, and D.A. Shanks, A.L., B.A. Grantham, and M.H. Carr. 2003. Williams. 2006. Weak genetic structure indi- Propagule dispersal distance and the size and spac- cates strong dispersal limits: A tale of two coral ing of marine reserves. Ecological Applications reef fish.Proceedings of the Royal Society, Series B 13:S159–S169. 273:1,483–1,490. Simberloff, D. 1988. The contribution of popula- Reynolds, J.D., N.K. Dulvy, N.B. Goodwin, and J.A. tion and community biology to conservation sci- Hutchings. 2005. Biology of extinction risk in ence. Annual Review of Ecology and Systematics marine fishes. Proceeding of the Royal Society, Series 19:473–511. B 272:2,337–2,344. Steneck, R.S., M.H. Graham, B.J. Bourque, D. Corbett, Roberts, C.M. 1997. Connectivity and management of J.M. Erlandson, J.A. Estes, and M.J. Tegner. 2002. Caribbean coral reefs. Science 278:1,454–1,457. ecosystems: Biodiversity, stability, Roberts, C.M., S. Andelman, G. Branch, R.H. resilience and future. Environmental Conservation Bustamante, J.C. Castilla, J. Dugan, B.S. Halpern, 29:436–459. K.D. Lafferty, H. Leslie, J. Lubchenco, and others. Stockhausen, W.T., and R.N. Lipcius. 2001. Single large 2003. Ecological criteria for evaluating candidate or several small marine reserves for the Caribbean sites for marine reserves. Ecological Applications spiny lobster? Marine and Freshwater Research 13:S199–214. 52:1,605–1,614. Roberts, C.M., and J.P. Hawkins. 1997. How small can Swearer, S.E., J.E. Caselle, D.W. Lea, and R.R. Warner. a marine reserve be and still be effective? Coral 1999. Larval retention and recruitment in an Reefs 16:150. island population of a coral-reef fish.Nature Roberts, C.M., and J.P. Hawkins. 1999. Extinction 402:799–802. risk in the sea. Trends in Ecology and Evolution Thorrold, S.R., R.S. Burton, G.P. Jones, M.E. Hellberg, 14:241–246. S.E. Swearer, J.E. Niegel, S.G. Morgan, and R.R. Roberts, C.M., C.J. McClean, J.E.N. Veron, J.P. Warner. 2002. Quantifying larval retention and Hawkins, G.R. Allen, D.E. McAllister, C.G. connectivity in marine populations with artificial Mittermeier, F.W. Schueler, M. Spalding, F. Wells, and natural markers: Can we do it right? Bulletin of and others. 2002. Marine biodiversity hotspots and Marine Science 70:291–308. conservation priorities for tropical reefs. Science Turpie, J.K., L.E. Beckley, and S.M. Katua. 2000. 295:1,280–1,284. Biogeography and the selection of priority areas Roberts, C.M., and N.V.C. Polunin. 1991. Are marine for conservation of South African coastal fishes. reserves effective in management of reef fisheries? Biological Conservation 92:59–72. Reviews in Fish Biology and Fisheries 1:65–91. Vincent, A.C.J., and Y. Sadovy. 1998. Reproductive Roberts, C.M., J.D. Reynolds, I.M. Côté, and J.P. ecology in the conservation management of Hawkins. 2006. Redesigning coral reef conserva- fishes. Pp. 209–245 in Behavioural Ecology tion. Pp. 515–537 in Coral Reef Conservation, I.M. and Conservation Biology, T. Caro, ed., Oxford Cote and J.D. Reynolds, eds, Cambridge University University Press, New York. Press. Worthen, W.B. 1996. Community composition and Rogers, C.S., and J. Beets. 2001. Degradation of marine nested-subset analyses: Basic descriptors for com- ecosystems and decline of fishery resources in munity ecology. Oikos 76:417–426. marine protected areas in the US Virgin Islands. Environmental Conservation 28:312–322. Sadovy, Y. 1993. The Nassau grouper: Endangered or just unlucky? Reef Encounter 13:10–12. Sala, E., O. Aburto-Oropeza, G. Paredes, I. Parra, J.C. Barrera, and P.K. Dayton. 2002. A general model for designing networks of marine reserves. Science 298:1,991–1,993.

Oceanography September 2007 111