Quantifying dispersal from hydrothermal vent fields in the western Pacific Ocean

Satoshi Mitaraia,1, Hiromi Watanabeb, Yuichi Nakajimaa, Alexander F. Shchepetkinc, and James C. McWilliamsc,d

aMarine Biophysics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa, 904-0495, Japan; bDepartment of Marine Biodiversity Research and Research and Development Center for Submarine Resources, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Kanagawa, 237-0061, Japan; cInstitute of Geophysics and Planetary Physics, University of California, Los Angeles, CA 90095-1567; and dDepartment of Atmospheric and Oceanic Sciences, University of California, Los Angeles, CA 90095-1565

Edited by Christopher J. R. Garrett, University of Victoria, Victoria, Canada, and approved February 5, 2016 (received for review September 16, 2015) Hydrothermal vent fields in the western Pacific Ocean are mostly among vent populations in the western Pacific basins have not been distributed along spreading centers in submarine basins behind previously addressed. convergent plate boundaries. Larval dispersal resulting from deep- Detailed observations and models for eastern Pacific vents have ocean circulations is one of the major factors influencing gene flow, revealed mechanisms of near-bottom circulation strongly influenced diversity, and distributions of vent animals. By combining a bio- by distinct topographic features of midocean ridges (19–23). Con- physical model and deep-profiling float experiments, we quantify duit-like structures of midocean ridges may shield larvae from cross- potential larval dispersal of vent species via ocean circulation in the axial dispersal and also may enable long-distance dispersal that western Pacific Ocean. We demonstrate that vent fields within back- connects distant vent fields (20). Similar long-dispersal mechanisms, arc basins could be well connected without particular directionality, however, do not apply to species in the western Pacific, where whereas basin-to-basin dispersal is expected to occur infrequently, midocean ridges do not exist. If dispersal were limited to near- once in tens to hundreds of thousands of years, with clear dispersal bottom depths, vent species of the western Pacific would largely be barriers and directionality associated with ocean currents. The contained within a given back-arc basin. southwest Pacific vent complex, spanning more than 4,000 km, may Although most species likely remain near the bottom, some be connected by the South Equatorial Current for species with a strong-swimming larvae (e.g., shrimp and crabs) may disperse higher longer-than-average larval development time. Depending on larval in the water column, possibly ∼1,000 m above the bottom, where dispersal depth, a strong western boundary current, the Kuroshio they can be transported by faster currents (24, 25). Lagrangian Current, could bridge vent fields from the Okinawa Trough to the Izu- measurement methods, using deep-ocean profiling floats pro- Bonin Arc, which are 1,200 km apart. Outcomes of this study should grammed to drift at a specified depth or constant density surface, can help marine ecologists estimate gene flow among vent populations be used to measure dispersal in the water column. This approach has and design optimal marine conservation plans to protect one of the been used for hydrothermal vent surveys as well (26, 27). One ex- most unusual ecosystems on Earth. ample was the Lau Basin Float Experiment (27), which captured boundary currents within the back-arc basin and westward outflow hydrothermal vents | larval dispersal | deep-ocean circulation | from the basin resulting from the South Equatorial Current. For analytical approach various reasons, it is challenging to quantify vent-to-vent transport using only in situ experiments; therefore, one promising approach is ydrothermal vent fields in the western Pacific have received to combine dispersal experiments with ocean circulation models. Hsubstantially less attention than have eastern Pacific vents. Properly analyzed, such observation and modeling data should Western Pacific vents are mostly distributed along spreading yield reasonable estimates of dispersal processes by ocean circulation centers in submarine basins behind convergent plate boundaries, and should help marine ecologists understand biogeography and whereas those of the eastern Pacific occur mainly at midocean ridges. It is estimated that vent-endemic species in back-arc basins Significance were introduced along now-extinct midocean ridges that bridged the eastern and western Pacific Oceans ∼55 million years ago, with Submarine hot springs known as hydrothermal vents host unique a potential origin at the East Pacific Rise (1, 2). More recent ecosystems of endemic animals that do not depend on pho- tosynthesis. Quantifying larval dispersal processes is essential studies suggest the possibility that Indian Ocean ridge systems once to understanding gene flows and diversity distributions of vent connected Atlantic and Pacific vent fields (3). Spreading centers in – endemic species, as well as to protect vent communities from back-arc basins are active for typically 5 10 million years (4, 5). anthropological disturbances (e.g., deep-sea mining). In this Thus, life spans of back-arc spreading centers are significantly study, we assess the potential frequency of larval exchange longer than population lifetimes of vent animals observed in the between vent fields throughout the entire western Pacific via eastern Pacific (∼1 million years) (6). ocean circulation processes, so that population geneticists can Recent genetic studies have addressed the matter of genetic make quantitative comparisons. We show that western Pacific differentiation among vent populations (7–11). Genetic data imply vents in distant basins are potentially connected with strong that back-arc basin populations are well-mixed genetic pools (12, directionality. This article makes a valuable contribution to a 13). In contrast, vent populations in distant basins (∼3,000 km difficult and important area of deep ocean processes. apart) are genetically distinct, suggesting that occasional migrations may have occurred over the course of several hundred thousand Author contributions: S.M. and J.C.M. designed research; S.M., H.W., Y.N., and A.F.S. per- formed research; S.M., H.W., Y.N., A.F.S., and J.C.M. contributed new reagents/analytic tools; generations (14). There is one example of a widespread species S.M., H.W., Y.N., and A.F.S. analyzed data; and S.M. and J.C.M. wrote the paper. Bathymodiolus septemdierum ( complex) occurring in all western The authors declare no conflict of interest. Pacific back-arc basins (15). To interpret gene flows of vent species, This article is a PNAS Direct Submission. it is necessary to understand larval dispersal by ocean circulation, as Freely available online through the PNAS open access option. – well as tectonic history (16 18). However, quantitative data re- 1To whom correspondence should be addressed. Email: [email protected]. garding dispersal processes in the western Pacific are still woefully This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. inadequate, leaving many unanswered questions. Dispersal patterns 1073/pnas.1518395113/-/DCSupplemental.

2976–2981 | PNAS | March 15, 2016 | vol. 113 | no. 11 www.pnas.org/cgi/doi/10.1073/pnas.1518395113 Downloaded by guest on September 29, 2021 gene flow among vent populations in the western Pacific Ocean. We Temporal variability of flow is often measured with correlation assessed potential larval dispersal from hydrothermal vent fields in timescales, representing characteristic periods during which flow the western Pacific on varying spatial scales, from intra- to interbasin remains more or less consistent in speed and direction. Correla- vent communications, by integrating information from a deep-ocean tion timescales could be qualitatively inferred from float tracks profiling float experiment and predictions derived from an ocean during the first several months of this study (Fig. 1B). Float de- circulation model. ployments separated by ∼30 d or longer demonstrate different dispersal patterns, although some consecutive releases are similar. Results and Discussion In other words, the Eulerian correlation time is less than 1 mo. Dispersal in a Back-Arc Basin. As a base case, we focused on dispersal We calculated the Eulerian correlation time (e-folding time) from processes from a vent field in the Okinawa Trough. The Okinawa time series of model flow fields. The estimated correlation time is Trough is an active back-arc spreading basin behind the Ryukyu about 2 wk, which is longer than that of the ocean surface (several arc-trench system, where the Philippine Sea Plate subducts beneath days) (31), reflecting less energetic circulation. Current observa- the Eurasian Plate (Fig. 1). The current rifting started about tion data from northern East Pacific Rise (32) appear to have a 2 million years ago (28). Depths of vent fields in the Okinawa similar Eulerian correlation time. Trough registered in the InterRidge vents database (29) vary be- tween 560 and 1,850 m, with a mean depth of 1,100 m. Dispersal Probability. Because of the unpredictable nature of dis- To assess spatial and temporal scales of dispersal at Hatoma persal, a large number of cases (degrees of freedom) are necessary to have sufficient statistical power. In the model domain, nearly Knoll (1,520 m) in the southern Okinawa Trough, we deployed “ ” 10 deep-ocean profiling floats (OPTIMARE NEMO-Floats), 1 million simulated model floats were released from Hatoma Knoll. Similar to actual floats, model floats were passively trans- introduced semimonthly from spring to fall over the course of 2 y ported by the simulated current at a constant depth of 1,000 m. By (April 17, 2013–October 25, 2014). These floats were pre- spatially binning the model float distribution for a given advection programmed to maintain a depth of 1,000 m while being pas- time, it is possible to evaluate a probability density function of float sively transported by ocean currents. Floats continuously displacement (Lagrangian PDF), both descriptively and quantita- recorded data, and they surfaced every 30 d to transmit their tively (33). Comparisons of Lagrangian PDFs with movements of coordinates (and a vertical water profile) to the Iridium satellite. actual floats show reasonable qualitative agreement (Fig. 2A). The One unit failed to surface; another stopped surfacing after 2 mo. ocean circulation model quantifies dispersal from Hatoma Knoll All other floats continue to function. The descending and as- well, assuming a dispersal depth of 1,000 m. cending speeds of floats are adjusted to minimize drift caused by To quantify larval dispersal, among other things, we need a the surfacing process. Long-distance movements of the floats are reasonable assessment of planktonic larval duration (PLD). Larval mostly a result of deep ocean circulation, and float trajectories development of marine animals should be more protracted in deeper, Drift at allow us to understand dispersal from a single vent field ( colder water because of reduced metabolic rate. Water temperature the Sea Surface). declines rapidly with depth, but is rather consistent for the latitude of Deployed floats traced complicated spaghetti-like patterns interest at a constant depth. The ocean model shows 4.8 ± 0.4 °C at through the ocean, even 1,000 m below the sea surface, and sur- 1,000 m and 9.4 ± 1.0 °C at 500 m throughout the western Pacific prisingly, even within semiclosed back-arc basins (Fig. 1A). Even at vent fields. On average, larvae of vent barnacles, genus Neoverruca, this dispersal depth, float trajectories are characterized by com- widely encountered in western Pacific vent fields, require 99 d at 4 °C plicated time-dependent, chaotic, eddy-like motions having radii on (∼1,000 m) and 50 d at 10 °C (∼500 m) to reach the last larval life the scale of 10s of kilometers, similar to those of shallow-water stage (34). These data suggest that PLD is a function of the depth at floats (30). Most floats remained in the southern part of the Oki- which larval dispersal occurs; that is, the deeper the dispersal depth, nawa Trough, although one float traveled more than 500 km to the the longer the PLD. northern Okinawa Trough. Long-distance larval dispersal probably To express this temperature dependence of larval development, occurs intermittently. for the sake of simplicity, we used a unified model deduced from

A

B 2 2 3 3

3 3 SCIENCES 2 3 3 1 2 2 3 ENVIRONMENTAL 2 2 1 2 1 1 1 2 1 1 1 1 Fig. 1. Dispersal processes in the deep sea show 17 3 complex eddy motions, changing monthly or more Hatoma Knoll Amami Island often. (A) Trajectories of deep-sea profiling floats released from Hatoma Knoll (indicated with white arrows) in the Okinawa Trough, illustrating dis- persal originating at a vent field within a back-arc basin. Floats were deployed semimonthly in 2013 4 Okinawa Island 19 and 2014 on dates indicated at the bottom right 9 2 7 corner of the figure. Float tracks until March 2015 are shown here. These passively transported floats Taiwan 11 13 maintain their depth 1,000 m below the sea surface Miyako Island 10 and return to the surface every 30 d (circles). Posi- Releases in 2013 In 2014 tions of each float at the sea surface are connected April 17 April 28 Iriomote Island May 16 June 2 with cubic splines. The numbers show the cumula- June 15 July 17 tive sum of surfacing events, which indicate ap- July 17 October 25 proximate drift times in months. (B) Close-up view August 15 of the same trajectories for the first three surfacing events.

Mitarai et al. PNAS | March 15, 2016 | vol. 113 | no. 11 | 2977 Downloaded by guest on September 29, 2021 published experimental laboratory studies, mostly for shallow-water from Hatoma Knoll changes every 2 wk, there are 26 statistically vertebrates and invertebrates (35). Population-averaged PLD independent dispersal events (float releases) per year or 100 million (mean of species-specific values) is given as 83 d at 1,000 m and 43 d dispersal events in 3.8 million years. Hence, the numbers in Fig. 2B at 500 m (Methods). This represents the vent barnacle case described can be regarded as the expected number of times larvae would earlier reasonably well. be transported in 3.8 million years, close to a typical lifetime of a spreading center in the back-arc basins of the Western Pacific Potential Larval Dispersal in the Okinawa Trough. The Lagrangian (5–10 million years). PDF corresponding to a PLD of 83 d suggests that all vent fields In terms of frequency, connections from Hatoma Knoll to (deeper than 1,000 m) should be within reach of Hatoma Knoll neighboring Irabu Knoll could occur once every ∼400 y. Simi- (Fig. 2B) if dispersal trajectories maintain that initial depth. Po- larly, we can estimate potential larval dispersal from each of the tential larval transport from Hatoma Knoll to other vent fields can vent fields in the Okinawa Trough (Fig. 3B). By accounting for be deduced from the Lagrangian PDF by multiplying the PDF at a all possibilities, larval transport between Hatoma Knoll and all destination site by its representative area. Assuming a vent area other vent fields could occur every ∼80 y at 1,000 m depth. As more radius of 1 km, for instance, transport from Hatoma Knoll to the vent fields are continually being discovered, actual larval transport neighboring Irabu Knoll (∼100 km) at depth of 1,000 m is realized may be more frequent than estimated here. In September 2014, × 8,571 times in 100 million independent dispersal events. As another for example, a large tract of vent chimneys (1,500 m 300 m) was example, transport from Hatoma to the furthest point in the discovered between known vent fields in the Central and Southern Okinawa Trough, Iheya Ridge (∼400 km), is 567 in 100 million in- Okinawa Trough. dependent events. Assuming that the dispersal pattern or direction These timescale estimates depend on accurate assessment of independent dispersal events. Potential larval dispersal will be more frequent if the Eulerian correlation time is shorter than our estimates. Consideration of additional biological traits (e.g., A seasonal spawning) will reduce the estimated independent dis- persal events and resulting connectivity.

Potential Larval Dispersal from the Western Pacific Vents. Using this modeling framework, we assessed potential larval dispersal among all vent fields in the entire western Pacific Ocean. To assess basin-to-basin transport, we grouped vent fields into 12 geographically separated regions (Fig. 3). Although four of these regions (Izu-Bonin, Solomon, New Hebrides, and Kermadec) are -5 relatively young and have not fully developed back-arc basins, we x10 included them because of their potential as stepping stones to 2.5 connect distant basins. 2 To the best of our knowledge, quantitative information for onto- Hatoma Knoll (1520) 1.5 genetic vertical migration of vent animals is very scarce (36) and is 1 not available relative to larval developmental stages. We tested cases 0.5 – 0 with dispersal depths of 100 1,500 m below the sea surface. Only active, confirmed vent fields deeper than a given dispersal depth were includedintheanalysis.Asadefaultcase,weshowpotentiallarval B transport at a dispersal depth of 1,000 m for a mean PLD of 83 d. For the 1,000-m dispersal case, there are four potential basin-to- basin connections with distinctive directionality and four regions (Okinawa, Izu-Bonin, Solomon, and Kermadec) that are isolated A North Knoll, Iheya Ridge (1070) (Fig. 3 ). Unidirectional transport is predicted from South Mariana to North Mariana, from Woodlark to Manus, and from 567 Lau-Tonga to the North Fiji region. Only the North Fiji and New Izena Cauldron (1450) 755 Hebrides regions could be connected in both directions. Long dispersal connecting these distant basins could occur 32–747 -5 x10 times in 100 million independent dispersal events. In other Yonaguni Knoll (1385) Irabu Knoll (1850) ∼ 8571 out of 100M 2.5 words, these connections could be successful once every 5,000 3714 8600 2 to ∼12,000 y, assuming a 2-wk Eulerian correlation time. West- Hatoma Knoll (1520) 1.5 ward transport in the Southern Hemisphere should reflect the 1 deep South Equatorial Current system (27). 0.5 Close-up views of potential larval dispersal in the Okinawa 0 Trough, Manus Basin, and Lau Basin (Fig. 3 B–D) show that vent fields could be well connected within back-arc basins with- Fig. 2. The ocean circulation model effectively quantifies potential larval dis- out particular directionality. Within each of these back-arc ba- persal from Hatoma Knoll. (A) Distributions of deep-profiling floats (cross sins, one vent field could be connected with many others, and markers) from Hatoma Knoll (white arrow) after 90 d of drifting 1,000 m below larval dispersal would be mostly bidirectional, unlike long-dis- the sea surface show good agreement with predictions by the ocean circulation tance basin-to-basin transport. model (color contour). Colors indicate probability densities of float displace- ment per unit area (square kilometers). (B) Transport from Hatoma Knoll to Other Combinations of Dispersal Depths and PLD. Transport patterns other vent fields at a dispersal depth of 1,000 m (lines and numbers) deduced were similar at dispersal depths of 100–1,500 m for mean PLDs, from the model. Five representative vent fields are shown. Numbers in brackets indicate the depth of each vent field. Drift time was set to the population mean except for the northwest Pacific, where the strong Kuroshio Cur- for the mean temperature at a depth of 1,000 m (83 d). Numbers indicate the rent enables long-distance connections for shallower dispersal number of expected connections out of 100 million independent events. The depths (within the upper ∼600 m). Vent fields in the Okinawa number beside Hatoma Knoll represents likelihood of self-recruitment. Trough and the Izu-Bonin Arc (∼1,200 km apart) can be bridged

2978 | www.pnas.org/cgi/doi/10.1073/pnas.1518395113 Mitarai et al. Downloaded by guest on September 29, 2021 A Izu-Bonin B 1366 479 567 274 21010 Okinawa Northern Mariana 131 6281

4335 Okinawa Southern Mariana 0 C D 100 454 75 1057 378 1467 91 1022 35 747 142

Manus 480

Northward 133 Manus 92 172 Westward Eastward Lau

Southward Woodlark

Solomon North Fiji E Lau-Tonga

Woodlark Solomon North Fiji

New Hebrides 19-36

New Hebrides

Kermadec Longer PLD (170 days)

Fig. 3. Vent fields within back-arc basins could be well connected, whereas basin-to-basin transport shows dispersal barriers and directionality. (A) Potential larval dispersal from western Pacific vent fields quantified from the biophysical model (lines and numbers). Dispersal depth is assumed to be 1,000 m. PLD is set to 83 d. White ovals show 11 geographically separated regions defined in this study. Line colors show the direction of connections (see the circular diagram in the figure). For an explanation of the numbers, refer to the Fig. 2 legend. Close-up views of the (B) Okinawa Trough, (C) Manus Basin, and (D) Lau Basin suggest that back-arc basins should form well-mixed pools without directionality. (E) The gap between North Fiji and Woodlark could be bridged with above- average PLD (∼twice the mean). When there were multiple vent fields within a 30-km radius, only one of them was randomly selected so as to avoid graphical complications. See Movie S1 for dispersal patterns from all selected vent fields.

by the Kuroshio Current (Fig. S1). Also, communication is estab- vent fields in the southwest Pacific complex may be connected for lished between Izu-Bonin and Northern Mariana, which is associ- long dispersers with PLDs of two or more times the mean (Fig. E ated with meandering of the Kuroshio Current (Fig. S1). 3 ). This extended connection would be relatively infrequent, SCIENCES

There are two counteracting effects as a function of dispersal occurring once every hundreds of thousands of years. ENVIRONMENTAL depth. As dispersal depth becomes shallower, current speed Nonetheless, there remain clear gaps even with longer PLDs. increases, which should extend larval dispersal distance, but at the The Okinawa Trough is almost completely sealed if dispersal same time, PLD diminishes, which limits dispersal distance. Our depth is deeper than 600 m. Gaps between vents in the southwest model suggests these two counteracting effects should nearly cancel and northwest Hemispheres may be too large to be spanned by each other, resulting in similar transport patterns regardless of dis- realistic PLDs. It has been reported that larvae of cold-seep persal depth, except for regions affected by the Kuroshio Current. mussels, Bathymodiolus childressi, may disperse at depths as Ontogenetic vertical migration of vent larvae may substantially alter shallow as 100 m for more than a year (37). This is rather an dispersal distance in the northwest Pacific, but less in other regions. extreme combination of PLD and dispersal depth compared with The cases presented here assume population mean PLDs. population mean PLDs of shallower species (12 d). Our model Larval dispersal from one basin to neighboring regions may be suggests that even with a PLD of 1 y at 100 m, the Mariana achieved even with below-average PLDs. For a dispersal depth of Trough and Manus Basin should not be directly connected, be- 500 m, transport from the Okinawa to the Izu-Bonin region could cause the Equatorial Countercurrent inhibits transport across be established for a PLD of 20 d or longer. Species with above- the Equator at a dispersal depth of 100 m. Ocean circulation average PLDs will disperse longer distances and may reach more processes imply that there should be other means that enable the distant vent fields. Gaps between the New Hebrides and Wood- connection across the Equator (e.g., undiscovered vents, whale lark regions could be bridged by the South Equatorial Current. All carcasses, and cold seeps as stepping stones).

Mitarai et al. PNAS | March 15, 2016 | vol. 113 | no. 11 | 2979 Downloaded by guest on September 29, 2021 Comparisons with Population Genetic Data. A recent population ge- anthropological disturbances, it will be necessary to un- netic study, using mitochondrial DNA and microsatellite markers, derstand connectivity on intraregional scales in greater detail revealed that populations of the vent-restricted gastropod, Ifremeria (40). Information from this study will also be valuable in nautilei, in the Manus Basin were genetically distinct from those of environmental assessment; for example, to identify potential the North Fiji and Lau Basins (14). Estimates of gene flow also im- deep-ocean mining sites with minimal (or maximal) risk to plied migration from the Lau to North Fiji Basin with a splitting time vent communities. Near-bottom circulation processes in back- of tens of thousands of generations and genetic isolation between arc basins may be less important than those of midocean those two Basins and the Manus Basin for several hundred thousand ridges, because of the lack of conduit-like topographic fea- generations. Our biophysical model, in contrast, predicts that unidi- tures. However, accurate predictions of bottom boundary rectional larval transport from the Lau to North Fiji vent fields should layers will be of importance for assessment of self-recruitment. occur only once in tens of thousands of years. Our model also sug- Quantitative data describing deep-ocean dispersal processes gests that using the New Hebrides and Solomon arcs as stepping are limited. One might think that existing Argo float data (41) stones, the connection can be further extended all of the way to the could fill this void. However, a majority of Argo floats used Argos west end of the Manus Basin once in hundreds of thousands of years satellite communications, which necessitate long drift times on for species with longer PLDs (Fig. 3E). These genetic estimates agree the sea surface during data uploads. Cycle times of Argo floats with our flow-based assessment, assuming that the generation time of (essentially the time spent in deep water) are mostly 10 d or less, Ifremeria is on the order of a year. Thus, the rather weak gene flow which is much shorter than the 30-d cycle time used in our ex- from Lau to North Fiji and the genetic barrier between Manus and periments. Time-series based on Argo float surfacing points do NorthFijicanbeexplainedbytheoceancirculation. not accurately represent deep ocean circulation because they are Population genetics of Neoverruca barnacles, based on the heavily influenced by strong surface currents. Among existing mitochondrial cytochrome c oxidase subunit I gene, show no Argo floats in the Pacific Ocean, we found only two units that significant genetic differentiation among populations within could be used to examine dispersal patterns emanating from the Okinawa Trough (12). Furthermore, haplotype analyses western Pacific vent fields (one from the 13 N Ridge Site and the Neoverruca of the barnacles imply that populations inhabiting other from the Alice Springs Field). More observation data are the Izu-Bonin region originated in the Okinawa Trough, al- required to fully examine the dispersal estimates from this study. though these two populations are genetically distinct (12). Our model predicts that within the Okinawa Trough, a vent field can Methods be interconnected with other vent fields on average once every The model domains covered all active western Pacific vent fields between ∼80 y at a dispersal depth of 1,000 m. Given that more vent fields 32°N and 36°S registered in the InterRidge vents database (29). The latest are being discovered, actual larval exchange should be even more version of the 3D hydrodynamic model Regional Ocean Modeling System is frequent, which may result in well-mixed genetic pools. Transport used to integrate the rotating primitive equations with a realistic equation from the Okinawa Trough to the Izu-Bonin Arc is predicted to be of state (42, 43). There are two domains with a 5-km mesh resolution: one less frequent, once every tens of thousands of years, which appar- covering the northwest Pacific Ocean (43°N–15°S) and the other including ently is not frequent enough to prevent genetic differentiation. the southwest Pacific Ocean (40°S–10°N) with substantial overlap around the equatorial Manus Basin. Two semiclosed basins, the Okinawa Trough and Dispersal Patterns in the Past. The dispersal assessment of this study the Manus Basin, are discretized with a finer 1-km mesh, including eight was based on present-day oceanographic information. Estimates tidal constituents. The model domains and time-lapse movies of ocean cir- culation processes are provided in Detailed Model Configuration and Movie are not necessarily applicable to the past, when currently active S2 and S3. More than 1 million (1,098,000) simulated model floats were basins started spreading. The present global, thermohaline oceanic released from each of the vent fields in the model and randomly distributed circulation commenced ∼38 million years ago, when substantial (uniform distribution) within 5-km radii of registered vent locations: 250 Antarctic sea ice began to form (38). The earth has experienced floats every 3 h from April 1 through September 30 of 2011–2014. glacial and interglacial periods since then. During glacial periods, 10 OPTIMARE NEMO-Floats, developed on the basis of the SOLO-Float for warm, thermohaline return flow may have weakened, and mon- the Argo program (41, 44), were deployed above Hatoma Knoll (123.8410°N, soon circulation could have been intensified in winter, but overall 24.8550°E). Parking depth was set to 1,000 m. The mean descending (as- ocean circulation patterns were likely similar to the present pattern cending) speed of the floats was set to a relatively fast 50 cm/s (18 cm/s) to (39). We believe that quantified dispersal patterns and scaling minimize drift occurring during descent/ascent. Floats spend ∼15 min on the ∼ analyses of this study are reasonable and applicable to the past sea surface for satellite communications and 125 min ascending and 5–10 million years. However, there may have been prehistoric descending. Cycle times of floats are set to 30 d. Our estimates indicate that cycle times should be 30 d or longer so that surface drifting distances <5% of larval transport among some presently disconnected vent fields. total travel distance (Drift at the Sea Surface). Paleo-oceanographic information will be important to accurately We use a unified model proposed by O’Connor et al. (35) to account for the estimate gene flow among contemporary vent species. temperature dependence of larval development in marine animals. Deduced from 69 species, PLD is represented as a function of water temperature by ln 2 Future Studies. Information about biological traits (e.g., larval de- (PLD) = B0 − 1.34 × ln (T/Tc) − 0.28 × [ln (T/Tc)] ,whereT is ocean temperature and velopment, ontogenetic vertical migration, and settling behaviors) B0 is the value of ln (PLD) at Tc = 15 °C. To describe a generic case of larval is essential to accurately predict larval dispersal range (distance), dispersal processes, we use B0 = 3.17, which describes the population mean PLD = combined with knowledge of ocean circulation processes above vent as a default case (35), and B0 10.0 for a longer PLD case (twice the mean). We fields. Although life histories and demographic structures for most assumed that metabolic rates of vent animals are relatively insensitive to hy- vent animals are largely unknown, recent advances in larval culturing drostatic pressure (45). and in situ time-series observations have provided useful insights into ACKNOWLEDGMENTS. Comments from and discussions with Dennis larval dispersal processes (36). Species-specific dispersal predictions McGillicuddy, Lauren Mullineaux, Tadashi Maruyama, Yasuo Furushima, should be able to made, given quantitative biological information. Yoshihiro Fujiwara, Masako Nakamura, and Mary Grossmann were help- Further study based on network analysis would be useful in ful in focusing this contribution. We thank Shohei Nakada and the 11th identifying key sites for effective conservation. Optimal designs for Regional Coast Guard Headquarters, Naha, Okinawa, for aiding in many aspects of this work. We thank Steve Aird for his careful editing. This work marine protected areas will require consideration of appropriate was supported by a Canon Foundation Grant (2011–2014) and internal spatial and temporal scales. To assess resilience of vent commu- funding from the Okinawa Institute of Science and Technology nities and to facilitate their recoveries from natural and Graduate University.

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