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Global marine protected areas do not secure the evolutionary history of tropical corals and fishes

Global marine protected areas do not secure the evolutionary history of tropical corals and fishes ARTICLE Received 18 May 2015 | Accepted 3 Dec 2015 | Published 12 Jan 2016 DOI: 10.1038/ncomms10359 OPEN Global marine protected areas do not secure the evolutionary history of tropical corals and fishes 1,2 3 2 1 4 5 6 2 D. Mouillot , V. Parravicini , D.R. Bellwood , F. Leprieur , D. Huang , P.F. Cowman , C. Albouy , T.P. Hughes , 7,8 1 W. Thuiller & F. Guilhaumon Although coral reefs support the largest concentrations of marine biodiversity worldwide, the extent to which the global system of marine-protected areas (MPAs) represents individual species and the breadth of evolutionary history across the Tree of Life has never been quantified. Here we show that only 5.7% of scleractinian coral species and 21.7% of labrid fish species reach the minimum protection target of 10% of their geographic ranges within MPAs. We also estimate that the current global MPA system secures only 1.7% of the Tree of Life for corals, and 17.6% for fishes. Regionally, the Atlantic and Eastern Pacific show the greatest deficit of protection for corals while for fishes this deficit is located primarily in the Western Indian Ocean and in the Central Pacific. Our results call for a global coordinated expansion of current conservation efforts to fully secure the Tree of Life on coral reefs. 1 2 UMR 9190 MARBEC, IRD-CNRS-IFREMER-UM, Universite de Montpellier, Montpellier 34095, France. Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia. CRIOBE, USR 3278 CNRS-EPHE-UPVD, Labex ‘Corail’, University of Perpignan, Perpignan 66860, France. Department of Biological Sciences and Tropical Marine Science Institute, National University of Singapore, Singapore 117543, Singapore. Department of Ecology & Evolutionary Biology, Yale University, 21 Sachem St, New Haven, Connecticut 06511 USA. 6 7 De´partement de biologie, chimie et ge´ographie, Universite´ du Que´bec a` Rimouski, 300 Alle´e des Ursulines, Rimouski, Canada G5L 3A1. Laboratoire ´ ´ d’Ecologie Alpine (LECA), Univ. Grenoble Alpes, Grenoble F-38000, France. Laboratoire d’Ecologie Alpine (LECA), CNRS, Grenoble F-38000, France. Correspondence and requests for materials should be addressed to D.M. (email: david.mouillot@univ-montp2.fr). NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 uman activities are altering ecosystems worldwide, maintain the integrity of coral reefs, thousands of changing their biodiversity and composition, and marine-protected areas (MPAs) have been created worldwide . Himperilling their capacity to deliver ecosystem services . However, the spatial design of the global MPA system is largely In this context, protected areas are indisputably the flagship tool contingent on local socioeconomic conditions and history rather 27,28 for protecting both ecosystems and biodiversity by limiting than regional or global considerations . Furthermore, given 2 29 direct human impacts . Conservation strategies have traditionally the limited resources dedicated to conservation efforts and the 21,30 focused on vulnerable components of taxonomic diversity such need to maintain coastal fisheries for people’s livelihoods , 3,4 as endemic, rare or threatened species . However, phylogenetic MPAs cannot be extended to all coral reefs. Guiding future diversity, represented by the Tree of Life, is becoming an conservation strategies thus remains a key challenge, particularly 5,6 increasingly important component of conservation science at a global scale where deficits of protection must be identified since it represents the breadth of evolutionary history and addressed to achieve effective protection of evolutionary and supports biodiversity benefits and uses, often unanticipated, history on coral reefs. Here we assessed the extent to which the 8,9 for future generations . Phylogenetically related species tend global system of MPAs represents individual species and to have similar functional traits, environmental niches and phylogenetic diversity for two major components of coral 10,11 ecological interactions , although numerous counter examples reef ecosystems, shallow-water corals in the order Scleractinia 12,13 exist . Therefore, species that are more phylogenetically (805 species) and fishes in the family of Labridae (452 species). distinct may have greater functional complementarity. In These groups contribute to the high biodiversity of tropical seas 32,33 turn, species assemblages that are more phylogenetically and help maintaining productive and resilient reefs . We show diverse may promote greater biomass production within and that the current global MPA system, covering 5.9% of the world’s across trophic levels even though a universal relationship coral reef area, does not meet the minimum conservation targets between phylogenetic diversity and ecosystem functioning considered necessary to adequately secure the branches of the 9,16 remains questionable . Yet, few studies have quantitatively Tree of Life for corals or fishes, particularly the longest branches assessed the extent to which protected areas encompass that represent the greatest amount of evolutionary history. 17,18 phylogenetic diversity and none have focused on marine taxa at a global scale. Here, we tackle this critical issue for the iconic but threatened Results and Discussion coral reefs of the world that support one of the largest Lag behind minimum conservation targets. Using global concentrations of biodiversity, around 830,000 multi-cellular distribution maps of each scleractinian coral and labrid fish species , and provide vital ecosystem services to half a billion species (Methods), we reveal that only 5.7% of coral species and 20 21 people including food security , financial incomes and 21.7% of fish species meet a minimum protection target of 10% protection against natural hazards . There is overwhelming potential coverage of their geographic range by the global system evidence that human activities, particularly fishing pressure of MPAs (Fig. 1). Regionally, the situation is even more 23 24 and pollution, affect coral reef ecosystem state , functioning contrasted. For example, coral species that occur exclusively in and resilience . Thus, to counteract human impacts and the Tropical Eastern Pacific all fall below the critical 10% coverage a b Scleractinian corals Labrid fishes 0 0 0.8 0.8 Alantic endemics Alantic endemics Eastern-Pacific endemics Eastern-Pacific endemics All other species All other species 0.7 0.7 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 0 01 2 3 4 0 100 200 300 012 3 4 040 80 120 6 2 6 2 Geographic range (×10 km ) Number of species Geographic range (×10 km ) Number of species Figure 1 | Relationship between the total geographic range of species and the proportion of that range covered by the global system of MPAs. (a) Scleractinian coral species and (b) fish species of the family Labridae. Histograms on top and to the right represent the distributions of total ranges and proportion of protection among species respectively. Coloured squares and triangles represent endemic species, that is, only present in one of the two biogeographic realms: Atlantic and Eastern Pacific, respectively. Dotted lines represent the 10% threshold corresponding to the minimum representation target for sustaining species persistence. 2 NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications Number Proportion of range covered by MPAs of species Number Proportion of range covered by MPAs of species NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 ARTICLE ab MPAs Scleractinian corals Labrid fishes % of PD coverage % of PD 0.50 > 20% 10.2 >10% & <20% 1.15 7.4 98.3 < 10% 82.3 Figure 2 | Percentages of geographic ranges covered by the global system of MPAs for species and internal branches across the Tree of Life. (a) Scleractinian coral species and (b) fish species of the family Labridae. Species or branches in red do not meet the minimum 10% representation threshold, that is, o10% of their geographic range is covered by MPAs, while green and blue colours indicate 10–20% and more than 20% coverage respectively. The corresponding percentage of total phylogenetic diversity (PD) is indicated for each coverage category. threshold. Similarly, all coral and fish species found only in extinctions remain scarce, partly due to limited assessment , the Atlantic have o20% coverage (Fig. 1). This 10% threshold but the functionally most distinctive fish species on coral reefs has been specifically advocated for wide-ranging species tend to be rare either in their geographic extent or their local 2 37 (4250,000 km ) and is regarded as a conservative target of abundance . We may thus anticipate a disproportional local loss 3,34 coverage by protected areas for sustaining species persistence . of functional diversity within coral reef communities if the This conservative cut-off takes into account commission errors, longest evolutionary branches are under threat and inadequately that is, the potential absence of a given species from protected protected . For instance long-branched lineages include areas that lie within its geographic distribution due to chance or relatively specialized forms, such as the large invertivore unsuitable habitats . Lachnolaimus and the world’s largest excavating parrotfsh By applying the same reasoning to the internal branches of the Bolbometopon which are severely overexploited, suggesting that phylogenetic trees (Methods), we show that only 1.7% ( 0.2 s.d.) the loss of long branches may result in the loss of unique and of the Tree of Life of corals and 17.6% ( 0.6 s.d.) of fishes attain functionally important groups . the minimum 10% coverage (Fig. 2). Thus 7,160 Myr of the evolutionary history of corals and 3,586 Myr of fishes are inadequately represented by the global MPA system, far more Global distribution of protection deficits. To highlight the than for many other threatened taxonomic groups . Globally, the critical gaps in protecting the Tree of Life on coral reefs, we amount of evolutionary history potentially covered by MPAs, that mapped the locations where the longest evolutionary branches is, the proportion of the geographic range of evolutionary that receive o10% coverage are concentrated using a regular grid branches overlapping with the global MPA system, is only of 5 5 cells (Methods). For corals, the longest evolutionary ± ± 6.0% ( 0.1 s.d.) and 8.7% ( 0.2 s.d.) for corals and fishes, branches with low protection are predominantly in the Atlantic, respectively. Coral evolutionary history receives significantly less Eastern Pacific and, to a lesser extent, the North Indian coverage than expected under a random distribution of species Ocean (Fig. 3b). These deficits of protection are only marginally geographic ranges across the Tree of Life (Po0.001, n¼ 999, correlated with the heterogeneous MPA coverage at the global randomization test) while fishes receive significantly more scale (r¼ 0.045, n¼ 304 5 5 grid cells, P40.05, Fig. 3a). protection than expected by chance (Po0.001, n¼ 999, Instead, the high proportion of longest branches, and their unique randomization test) (Methods). The greatest amount of evolutionary history, in the Atlantic and Eastern Pacific primarily evolutionary history is supported by the longest branches on drives this pattern (Fig. 4a,b). For fishes, the highest the Tree of Life. In our case, the top 10% longest extant and concentrations of poorly protected long branches are located in internal branches, corresponding to 48.68 Myr ( 0.5 s.d.) for the Western Indian, Central Pacific and, to a lesser extent, the corals and 410.7 Myr ( 0.25 s.d.) for fishes, support a Eastern Atlantic (Fig. 3c). As in corals, these deficits of protection disproportional amount of evolutionary history, with 62% are not correlated with the heterogeneous distribution of MPA ± ± ( 0.9% s.d.) and 34% ( 0.5% s.d.) for corals and fishes, coverage (r¼ 0.025, n¼ 287 grid cells, P40.05, Fig. 3a). Instead, respectively. These longest branches are overwhelmingly the pattern is driven by the relatively high proportion of under-represented within the global MPA system (Fig. 2). long evolutionary branches of fishes at the periphery of the Only 1.3% ( 0.6% s.d.) of the longest branches in corals and Indo-Pacific (Fig. 4c,d). The correlation between the proportion 20.2% ( 2.3% s.d.) in fishes are adequately protected by the of poorly protected longest evolutionary branches for corals and minimum threshold of 10% geographic coverage by MPAs. If fishes within assemblages is negative (r¼ 0.15; n¼ 287 grid those poorly protected longest branches support endangered cells, P¼ 0.30) suggesting that there is a global spatial mismatch, species we may expect large and abrupt changes in ecosystem albeit weak, of conservation needs for these two taxa. The Atlantic functioning following extinctions. This situation already exists for and Eastern Pacific tend to concentrate many long and poorly the world’s primates, where the most endangered species are both protected branches for corals but substantially less for fishes evolutionarily and ecologically distinct . In the sea global (Fig. 5). This most likely reflects the biogeographic history of the NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 3 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 MPAs Percentage of cell area covered by MPAs 0 10 20 100 Scleractinian corals Percentage of longest branches poorly protected (<10%) within each cell 911 16 42 c Labrid fishes Percentage of longest branches poorly protected (<10%) within each cell 489 12 Figure 3 | Global distribution of protection deficits to secure the Tree of Life on coral reefs. Global maps representing, for each cell (5 5), the percentage of coral reef habitat covered by MPAs (a), and the proportion of the longest evolutionary branches (top 10%) that receive less than the critical 10% coverage by the MPA system within coral (b) and fish (c) local assemblages. Colours correspond to three categories of values based on percentage of coverage for MPAs and on tertiles for corals and fishes. tropical Atlantic which has been characterized by isolation, thus the slowest rate of MPA establishment worldwide although maintaining old coral lineages in contrast to the recent positive outliers in environmental governance also occur at both 42 28 diversification in younger fish lineages , especially along the national and local levels . For example, the Dominican Republic Brazilian coast where there is extensive evidence of recent has already reached the target of 10% coverage. Similarly an colonization . In the Atlantic, therefore, there is a logical priority increase in conservation investment has promoted MPA to emphasize the protection of older coral lineages. For fishes, the establishment in Eastern Africa . Other countries of Western Atlantic hosts younger labrid lineages than the Indo-Pacific Africa and Eastern America remain far below the 10% coverage particularly in the Caribbean following cryptic speciation and and should be priority areas to better protect the evolutionary in the North Eastern Atlantic with subsequent diversification history of corals. For fishes, conservation investment are of Mediterranean lineages following the Messinian Salinity Crisis primarily needed in the Western Indian Ocean where poorly at 6 Myr (ref. 44). By contrast, the Coral Triangle, at the centre of protected longest branches are concentrated. the Indo-Pacific region, harboured most of the coral reef refugia during the Quaternary glaciations, hence acting as a ‘museum’ for the older labrid lineages . Limitations and less conservative protection assessment. Globally, the proportion of poorly protected longest branches Overall, our results show that the Tree of Life on coral reefs is in corals ranges from 9 to 42% compared with 4 to 12% in fishes inadequately represented by the current global MPA system, with (Fig. 3b,c), suggesting that conservation efforts should initially be most evolutionary branches, particularly the longest ones, focused on the Atlantic to better preserve the coral Tree of Life receiving o10% protection. Despite the magnitude of this where it is most at risk. West African and, to a lesser extent, South shortfall, our estimates are highly conservative because they are American countries that border each side of the Atlantic, show based on the assumption that all MPAs are able to protect every 4 NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 ARTICLE Scleractinian corals Percentage of longest branches within each cell Scleractinian corals Mean branch length within each cell Labrid fishes Percentage of longest branches within each cell Labrid fishes Mean branch length within each cell Figure 4 | Global distribution of the amount of evolutionary history on coral reefs. Global maps representing, for each grid cell (5 5), the percentage of the longest evolutionary branches (top 10%) and the mean evolutionary branch length within coral (a,b) and fish (c,d) local assemblages, respectively. Colours correspond to classes of the histograms representing the distribution of values across the cells. 49–51 coral and fish species that geographically overlaps with them. and recovery , the extent of these benefits may vary among It thus assumes that coral and fish species are present in all MPAs. Not all MPAs are able to ensure that fish and coral MPAs within their geographic ranges, and that all MPAs are communities are protected, due to poor compliance and effective in their protection. These assumptions may not be valid. enforcement . Furthermore, MPAs cannot prevent pulses of First, we have no proof of individual species presence within coral mortality from cyclones or coral bleaching , or from MPAs. These commission errors are inevitable given the chronic declines in coral recruitment and growth due to degraded 54,55 coarse grain of species geographic distributions and the small size water quality . MPAs in the Atlantic should better focus on of most MPAs. We therefore assess maximum potential coral lineages while those in the Western Indian Ocean should protection while the conservation target of 10% is partly set to primarily limit fish overexploitation to protect the amount of compensate for this limitation . Second, although there is evolutionary history on coral reefs. If we exclude MPAs that are overwhelming evidence that MPAs can maintain or increase not specifically designed to protect species and habitats and have 47,48 48 fish diversity, size and biomass , and strong evidence that the a reduced capacity to protect fish diversity and biomass , that is, presence of intact fish communities can enhance coral persistence if only IUCN categories I to IV are considered (Methods), the NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 5 9.64 12.84 16.05 19.25 22.45 25.65 28.85 32.05 35.25 38.46 41.66 4.52 6.86 9.21 11.55 13.9 16.24 18.59 20.93 23.28 25.62 0 27.97 1.01 2.03 3.04 4.06 5.07 6.09 7.1 8.12 9.13 5.31 10.14 5.71 6.12 6.53 6.94 7.35 7.75 8.16 8.57 8.98 9.39 Number of cells Number of cells Number of cells Number of cells ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 from 169 locations worldwide . From these distributional data we obtained a range map for each species, defined as the convex polygon shaping the area where each species is present . These were individually checked by expert to avoid the combination of disjointed ranges, for example, anti-tropical species. We focused on labrid fishes since they (i) represent an exceptionally rich and diverse reef associated family, (ii) live in shallow waters, (iii) benefit from MPAs 24 41 as a common fisheries target and (iv) have a well resolved phylogeny .To incorporate unsampled taxa, new tips were grafted onto a backbone phylogeny 60,61 based on other published phylogenies for the group , supplemented by species accounts from fish identification guides and FishBase (www.fishbase.org). Where information allowed, new tips representing unsampled species were added to direct sister species or to the base of the clade representing its genus. The full list of labrid fishes is provided as Supplementary Data 1. We selected 805 coral species for which global range maps were downloaded at http://www.iucnredlist.org/technical-documents/spatial-data#corals. We considered only hard corals in shallow habitats. We used the supertree method to reconstruct the phylogeny of the scleractinian clade, comprising a total of 842 reef and 705 non-reef species . The source trees were derived from a molecular 20 phylogeny of 474 species (based on seven mitochondrial DNA markers), 13 morphological trees and 1 taxonomic tree. These were combined via the SuperFine- boosted Matrix Representation with Parsimony and Matrix Representation with Likelihood . The full list of coral species is provided as Supplementary Data 2. We collected spatial information on MPAs from the WDPA (World Database on Protected Areas) database available at: http://protectedplanet.net/. The original database included 9,600 PAs covering a total surface of 17,633,881 km .We eliminated PAs on land, those that did not involve coastal habitat, defined as the portion of sea bottom from 0 to 200 m depth, and MPAs designated to protect species not considered in the present study (for example, birds). The latter were discarded after evaluating the description of the ‘Designation’ field in the original IUCN-WDPA database. MPAs for which IUCN criteria were either ‘not applicable’ or ‘unknown’ (for example, not communicated by the Authority), and are likely to Figure 5 | Representation in MPAs for branches of the Tree of Life on be unreliable, were also removed. The final database included 3,625 MPAs covering coral reefs across marine realms. (a) Global map representing the three a total surface of 942,568 km (IUCN categories I–VI). We also used another marine realms: Indo-Pacific (grey), Tropical Eastern Pacific (orange), and restricted data set where we eliminated MPAs that are not specifically designed to Atlantic (green). (b) Boxplots (median and quartiles) representing the protect species or habitats. We retained the 2,224 MPAs belonging to IUCN percentage of the longest evolutionary branches (top 10%) that receive less categories I to IV covering a total surface of 575,806 km with a relatively higher degree of protection. than the critical 10% coverage by the MPA system within coral and fish We then used a 5 5 grid cell corresponding to B550 550 km at the local assemblages (in 5 5 grid cells) of the three marine realms. equator to collate the presence of species, the area of tropical reef habitat, and the area of reef habitat protected within MPAs . proportion of the Tree of Life attaining the minimum target of 10% coverage by MPAs drops to 0.9% ( 0.2 s.d.) and 14.9% Analyses. Fossil records show that species extinction risk is primarily determined 65,66 ( 2.0 s.d.) for corals and fishes, respectively. by geographic range size in the marine realm with restricted ranged species being less buffered against demographic variability under changing environments. However, having at least ‘one foot’ in the MPA system does not ensure persistence . Conclusions We thus examined the proportion of the geographic range of species overlapping with the global MPA system. This represents a potential overlap since the presence of Phylogenetic diversity is one of the key components of 5,14 species within MPAs overlapping with their geographic range was not measured biodiversity . However, the existing global system of MPAs directly. We adopted a threshold of 10% spatial coverage by MPAs corresponding to does not meet the minimum levels considered necessary to 3,34 a minimum (and conservative) target for effective protection . This minimum adequately protect the Tree of Life for corals or fishes. If MPAs are threshold is based on the rational that some MPAs may be unsuitable for a given species, that protection is not effective in all MPAs and that the coarse grain of to protect the Tree of Life, we need to carefully consider their species distribution maps may induce commission errors by which species can be features and future placement. Geographic variation in absent from protected areas that overlap their geographical ranges . evolutionary history, and variable susceptibility to human We applied the same reasoning to the internal branches of phylogenetic trees. impacts differs among fish and corals. The most notable example The coverage by MPAs of the evolutionary history of a branch is therefore defined is in the Atlantic where there is a predominance of old coral as the relative coverage by MPAs of the combined geographic ranges of the species subtending this branch. To evaluate the effectiveness with which MPAs protect the lineages but a larger proportion of younger fish lineages. This overall Tree of Life we measured the amount of evolutionary history represented by mismatch brings to the fore the potential limitations of MPAs, and branches that pass the coverage threshold of 10%. the differing needs of fishes, corals and other taxa. For corals, many By grafting species we create polytomies on the phylogenetic trees that may bias of the major ongoing threats are not mitigated by MPAs. For the results since many species have artificially identical branch lengths. This may ultimately inflate the amount of evolutionary history supported by the tips and the effective protection we may need to look beyond traditional MPAs level of phylogenetic conservatism . To limit this bias and estimate the uncertainty and develop new strategies that can encompass the full range of of our results linked to the unresolved recent diversification events, polytomies threats to reef biodiversity. A broader approach could include the 69 70 were randomly resolved by a birth–death model using BEAST . Using 100 protection of herbivorous fishes that promote local recovery of ± resolved trees for both corals and fishes, we provided the mean value and s.d. ( ) for each result. corals , management to control terrestrial influences and water 56 57 We also tested whether the current global system of MPAs is effective given the quality and effective action to mitigate climate change .For topology of the phylogenetic tree and thus the evolutionary constraints that have future conservation efforts, we need to adequately secure greater shaped species geographic ranges across history. To do so we performed a null amounts of evolutionary history on coral reefs in the Atlantic, model analysis where species labels were shuffled across the tips of the two Eastern Pacific and in the Western Indian Ocean. phylogenies. By so doing the null model breaks the relationships between species ranges and their position on the phylogenetic tree while maintaining the amount of species coverage by MPAs. This procedure was applied 999 times for each of the Methods 100 resolved trees to obtain a null frequency distribution for the overall amount of Data. We restricted our database to shallow reef habitats (o50 m) showing a evolutionary history covered by MPAs. From this distribution, we extracted a minimum monthly sea surface temperature (hereafter SST) of at least 17 Cto P value for each resolved tree by assessing the positions of the observed in the null define tropical marine waters . We built the geographic distribution of 452 frequency distribution. 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NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 7 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 Author contributions 62. Swenson, M. S., Suri, R., Linder, C. R. & Warnow, T. SuperFine: fast and D.M., D.R.B., W.T. and F.G. conceived the project; all authors designed the study; V.P., accurate supertree estimation. Syst. Biol. 61, 214–227 (2012). F.L., D.H., P.F.C, C.A. and F.G. collected the data and performed the analyses; D.R.B, 63. Nguyen, N., Mirarab, S. & Warnow, T. MRL and SuperFine plus MRL: new F.L., T.P.H., C.A. and F.G. drew the figures, D.M. and F.G. wrote the first draft and all supertree methods. Algorithms Mol. Biol. 7, 3 (2012). authors contributed substantially to revisions. 64. Parravicini, V. et al. Global mismatch between species richness and vulnerability of reef fish assemblages. Ecol. Lett. 17, 1101–1110 (2014). 65. Harnik, P. G., Simpson, C. & Payne, J. L. Long-term differences in extinction risk among the seven forms of rarity. Proc. R. Soc. B Biol. Sci. 279, 4969–4976 (2012). Additional information 66. Payne, J. L. & Finnegan, S. The effect of geographic range on extinction Supplementary Information accompanies this paper at http://www.nature.com/ risk during background and mass extinction. Proc. Natl Acad. Sci. USA 104, naturecommunications 10506–10511 (2007). Competing financial interests: The authors declare no competing financial interests. 67. Boyd, C. et al. Spatial scale and the conservation of threatened species. Conserv. Lett. 1, 37–43 (2008). Reprints and permission information is available online at http://npg.nature.com/ 68. Davies, T. J., Kraft, N. J. B., Salamin, N. & Wolkovich, E. M. Incompletely reprintsandpermissions/ resolved phylogenetic trees inflate estimates of phylogenetic conservatism. Ecology 93, 242–247 (2012). How to cite this article: Mouillot, D. et al. Global marine protected areas do 69. Kuhn, T. S., Mooers, A. O. & Thomas, G. H. A simple polytomy resolver for not secure the evolutionary history of tropical corals and fishes. Nat. Commun. 7:10359 dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011). doi: 10.1038/ncomms10359 (2016). 70. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 This work is licensed under a Creative Commons Attribution 4.0 (2012). International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise Acknowledgements in the credit line; if the material is not included under the Creative Commons license, The FRB CESAB-GASPAR project is thanked for providing fish geographical data. D.H. users will need to obtain permission from the license holder to reproduce the material. is supported by NUS Start-up Grant R-154-000-671-133. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ 8 NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Nature Communications Springer Journals

Global marine protected areas do not secure the evolutionary history of tropical corals and fishes

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Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
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Abstract

ARTICLE Received 18 May 2015 | Accepted 3 Dec 2015 | Published 12 Jan 2016 DOI: 10.1038/ncomms10359 OPEN Global marine protected areas do not secure the evolutionary history of tropical corals and fishes 1,2 3 2 1 4 5 6 2 D. Mouillot , V. Parravicini , D.R. Bellwood , F. Leprieur , D. Huang , P.F. Cowman , C. Albouy , T.P. Hughes , 7,8 1 W. Thuiller & F. Guilhaumon Although coral reefs support the largest concentrations of marine biodiversity worldwide, the extent to which the global system of marine-protected areas (MPAs) represents individual species and the breadth of evolutionary history across the Tree of Life has never been quantified. Here we show that only 5.7% of scleractinian coral species and 21.7% of labrid fish species reach the minimum protection target of 10% of their geographic ranges within MPAs. We also estimate that the current global MPA system secures only 1.7% of the Tree of Life for corals, and 17.6% for fishes. Regionally, the Atlantic and Eastern Pacific show the greatest deficit of protection for corals while for fishes this deficit is located primarily in the Western Indian Ocean and in the Central Pacific. Our results call for a global coordinated expansion of current conservation efforts to fully secure the Tree of Life on coral reefs. 1 2 UMR 9190 MARBEC, IRD-CNRS-IFREMER-UM, Universite de Montpellier, Montpellier 34095, France. Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia. CRIOBE, USR 3278 CNRS-EPHE-UPVD, Labex ‘Corail’, University of Perpignan, Perpignan 66860, France. Department of Biological Sciences and Tropical Marine Science Institute, National University of Singapore, Singapore 117543, Singapore. Department of Ecology & Evolutionary Biology, Yale University, 21 Sachem St, New Haven, Connecticut 06511 USA. 6 7 De´partement de biologie, chimie et ge´ographie, Universite´ du Que´bec a` Rimouski, 300 Alle´e des Ursulines, Rimouski, Canada G5L 3A1. Laboratoire ´ ´ d’Ecologie Alpine (LECA), Univ. Grenoble Alpes, Grenoble F-38000, France. Laboratoire d’Ecologie Alpine (LECA), CNRS, Grenoble F-38000, France. Correspondence and requests for materials should be addressed to D.M. (email: david.mouillot@univ-montp2.fr). NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 uman activities are altering ecosystems worldwide, maintain the integrity of coral reefs, thousands of changing their biodiversity and composition, and marine-protected areas (MPAs) have been created worldwide . Himperilling their capacity to deliver ecosystem services . However, the spatial design of the global MPA system is largely In this context, protected areas are indisputably the flagship tool contingent on local socioeconomic conditions and history rather 27,28 for protecting both ecosystems and biodiversity by limiting than regional or global considerations . Furthermore, given 2 29 direct human impacts . Conservation strategies have traditionally the limited resources dedicated to conservation efforts and the 21,30 focused on vulnerable components of taxonomic diversity such need to maintain coastal fisheries for people’s livelihoods , 3,4 as endemic, rare or threatened species . However, phylogenetic MPAs cannot be extended to all coral reefs. Guiding future diversity, represented by the Tree of Life, is becoming an conservation strategies thus remains a key challenge, particularly 5,6 increasingly important component of conservation science at a global scale where deficits of protection must be identified since it represents the breadth of evolutionary history and addressed to achieve effective protection of evolutionary and supports biodiversity benefits and uses, often unanticipated, history on coral reefs. Here we assessed the extent to which the 8,9 for future generations . Phylogenetically related species tend global system of MPAs represents individual species and to have similar functional traits, environmental niches and phylogenetic diversity for two major components of coral 10,11 ecological interactions , although numerous counter examples reef ecosystems, shallow-water corals in the order Scleractinia 12,13 exist . Therefore, species that are more phylogenetically (805 species) and fishes in the family of Labridae (452 species). distinct may have greater functional complementarity. In These groups contribute to the high biodiversity of tropical seas 32,33 turn, species assemblages that are more phylogenetically and help maintaining productive and resilient reefs . We show diverse may promote greater biomass production within and that the current global MPA system, covering 5.9% of the world’s across trophic levels even though a universal relationship coral reef area, does not meet the minimum conservation targets between phylogenetic diversity and ecosystem functioning considered necessary to adequately secure the branches of the 9,16 remains questionable . Yet, few studies have quantitatively Tree of Life for corals or fishes, particularly the longest branches assessed the extent to which protected areas encompass that represent the greatest amount of evolutionary history. 17,18 phylogenetic diversity and none have focused on marine taxa at a global scale. Here, we tackle this critical issue for the iconic but threatened Results and Discussion coral reefs of the world that support one of the largest Lag behind minimum conservation targets. Using global concentrations of biodiversity, around 830,000 multi-cellular distribution maps of each scleractinian coral and labrid fish species , and provide vital ecosystem services to half a billion species (Methods), we reveal that only 5.7% of coral species and 20 21 people including food security , financial incomes and 21.7% of fish species meet a minimum protection target of 10% protection against natural hazards . There is overwhelming potential coverage of their geographic range by the global system evidence that human activities, particularly fishing pressure of MPAs (Fig. 1). Regionally, the situation is even more 23 24 and pollution, affect coral reef ecosystem state , functioning contrasted. For example, coral species that occur exclusively in and resilience . Thus, to counteract human impacts and the Tropical Eastern Pacific all fall below the critical 10% coverage a b Scleractinian corals Labrid fishes 0 0 0.8 0.8 Alantic endemics Alantic endemics Eastern-Pacific endemics Eastern-Pacific endemics All other species All other species 0.7 0.7 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 0 01 2 3 4 0 100 200 300 012 3 4 040 80 120 6 2 6 2 Geographic range (×10 km ) Number of species Geographic range (×10 km ) Number of species Figure 1 | Relationship between the total geographic range of species and the proportion of that range covered by the global system of MPAs. (a) Scleractinian coral species and (b) fish species of the family Labridae. Histograms on top and to the right represent the distributions of total ranges and proportion of protection among species respectively. Coloured squares and triangles represent endemic species, that is, only present in one of the two biogeographic realms: Atlantic and Eastern Pacific, respectively. Dotted lines represent the 10% threshold corresponding to the minimum representation target for sustaining species persistence. 2 NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications Number Proportion of range covered by MPAs of species Number Proportion of range covered by MPAs of species NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 ARTICLE ab MPAs Scleractinian corals Labrid fishes % of PD coverage % of PD 0.50 > 20% 10.2 >10% & <20% 1.15 7.4 98.3 < 10% 82.3 Figure 2 | Percentages of geographic ranges covered by the global system of MPAs for species and internal branches across the Tree of Life. (a) Scleractinian coral species and (b) fish species of the family Labridae. Species or branches in red do not meet the minimum 10% representation threshold, that is, o10% of their geographic range is covered by MPAs, while green and blue colours indicate 10–20% and more than 20% coverage respectively. The corresponding percentage of total phylogenetic diversity (PD) is indicated for each coverage category. threshold. Similarly, all coral and fish species found only in extinctions remain scarce, partly due to limited assessment , the Atlantic have o20% coverage (Fig. 1). This 10% threshold but the functionally most distinctive fish species on coral reefs has been specifically advocated for wide-ranging species tend to be rare either in their geographic extent or their local 2 37 (4250,000 km ) and is regarded as a conservative target of abundance . We may thus anticipate a disproportional local loss 3,34 coverage by protected areas for sustaining species persistence . of functional diversity within coral reef communities if the This conservative cut-off takes into account commission errors, longest evolutionary branches are under threat and inadequately that is, the potential absence of a given species from protected protected . For instance long-branched lineages include areas that lie within its geographic distribution due to chance or relatively specialized forms, such as the large invertivore unsuitable habitats . Lachnolaimus and the world’s largest excavating parrotfsh By applying the same reasoning to the internal branches of the Bolbometopon which are severely overexploited, suggesting that phylogenetic trees (Methods), we show that only 1.7% ( 0.2 s.d.) the loss of long branches may result in the loss of unique and of the Tree of Life of corals and 17.6% ( 0.6 s.d.) of fishes attain functionally important groups . the minimum 10% coverage (Fig. 2). Thus 7,160 Myr of the evolutionary history of corals and 3,586 Myr of fishes are inadequately represented by the global MPA system, far more Global distribution of protection deficits. To highlight the than for many other threatened taxonomic groups . Globally, the critical gaps in protecting the Tree of Life on coral reefs, we amount of evolutionary history potentially covered by MPAs, that mapped the locations where the longest evolutionary branches is, the proportion of the geographic range of evolutionary that receive o10% coverage are concentrated using a regular grid branches overlapping with the global MPA system, is only of 5 5 cells (Methods). For corals, the longest evolutionary ± ± 6.0% ( 0.1 s.d.) and 8.7% ( 0.2 s.d.) for corals and fishes, branches with low protection are predominantly in the Atlantic, respectively. Coral evolutionary history receives significantly less Eastern Pacific and, to a lesser extent, the North Indian coverage than expected under a random distribution of species Ocean (Fig. 3b). These deficits of protection are only marginally geographic ranges across the Tree of Life (Po0.001, n¼ 999, correlated with the heterogeneous MPA coverage at the global randomization test) while fishes receive significantly more scale (r¼ 0.045, n¼ 304 5 5 grid cells, P40.05, Fig. 3a). protection than expected by chance (Po0.001, n¼ 999, Instead, the high proportion of longest branches, and their unique randomization test) (Methods). The greatest amount of evolutionary history, in the Atlantic and Eastern Pacific primarily evolutionary history is supported by the longest branches on drives this pattern (Fig. 4a,b). For fishes, the highest the Tree of Life. In our case, the top 10% longest extant and concentrations of poorly protected long branches are located in internal branches, corresponding to 48.68 Myr ( 0.5 s.d.) for the Western Indian, Central Pacific and, to a lesser extent, the corals and 410.7 Myr ( 0.25 s.d.) for fishes, support a Eastern Atlantic (Fig. 3c). As in corals, these deficits of protection disproportional amount of evolutionary history, with 62% are not correlated with the heterogeneous distribution of MPA ± ± ( 0.9% s.d.) and 34% ( 0.5% s.d.) for corals and fishes, coverage (r¼ 0.025, n¼ 287 grid cells, P40.05, Fig. 3a). Instead, respectively. These longest branches are overwhelmingly the pattern is driven by the relatively high proportion of under-represented within the global MPA system (Fig. 2). long evolutionary branches of fishes at the periphery of the Only 1.3% ( 0.6% s.d.) of the longest branches in corals and Indo-Pacific (Fig. 4c,d). The correlation between the proportion 20.2% ( 2.3% s.d.) in fishes are adequately protected by the of poorly protected longest evolutionary branches for corals and minimum threshold of 10% geographic coverage by MPAs. If fishes within assemblages is negative (r¼ 0.15; n¼ 287 grid those poorly protected longest branches support endangered cells, P¼ 0.30) suggesting that there is a global spatial mismatch, species we may expect large and abrupt changes in ecosystem albeit weak, of conservation needs for these two taxa. The Atlantic functioning following extinctions. This situation already exists for and Eastern Pacific tend to concentrate many long and poorly the world’s primates, where the most endangered species are both protected branches for corals but substantially less for fishes evolutionarily and ecologically distinct . In the sea global (Fig. 5). This most likely reflects the biogeographic history of the NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 3 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 MPAs Percentage of cell area covered by MPAs 0 10 20 100 Scleractinian corals Percentage of longest branches poorly protected (<10%) within each cell 911 16 42 c Labrid fishes Percentage of longest branches poorly protected (<10%) within each cell 489 12 Figure 3 | Global distribution of protection deficits to secure the Tree of Life on coral reefs. Global maps representing, for each cell (5 5), the percentage of coral reef habitat covered by MPAs (a), and the proportion of the longest evolutionary branches (top 10%) that receive less than the critical 10% coverage by the MPA system within coral (b) and fish (c) local assemblages. Colours correspond to three categories of values based on percentage of coverage for MPAs and on tertiles for corals and fishes. tropical Atlantic which has been characterized by isolation, thus the slowest rate of MPA establishment worldwide although maintaining old coral lineages in contrast to the recent positive outliers in environmental governance also occur at both 42 28 diversification in younger fish lineages , especially along the national and local levels . For example, the Dominican Republic Brazilian coast where there is extensive evidence of recent has already reached the target of 10% coverage. Similarly an colonization . In the Atlantic, therefore, there is a logical priority increase in conservation investment has promoted MPA to emphasize the protection of older coral lineages. For fishes, the establishment in Eastern Africa . Other countries of Western Atlantic hosts younger labrid lineages than the Indo-Pacific Africa and Eastern America remain far below the 10% coverage particularly in the Caribbean following cryptic speciation and and should be priority areas to better protect the evolutionary in the North Eastern Atlantic with subsequent diversification history of corals. For fishes, conservation investment are of Mediterranean lineages following the Messinian Salinity Crisis primarily needed in the Western Indian Ocean where poorly at 6 Myr (ref. 44). By contrast, the Coral Triangle, at the centre of protected longest branches are concentrated. the Indo-Pacific region, harboured most of the coral reef refugia during the Quaternary glaciations, hence acting as a ‘museum’ for the older labrid lineages . Limitations and less conservative protection assessment. Globally, the proportion of poorly protected longest branches Overall, our results show that the Tree of Life on coral reefs is in corals ranges from 9 to 42% compared with 4 to 12% in fishes inadequately represented by the current global MPA system, with (Fig. 3b,c), suggesting that conservation efforts should initially be most evolutionary branches, particularly the longest ones, focused on the Atlantic to better preserve the coral Tree of Life receiving o10% protection. Despite the magnitude of this where it is most at risk. West African and, to a lesser extent, South shortfall, our estimates are highly conservative because they are American countries that border each side of the Atlantic, show based on the assumption that all MPAs are able to protect every 4 NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 ARTICLE Scleractinian corals Percentage of longest branches within each cell Scleractinian corals Mean branch length within each cell Labrid fishes Percentage of longest branches within each cell Labrid fishes Mean branch length within each cell Figure 4 | Global distribution of the amount of evolutionary history on coral reefs. Global maps representing, for each grid cell (5 5), the percentage of the longest evolutionary branches (top 10%) and the mean evolutionary branch length within coral (a,b) and fish (c,d) local assemblages, respectively. Colours correspond to classes of the histograms representing the distribution of values across the cells. 49–51 coral and fish species that geographically overlaps with them. and recovery , the extent of these benefits may vary among It thus assumes that coral and fish species are present in all MPAs. Not all MPAs are able to ensure that fish and coral MPAs within their geographic ranges, and that all MPAs are communities are protected, due to poor compliance and effective in their protection. These assumptions may not be valid. enforcement . Furthermore, MPAs cannot prevent pulses of First, we have no proof of individual species presence within coral mortality from cyclones or coral bleaching , or from MPAs. These commission errors are inevitable given the chronic declines in coral recruitment and growth due to degraded 54,55 coarse grain of species geographic distributions and the small size water quality . MPAs in the Atlantic should better focus on of most MPAs. We therefore assess maximum potential coral lineages while those in the Western Indian Ocean should protection while the conservation target of 10% is partly set to primarily limit fish overexploitation to protect the amount of compensate for this limitation . Second, although there is evolutionary history on coral reefs. If we exclude MPAs that are overwhelming evidence that MPAs can maintain or increase not specifically designed to protect species and habitats and have 47,48 48 fish diversity, size and biomass , and strong evidence that the a reduced capacity to protect fish diversity and biomass , that is, presence of intact fish communities can enhance coral persistence if only IUCN categories I to IV are considered (Methods), the NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 5 9.64 12.84 16.05 19.25 22.45 25.65 28.85 32.05 35.25 38.46 41.66 4.52 6.86 9.21 11.55 13.9 16.24 18.59 20.93 23.28 25.62 0 27.97 1.01 2.03 3.04 4.06 5.07 6.09 7.1 8.12 9.13 5.31 10.14 5.71 6.12 6.53 6.94 7.35 7.75 8.16 8.57 8.98 9.39 Number of cells Number of cells Number of cells Number of cells ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 from 169 locations worldwide . From these distributional data we obtained a range map for each species, defined as the convex polygon shaping the area where each species is present . These were individually checked by expert to avoid the combination of disjointed ranges, for example, anti-tropical species. We focused on labrid fishes since they (i) represent an exceptionally rich and diverse reef associated family, (ii) live in shallow waters, (iii) benefit from MPAs 24 41 as a common fisheries target and (iv) have a well resolved phylogeny .To incorporate unsampled taxa, new tips were grafted onto a backbone phylogeny 60,61 based on other published phylogenies for the group , supplemented by species accounts from fish identification guides and FishBase (www.fishbase.org). Where information allowed, new tips representing unsampled species were added to direct sister species or to the base of the clade representing its genus. The full list of labrid fishes is provided as Supplementary Data 1. We selected 805 coral species for which global range maps were downloaded at http://www.iucnredlist.org/technical-documents/spatial-data#corals. We considered only hard corals in shallow habitats. We used the supertree method to reconstruct the phylogeny of the scleractinian clade, comprising a total of 842 reef and 705 non-reef species . The source trees were derived from a molecular 20 phylogeny of 474 species (based on seven mitochondrial DNA markers), 13 morphological trees and 1 taxonomic tree. These were combined via the SuperFine- boosted Matrix Representation with Parsimony and Matrix Representation with Likelihood . The full list of coral species is provided as Supplementary Data 2. We collected spatial information on MPAs from the WDPA (World Database on Protected Areas) database available at: http://protectedplanet.net/. The original database included 9,600 PAs covering a total surface of 17,633,881 km .We eliminated PAs on land, those that did not involve coastal habitat, defined as the portion of sea bottom from 0 to 200 m depth, and MPAs designated to protect species not considered in the present study (for example, birds). The latter were discarded after evaluating the description of the ‘Designation’ field in the original IUCN-WDPA database. MPAs for which IUCN criteria were either ‘not applicable’ or ‘unknown’ (for example, not communicated by the Authority), and are likely to Figure 5 | Representation in MPAs for branches of the Tree of Life on be unreliable, were also removed. The final database included 3,625 MPAs covering coral reefs across marine realms. (a) Global map representing the three a total surface of 942,568 km (IUCN categories I–VI). We also used another marine realms: Indo-Pacific (grey), Tropical Eastern Pacific (orange), and restricted data set where we eliminated MPAs that are not specifically designed to Atlantic (green). (b) Boxplots (median and quartiles) representing the protect species or habitats. We retained the 2,224 MPAs belonging to IUCN percentage of the longest evolutionary branches (top 10%) that receive less categories I to IV covering a total surface of 575,806 km with a relatively higher degree of protection. than the critical 10% coverage by the MPA system within coral and fish We then used a 5 5 grid cell corresponding to B550 550 km at the local assemblages (in 5 5 grid cells) of the three marine realms. equator to collate the presence of species, the area of tropical reef habitat, and the area of reef habitat protected within MPAs . proportion of the Tree of Life attaining the minimum target of 10% coverage by MPAs drops to 0.9% ( 0.2 s.d.) and 14.9% Analyses. Fossil records show that species extinction risk is primarily determined 65,66 ( 2.0 s.d.) for corals and fishes, respectively. by geographic range size in the marine realm with restricted ranged species being less buffered against demographic variability under changing environments. However, having at least ‘one foot’ in the MPA system does not ensure persistence . Conclusions We thus examined the proportion of the geographic range of species overlapping with the global MPA system. This represents a potential overlap since the presence of Phylogenetic diversity is one of the key components of 5,14 species within MPAs overlapping with their geographic range was not measured biodiversity . However, the existing global system of MPAs directly. We adopted a threshold of 10% spatial coverage by MPAs corresponding to does not meet the minimum levels considered necessary to 3,34 a minimum (and conservative) target for effective protection . This minimum adequately protect the Tree of Life for corals or fishes. If MPAs are threshold is based on the rational that some MPAs may be unsuitable for a given species, that protection is not effective in all MPAs and that the coarse grain of to protect the Tree of Life, we need to carefully consider their species distribution maps may induce commission errors by which species can be features and future placement. Geographic variation in absent from protected areas that overlap their geographical ranges . evolutionary history, and variable susceptibility to human We applied the same reasoning to the internal branches of phylogenetic trees. impacts differs among fish and corals. The most notable example The coverage by MPAs of the evolutionary history of a branch is therefore defined is in the Atlantic where there is a predominance of old coral as the relative coverage by MPAs of the combined geographic ranges of the species subtending this branch. To evaluate the effectiveness with which MPAs protect the lineages but a larger proportion of younger fish lineages. This overall Tree of Life we measured the amount of evolutionary history represented by mismatch brings to the fore the potential limitations of MPAs, and branches that pass the coverage threshold of 10%. the differing needs of fishes, corals and other taxa. For corals, many By grafting species we create polytomies on the phylogenetic trees that may bias of the major ongoing threats are not mitigated by MPAs. For the results since many species have artificially identical branch lengths. This may ultimately inflate the amount of evolutionary history supported by the tips and the effective protection we may need to look beyond traditional MPAs level of phylogenetic conservatism . To limit this bias and estimate the uncertainty and develop new strategies that can encompass the full range of of our results linked to the unresolved recent diversification events, polytomies threats to reef biodiversity. A broader approach could include the 69 70 were randomly resolved by a birth–death model using BEAST . Using 100 protection of herbivorous fishes that promote local recovery of ± resolved trees for both corals and fishes, we provided the mean value and s.d. ( ) for each result. corals , management to control terrestrial influences and water 56 57 We also tested whether the current global system of MPAs is effective given the quality and effective action to mitigate climate change .For topology of the phylogenetic tree and thus the evolutionary constraints that have future conservation efforts, we need to adequately secure greater shaped species geographic ranges across history. To do so we performed a null amounts of evolutionary history on coral reefs in the Atlantic, model analysis where species labels were shuffled across the tips of the two Eastern Pacific and in the Western Indian Ocean. phylogenies. By so doing the null model breaks the relationships between species ranges and their position on the phylogenetic tree while maintaining the amount of species coverage by MPAs. This procedure was applied 999 times for each of the Methods 100 resolved trees to obtain a null frequency distribution for the overall amount of Data. We restricted our database to shallow reef habitats (o50 m) showing a evolutionary history covered by MPAs. From this distribution, we extracted a minimum monthly sea surface temperature (hereafter SST) of at least 17 Cto P value for each resolved tree by assessing the positions of the observed in the null define tropical marine waters . We built the geographic distribution of 452 frequency distribution. 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NATURE COMMUNICATIONS | 7:10359 | DOI: 10.1038/ncomms10359 | www.nature.com/naturecommunications 7 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10359 Author contributions 62. Swenson, M. S., Suri, R., Linder, C. R. & Warnow, T. SuperFine: fast and D.M., D.R.B., W.T. and F.G. conceived the project; all authors designed the study; V.P., accurate supertree estimation. Syst. Biol. 61, 214–227 (2012). F.L., D.H., P.F.C, C.A. and F.G. collected the data and performed the analyses; D.R.B, 63. Nguyen, N., Mirarab, S. & Warnow, T. MRL and SuperFine plus MRL: new F.L., T.P.H., C.A. and F.G. drew the figures, D.M. and F.G. wrote the first draft and all supertree methods. Algorithms Mol. Biol. 7, 3 (2012). authors contributed substantially to revisions. 64. Parravicini, V. et al. Global mismatch between species richness and vulnerability of reef fish assemblages. Ecol. Lett. 17, 1101–1110 (2014). 65. Harnik, P. G., Simpson, C. & Payne, J. L. Long-term differences in extinction risk among the seven forms of rarity. Proc. R. Soc. B Biol. Sci. 279, 4969–4976 (2012). Additional information 66. Payne, J. L. & Finnegan, S. The effect of geographic range on extinction Supplementary Information accompanies this paper at http://www.nature.com/ risk during background and mass extinction. Proc. Natl Acad. Sci. USA 104, naturecommunications 10506–10511 (2007). Competing financial interests: The authors declare no competing financial interests. 67. Boyd, C. et al. Spatial scale and the conservation of threatened species. Conserv. Lett. 1, 37–43 (2008). Reprints and permission information is available online at http://npg.nature.com/ 68. Davies, T. J., Kraft, N. J. B., Salamin, N. & Wolkovich, E. M. Incompletely reprintsandpermissions/ resolved phylogenetic trees inflate estimates of phylogenetic conservatism. Ecology 93, 242–247 (2012). How to cite this article: Mouillot, D. et al. Global marine protected areas do 69. Kuhn, T. S., Mooers, A. O. & Thomas, G. H. A simple polytomy resolver for not secure the evolutionary history of tropical corals and fishes. Nat. Commun. 7:10359 dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011). doi: 10.1038/ncomms10359 (2016). 70. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 This work is licensed under a Creative Commons Attribution 4.0 (2012). International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise Acknowledgements in the credit line; if the material is not included under the Creative Commons license, The FRB CESAB-GASPAR project is thanked for providing fish geographical data. D.H. users will need to obtain permission from the license holder to reproduce the material. is supported by NUS Start-up Grant R-154-000-671-133. 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