Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs

Design and decision-making for marine protected areas (MPAs) on coral reefs require prediction of MPA effects with population models. Modeling of MPAs has shown how the persistence of metapopulations in systems of MPAs depends on the size and spacing of MPAs, and levels of fishing outside the MPAs. However, the pattern of demographic connectivity produced by larval dispersal is a key uncertainty in those modeling studies. The information required to assess population persistence is a dispersal matrix containing the fraction of larvae traveling to each location from each location, not just the current number of larvae exchanged among locations. Recent metapopulation modeling research with hypothetical dispersal matrices has shown how the spatial scale of dispersal, degree of advection versus diffusion, total larval output, and temporal and spatial variability in dispersal influence population persistence. Recent empirical studies using population genetics, parentage analysis, and geochemical and artificial marks in calcified structures have improved the understanding of dispersal. However, many such studies report current self-recruitment (locally produced settlement/settlement from elsewhere), which is not as directly useful as local retention (locally produced settlement/total locally released), which is a component of the dispersal matrix. Modeling of biophysical circulation with larval particle tracking can provide the required elements of dispersal matrices and assess their sensitivity to flows and larval behavior, but it requires more assumptions than direct empirical methods. To make rapid progress in understanding the scales and patterns of connectivity, greater communication between empiricists and population modelers will be needed. Empiricists need to focus more on identifying the characteristics of the dispersal matrix, while population modelers need to track and assimilate evolving empirical results.     

Low Connectivity between Mediterranean Marine Protected Areas: A Biophysical Modeling Approach for the Dusky Grouper Epinephelus marginatus

Marine protected areas (MPAs) are major tools to protect biodiversity and sustain fisheries. For species with a sedentary adult phase and a dispersive larval phase, the effectiveness of MPA networks for population persistence depends on connectivity through larval dispersal. However, connectivity patterns between MPAs remain largely unknown at large spatial scales. Here, we used a biophysical model to evaluate connectivity between MPAs in the Mediterranean Sea, a region of extremely rich biodiversity that is currently protected by a system of approximately a hundred MPAs. The model was parameterized according to the dispersal capacity of the dusky grouper Epinephelus marginatus, an archetypal conservation-dependent species, with high economic importance and emblematic in the Mediterranean. Using various connectivity metrics and graph theory, we showed that Mediterranean MPAs are far from constituting a true, well-connected network. On average, each MPA was directly connected to four others and MPAs were clustered into several groups. Two MPAs (one in the Balearic Islands and one in Sardinia) emerged as crucial nodes for ensuring multi-generational connectivity. The high heterogeneity of MPA distribution, with low density in the South-Eastern Mediterranean, coupled with a mean dispersal distance of 120 km, leaves about 20% of the continental shelf without any larval supply. This low connectivity, here demonstrated for a major Mediterranean species, poses new challenges for the creation of a future Mediterranean network of well-connected MPAs providing recruitment to the whole continental shelf. This issue is even more critical given that the expected reduction of pelagic larval duration following sea temperature rise will likely decrease connectivity even more.     

Dependence of sustainability on the configuration of marine reserves and larval dispersal distance

Marine reserves hold promise for maintaining biodiversity and sustainable fishery management, but studies supporting them have not addressed a crucial aspect of sustainability: the reduction in viability of populations with planktonic larvae dispersing along a coastal habitat with noncontiguous marine reserves. We show how sustainability depends on the fraction of natural larval settlement (FNLS) remaining after reserves are implemented, which in turn depends on reserve configuration and larval dispersal distance. Sustainability requires FNLS to be greater than an empir-ically determined minimum. Maintaining an adequate value for all species requires either a large, unlikely fraction (> 35%) of coastline in reserves, or reserves that are larger than the mean larval dispersal distance of the target species. FNLS is greater for species dispersing shorter distances, which implies reserves can lead to: (1) changes in community composition and (2) genetic selection for shorter dispersal distance. Dependence of sustainability on dispersal distance is a new source of uncertainty.     

Larval connectivity in an effective network of marine protected areas

Acceptance of marine protected areas (MPAs) as fishery and conservation tools has been hampered by lack of direct evidence that MPAs successfully seed unprotected areas with larvae of targeted species. For the first time, we present direct evidence of large-scale population connectivity within an existing and effective network of MPAs. A new parentage analysis identified four parent-offspring pairs from a large, exploited population of the coral-reef fish Zebrasoma flavescens in Hawai'i, revealing larval dispersal distances ranging from 15 to 184 km. In two cases, successful dispersal was from an MPA to unprotected sites. Given high adult abundances, the documentation of any parent-offspring pairs demonstrates that ecologically-relevant larval connectivity between reefs is substantial. All offspring settled at sites to the north of where they were spawned. Satellite altimetry and oceanographic models from relevant time periods indicated a cyclonic eddy that created prevailing northward currents between sites where parents and offspring were found. These findings empirically demonstrate the effectiveness of MPAs as useful conservation and management tools and further highlight the importance of coupling oceanographic, genetic, and ecological data to predict, validate and quantify larval connectivity among marine populations.     

What can genetics tell us about population connectivity?

Genetic data are often used to assess ‘population connectivity’ because it is difficult to measure dispersal directly at large spatial scales. Genetic connectivity, however, depends primarily on the absolute number of dispersers among populations, whereas demographic connectivity depends on the relative contributions to population growth rates of dispersal vs. local recruitment (i.e. survival and reproduction of residents). Although many questions are best answered with data on genetic connectivity, genetic data alone provide little information on demographic connectivity. The importance of demographic connectivity is clear when the elimination of immigration results in a shift from stable or positive population growth to negative population growth. Otherwise, the amount of dispersal required for demographic connectivity depends on the context (e.g. conservation or harvest management), and even high dispersal rates may not indicate demographic interdependence. Therefore, it is risky to infer the importance of demographic connectivity without information on local demographic rates and how those rates vary over time. Genetic methods can provide insight on demographic connectivity when combined with these local demographic rates, data on movement behaviour, or estimates of reproductive success of immigrants and residents. We also consider the strengths and limitations of genetic measures of connectivity and discuss three concepts of genetic connectivity that depend upon the evolutionary criteria of interest: inbreeding connectivity, drift connectivity, and adaptive connectivity. To conclude, we describe alternative approaches for assessing population connectivity, highlighting the value of combining genetic data with capture‐mark‐recapture methods or other direct measures of movement to elucidate the complex role of dispersal in natural populations.     

Genetic recruitment patterns are patchy and spatiotemporally unpredictable in a deep-water snapper (Lutjanus vivanus) sampled in fished and protected areas of western Puerto Rico

Marine protected areas (MPAs) have the potential to conserve biodiversity and improve fishery sustainability, but their efficacy depends on sound design and implementation, which requires an understanding of connectivity among reserves and between reserves and fished areas. Most studies of connectivity involving reserves focus on fishes with characteristics atypical for exploited species, making the results less applicable to fisheries management. Here, patterns of genomic diversity were assessed within and among geographic samples of juvenile of silk snapper, Lutjanus vivanus, collected in protected and fished areas on the western coast of Puerto Rico. The results indicate significant variation in spatiotemporal genetic recruitment patterns, with the two MPAs located off the shelf having partially decoupled recruitment processes from sites on the shelf. Spatial autocorrelation was found at distances less than 20 km within years, but the degree and pattern of spatial structure differed across years, suggesting that recruitment along the west coast of Puerto Rico originates from semi-independent units of spawners whose contribution varies in space and time. The results suggest that while MPAs may work to supplement fisheries where recruitment is spatiotemporally predictable, in species for which adult contribution is variable in space and time, other management strategies should be explored as well.

     

Kinship analyses identify fish dispersal events on a temperate coastline

Connectivity is crucial for the persistence and resilience of marine species, the establishment of networks of marine protected areas and the delineation of fishery management units. In the marine environment, understanding connectivity is still a major challenge, due to the technical difficulties of tracking larvae. Recently, parentage analysis has provided a means to address this question effectively. To be effective, this method requires limited adult movement and extensive sampling of parents, which is often not possible for marine species. An alternative approach that is less sensitive to constraints in parental movement and sampling could be the reconstruction of sibships. Here, we directly measure connectivity and larval dispersal in a temperate marine ecosystem through both analytical approaches. We use data from 178 single nucleotide polymorphism markers to perform parentage and sibship reconstruction of the black-faced blenny (Tripterygion delaisi) from an open coastline in the Mediterranean Sea. Parentage analysis revealed a decrease in dispersal success in the focal area over 1 km distance and approximately 6.5% of the juveniles were identified as self-recruits. Sibship reconstruction analysis found that, in general, full siblings did not recruit together to the same location, and that the largest distance between recruitment locations was much higher (11.5 km) than found for parent–offspring pairs (1.2 km). Direct measurements of dispersal are essential to understanding connectivity patterns in different marine habitats, and show the degree of self-replenishment and sustainability of populations of marine organisms. We demonstrate that sibship reconstruction allows direct measurements of dispersal and family structure in marine species while being more easily applied in those species for which the collection of the parental population is difficult or unfeasible.     

Conspecific and heterospecific attraction in assessments of functional connectivity

Functional connectivity is known to have an important, positive influence on species persistence. Measurements of functional connectivity traditionally focus on structural attributes of landscapes such as the distance and matrix type between habitat patches as well as on how species interact with those structural attributes. However, we propose that the social behavior of a species, through conspecific and heterospecific attraction, will also impact connectivity by changing how dispersers move with respect to each other and occupied patches. We analyzed functional connectivity patterns using circuit and graph theory for golden-headed lion tamarins (Leontopithecus chrysomelas) in Brazil under three scenarios. In the first scenario, we looked at connectivity without the effects of attraction under varying maximum dispersal distance and ecological movement cost thresholds. In the second scenario, we allowed dispersers to travel over more hostile matrix than they normally would to reach an occupied patch. In the final scenario, we allowed dispersers to move only to occupied patches. We found that, according to the first scenario, range-wide functional landscape connectivity for golden-headed lion tamarins is low at realistic maximum dispersal distance and movement cost thresholds. Incorporating the effects of conspecific or heterospecific attraction would increase functional connectivity, in the case of scenario two, or decrease functional connectivity, in the case of scenario three. Because conspecific/heterospecific attraction can have an impact on movement for some species, this factor should be incorporated in assessments of functional connectivity patterns for social species and others where patch occupancy is likely to influence the movements of dispersers.     

Integrating multiple species connectivity and habitat quality into conservation planning for coral reefs

Incorporating connectivity into the design of marine protected areas (MPAs) has met with conceptual, theoretical, and practical challenges, which include: 1) the need to consider connectivity for multiple species with different dispersal abilities, and 2) the role played by variable habitat quality in determining the spatial patterns of connectivity. We propose an innovative approach, combining biophysical modeling with a routinely‐used tool for marine‐reserve design (Marxan), to address both challenges by using ecologically‐informed connectivity parameters. We showed how functional demographic connectivity for four candidate reef‐associated species with varying dispersal abilities and a suite of connectivity metrics weighted by habitat quality can be used to set conservation objectives and inform MPA placement. Overall, the strength of dispersal barriers varied across modeled species and, also across species, we found a lack of spatial concordance of reefs that were high‐quality sources, self‐persistent, and stepping‐stones. Including spatially‐heterogeneous habitat quality made a considerable difference to connectivity patterns, significantly reducing the potential reproductive output from many reefs. We also found that caution is needed in combining connectivity data from modeled species into multi‐species matrices, which do not perform reliably as surrogates for all connectivity metrics of individual species. We then showed that restricting the habitat available for conservation has an inequitable impact on different connectivity objectives and species, with greatest impact on betweenness centrality and long‐distance dispersers. We used Brazilian coral reefs as a case study but our approach is applicable to both marine and terrestrial conservation planning, and offers a holistic way to design functionally‐connected reserves to tackle the complex issues relevant to planning for persistence.     

Large‐scale,multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park

Larval dispersal is the key process by which populations of most marine fishes and invertebrates are connected and replenished. Advances in larval tagging and genetics have enhanced our capacity to track larval dispersal, assess scales of population connectivity, and quantify larval exchange among no‐take marine reserves and fished areas. Recent studies have found that reserves can be a significant source of recruits for populations up to 40 km away, but the scale and direction of larval connectivity across larger seascapes remain unknown. Here, we apply genetic parentage analysis to investigate larval dispersal patterns for two exploited coral reef groupers (Plectropomus maculatus and Plectropomus leopardus) within and among three clusters of reefs separated by 60–220 km within the Great Barrier Reef Marine Park, Australia. A total of 69 juvenile P. maculatus and 17 juvenile P. leopardus (representing 6% and 9% of the total juveniles sampled, respectively) were genetically assigned to parent individuals on reefs within the study area. We identified both short‐distance larval dispersal within regions (200 m to 50 km) and long‐distance, multidirectional dispersal of up to ~250 km among regions. Dispersal strength declined significantly with distance, with best‐fit dispersal kernels estimating median dispersal distances of ~110 km for P. maculatus and ~190 km for P. leopardus. Larval exchange among reefs demonstrates that established reserves form a highly connected network and contribute larvae for the replenishment of fished reefs at multiple spatial scales. Our findings highlight the potential for long‐distance dispersal in an important group of reef fishes, and provide further evidence that effectively protected reserves can yield recruitment and sustainability benefits for exploited fish populations.     

The effects of dispersal and recruitment limitation on community structure of odonates in artificial ponds

I examined the effects of isolation on the structure of both adult and larval dragonfly (Odonata: Anisoptera) communities forming at physically identical artificial ponds over two years. Isolation, whether measured by distance to the nearest source habitat or by connectivity to multiple sources, was significantly negatively related to the species richness of dragonflies observed at and collected in these ponds. These results indicate that dispersal and recruitment limitation acted as filters on the richness of communities at these artificial ponds. The richness of larval recruits in artificial ponds was lower than the richness of adult dispersers observed at ponds, and distance from a source habitat explained a greater fraction of the variation in larval than adult richness (83 and 50%, respectively). These results and a male biased sex-ratio in adults observed at artificial ponds suggest that isolated habitats may be more recruitment limited than observations of dispersers would suggest. A Mantel test indicated there was a spatial component to the composition of communities forming in tanks, and that distance between tanks and community dissimilarity (1-Jaccard's) were significantly positively related (r=0.52). This pattern suggests that their position with respect to alternative source environments influenced the composition of the communities that recruited into these ponds. These results provide further evidence of recruitment limitation in this system. Results from this study highlight the importance behaviorally limited dispersal may have in taxa morphologically capable of broad dispersal and suggest that the role of dispersal and recruitment limitation may be critical in shaping community structure across habitat gradients that include variation in habitat duration.     

Relative impacts of adult movement, larval dispersal and harvester movement on the effectiveness of reserve networks

Movement of individuals is a critical factor determining the effectiveness of reserve networks. Marine reserves have historically been used for the management of species that are sedentary as adults, and, therefore, larval dispersal has been a major focus of marine-reserve research. The push to use marine reserves for managing pelagic and demersal species poses significant questions regarding their utility for highly-mobile species. Here, a simple conceptual metapopulation model is developed to provide a rigorous comparison of the functioning of reserve networks for populations with different admixtures of larval dispersal and adult movement in a home range. We find that adult movement produces significantly lower persistence than larval dispersal, all other factors being equal. Furthermore, redistribution of harvest effort previously in reserves to remaining fished areas ('fishery squeeze') and fishing along reserve borders ('fishing-the-line') considerably reduce persistence and harvests for populations mobile as adults, while they only marginally changes results for populations with dispersing larvae. Our results also indicate that adult home-range movement and larval dispersal are not simply additive processes, but rather that populations possessing both modes of movement have lower persistence than equivalent populations having the same amount of 'total movement' (sum of larval and adult movement spatial scales) in either larval dispersal or adult movement alone.     

Population Connectivity Shifts at High Frequency within an Open-Coast Marine Protected Area Network

A complete understanding of population connectivity via larval dispersal is of great value to the effective design and management of marine protected areas (MPA). However empirical estimates of larval dispersal distance, self-recruitment, and within season variability of population connectivity patterns and their influence on metapopulation structure remain rare. We used high-resolution otolith microchemistry data from the temperate reef fish Hypsypops rubicundus to explore biweekly, seasonal, and annual connectivity patterns in an open-coast MPA network. The three MPAs, spanning 46 km along the southern California coastline were connected by larval dispersal, but the magnitude and direction of connections reversed between 2008 and 2009. Self-recruitment, i.e. spawning, dispersal, and settlement to the same location, was observed at two locations, one of which is a MPA. Self-recruitment to this MPA ranged from 50–84%; within the entire 60 km study region, self-recruitment accounted for 45% of all individuals settling to study reefs. On biweekly time scales we observed directional variability in alongshore current data and larval dispersal trajectories; if viewed in isolation these data suggest the system behaves as a source-sink metapopulation. However aggregate biweekly data over two years reveal a reef network in which H. rubicundus behaves more like a well-mixed metapopulation. As one of the few empirical studies of population connectivity within a temperate open coast reef network, this work can inform the MPA design process, implementation of ecosystem based management plans, and facilitate conservation decisions.     

Designing marine protected areas for migrating fish stocks

This paper extends an earlier analysis and presents an investigation of how migration rates affect the performance of various types of management regimes with respect to economic yield and conservation benefits. Particular emphasis is placed on evaluating the geometric design of marine protected areas (MPAs). Earlier results have shown that MPAs are only likely to provide significant benefits when they are used in conjunction with direct catch or effort controls, unless they are quite large and cover most of the resource in question. Conversely, catch and effort controls are far more effective when protected areas are included in the management regime as a buffer against uncertainty. Dispersal of reproduction (recruitment) to other areas is an important expected benefit of protected areas, but such dispersal increases the variability of the effects of the area protection. If fishing mortality rates outside of the protected area are not controlled then dispersal can result in nullifying some of the benefits of the protected area. Similarly, adult migration increases the variability in the results when an area is protected and critically depends upon an overall control of fishing mortality outside the area. For both dispersal and migration separately or in combination, however, there are clear benefits to using MPAs in conjunction with catch or effort controls. These benefits are expressed in terms of long-term yield and recovery probabilities. In addition, short-term yield declines relatively slowly with increasing area protected. Design of the protected areas is seen to be important since using contiguous areas provide greater protection against overfishing than protected areas in isolation.     

Marine Reserves: from Beverton and Holt to the Present

The idea of using marine reserves, where all fishing is banned is not new to fisheries management. It was first formally considered by Beverton and Holt but rejected in favour of approaches such as fleet and gear control. Since that analysis, many fisheries have collapsed worldwide, illustrating the vulnerability of fishery resources and the ineffectiveness of these approaches. Empirical data and modelling suggest that marine reserves would generally increase yields, especially at the high fishing mortality that occurs in most fisheries. However, the most interesting feature of reserves is their ability to provide resilience to overexploitation, thereby reducing the risk of stock collapse. Benefits from reserves come from the increase in biomass and individual size within them, resulting in adult migration and/or larval dispersal that would replenish fishing grounds. The use of marine reserves in managing fisheries necessitates a thorough understanding of critical habitat requirements, fish movement, fish behaviour, the relations between subpopulations and the critical density effect for larval dispersal. When properly designed, and coupled with other management practices, reserves may provide a better insurance against uncertainties in stock assessment, fishing control and management by protecting a part of the population from exploitation. This strategy can be used for both sedentary and migratory species.     

Larval Connectivity and the International Management of Fisheries

Predicting the oceanic dispersal of planktonic larvae that connect scattered marine animal populations is difficult, yet crucial for management of species whose movements transcend international boundaries. Using multi-scale biophysical modeling techniques coupled with empirical estimates of larval behavior and gamete production, we predict and empirically verify spatio-temporal patterns of larval supply and describe the Caribbean-wide pattern of larval connectivity for the Caribbean spiny lobster (Panulirus argus), an iconic coral reef species whose commercial value approaches $1 billion USD annually. Our results provide long sought information needed for international cooperation in the management of marine resources by identifying lobster larval connectivity and dispersal pathways throughout the Caribbean. Moreover, we outline how large-scale fishery management could explicitly recognize metapopulation structure by considering larval transport dynamics and pelagic larval sanctuaries.     

Spillover from marine protected areas to adjacent fisheries has an ecological and a fishery component

Marine Protected Areas (MPAs), if well designed and managed, can produce conservation benefits to fish assemblages within no-take zones and fishery benefits in neighboring areas through ‘spillover’. However, although plenty of studies have provided evidence of the benefits produced within MPA boundaries, overall benefits to local fisheries, especially via spillover, seem to be still unclear. Because of the lost fishing grounds following an MPA establishment, local fishermen usually oppose MPAs. There is, therefore, the urgent need for a better understanding of the mechanism(s) through which MPAs can export fishable fish biomass towards adjacent fished areas, a process that could counterbalance the loss of fishing grounds. Here we review the literature on spillover for refining the terminology, detailing the underlying mechanisms and identifying both the existing and needed methodological approaches to measure spillover. Operationally, two types of spillover should be considered: ecological spillover (i.e. the net export of juvenile, subadult and adult biomass from MPAs outwards driven by density-dependent processes) and the fishery spillover (i.e. the proportion of this biomass that can be fished, taking into account regulations and accessibility). Underwater visual census and tagging/tracking may allow getting evidence of ecological spillover, while experimental catch data are essential to assess and monitor fishery spillover, which is the main component of MPAs that can provide direct benefit to local fisheries.     

Small-scale manjuba fishery around Cardoso Island State Park, SP, Brazil.

This work was carried out in the Enseada da Baleia and Vila Rápida communities. Data was provided by the Co-Management Committee of the Cardoso Island State Park (PEIC) on manjuba fishery management, technique and strategies used by the fishermen, as well as locally accumulated knowledge. Based on the results, social, ecological, and economic aspects of this type of fishing were analyzed. The importance of the accumulated knowledge and experience of this community, as well as the limitations imposed by local fishing gear, was concluded to be essential in conserving manjuba fishery conditions in the area. Industrial fishing, relevant state legislation, and market conditions were found to be the main obstacles to local fishery. Various proposals are suggested for manjuba fishery management, with emphasis on the need for fishing community participation in whatever measures are ultimately implemented.     

An overview of commercial fishers’ attitudes towards marine protected areas

Marine protected areas (MPAs) are attracting widespread attention worldwide as a tool for fishery management and marine ecosystem conservation. The establishment of MPAs has increased greatly in recent years mostly due to international commitments to the establishment of a global network of MPAs by 2012. MPAs have the potential to strongly affect the fishing industry, and their success depends, at least partly, on fishers’ attitudes towards this management measure. However, research on MPAs tends to focus on the ecological and conservation aspects of this management approach and not on its human dimensions. Studies in attitudes, perceptions, beliefs and preferences related to MPA issues have been identified as priority social science topics in need of research. We present a ‘rapid review’, conducted systematically, of the literature published up to September 2009 and aimed at identifying the most investigated topics related to commercial fishers’ attitudes towards MPAs, describing the main findings from these studies, and analysing the implications for management. Most published work focuses on fishers’ attitudes towards issues of governance, conservation of biodiversity and the environment, and the impact of MPAs on fishing activity. Despite the recent increase in the literature on the human dimensions of MPAs, the present review reveals that little of this literature originates from empirical studies. Hence, given the forthcoming increase in the implementation of MPAs in the near future, research on fishers’ attitudes towards these management measures is critically needed.     

Marine reserve design theory for species with ontogenetic migration

Models for marine reserve design have been developed primarily with ‘reef fish’ life histories in mind: sedentary adults in patches connected by larval dispersal. However, many fished species undertake ontogenetic migrations, such as from nursery grounds to adult spawning habitats, and current theory does not fully address the range of reserve options posed by that situation. I modelled a generic species with ontogenetic migration to investigate the possible benefits of reserves under three alternative scenarios. First, the fishery targets adult habitat, and reserves can sustain yields under high exploitation, unless habitat patches are well connected. Second, the fishery targets the nursery, and reserves are highly effective, regardless of connectivity patterns. Third, the fishery targets both habitats, and reserves only succeed if paired on adjacent, well-connected nursery and adult patches. In all cases, reserves can buffer populations against overexploitation but would not enhance fishery yield beyond that achievable by management without reserves. These results summarize the general situations in which management using reserves could be useful for ontogenetically migrating species, and the type of connectivity data needed to inform reserve design.