Marine Environm ental Research 102 (2014) 59e 72

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Marine Environm ental Research

j o u r n al h o m ep ag e: w w w .el sev i er .co m /l o cat e/m ar en v r ev

Im pacts of anthropogenic disturbances at deep-sea hydrotherm al vent ecosystem s: A review

Cindy Lee Van Dover*

Marine Laboratory, Nicholas School of the Environment, Duke University, 135 Marine Lab Rd, Beaufort, NC 28516, USA a r t i c l e i n f o a b s t r a c t

Article history: Deep-sea hydrotherm al-vent ecosystem s have stim ulated decades of scientific research and hold Received 20 Septem ber 2013 prom ise of m ineral and genetic resources that also serve societal needs. Som e endem ic taxa thrive only Received in revised form in vent environm ents, and vent-associated organism s are adapted to a variety of natural disturbances, 25 February 2014 from tidal variations to earthquakes and volcanic eruptions. In this paper, physicochem ical and biological Accepted 11 March 2014 im pacts of a range of hum an activities at vents are considered. Mining is currently the only anthropo- Available online 20 March 2014 genic activity projected to have a m ajor im pact on vent ecosystem s, albeit at a local scale, based on our current understanding of ecological responses to disturbance. Natural recovery from a single m ining Keywords: Scientific research event depends on im m igration and larval recruitm ent and colonization; understanding processes and Mitigation dynam ics influencing life-history stages m ay be a key to effective m inim ization and m itigation of m ining Deep-sea m ining im pacts. Cum ulative im pacts on benthic com m unities of several m ining projects in a single region, Cum ulative im pacts w ithout proper m anagem ent, include possible species extinctions and shifts in com m unity structure and Resilience function. Com m ercial activities Ó 2014 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND Larval dynam ics license (http://creativecom m ons.org/licenses/by-nc-nd/3.0/). Colonization processes

1. In trodu ction (basalt) associated w ith new ocean crust along seafloor spreading centers, though there are sites w here active vents on spreading Since the discovery of hydrotherm al vents in the late 1970s, centers are sedim ent-hosted (e.g., Guaym as Basin in the Gulf of scientific research has been the prim ary source of anthropogenic California, Gorda Ridge in the northeast Pacific; Van Dover, 2000). disturbance in these ecosystem s (Glow ka, 2003), but there is Vents are also associated w ith seam ount volcanic systems (e.g., increasing interest in com m ercial exploitation of seafloor m assive Loihi Seam ount, Karl et al., 1988; seam ounts of the Kerm adec sulfides that host vent com m unities (Hannington et al., 2011; Hein Ridge; Clark and O’Shea, 2001). et al., 2013; Hoagland et al., 2010; Rona, 2008). Im pacts of The spatial extent of any given vent field depends on the anthropogenic disturbances at deep-sea vents are considered here geological setting, but they tend to be at m ost a hundred m eters or in the context of natural disturbance regim es and in m ore detail so in m axim um dim ension and separated from one another by 50e than has been provided elsew here (e.g., Baker et al., 2010; Halfar 100 km (e.g., the TAG m ound on the slow-spreading Mid-Atlantic and Fujita, 2007; Ram irez-Llodra et al., 2010, 2011; Van Dover, Ridge) at one extrem e or, at the other extrem e, to be m uch sm aller 2011a; Boschen et al., 2013). features (on the order of 10e 50 m m axim um dim ension) arrayed linearly in clusters and spaced at intervals ranging from a few ki- lom eters to 10s of kilom eters on the axis of fast spreading centers 2. Gen eral ch aracteristics of deep-sea ven t ecosystem s (e.g., the 9N vent field on the East Pacific Rise). While hydrotherm al fluids exiting the seafloor from black Hydrotherm al-vent ecosystem s are localized areas of the seabed sm oker chim neys reach tem peratures from 330 C to 400 C, w here heated and chem ically m odified seawater exits the seafloor m ixing of vent fluids w ith cold seawaterd either in subsurface as diffuse or focused flow and w here m icrobial chem oautotrophs rocks or through walls of black sm oker chim neysd results in are at the base of the food w eb (Van Dover, 2000). Most vent habitable zones of diffuse flow w ith tem peratures ranging from just ecosystem s tend to be linearly distributed on hard substrata above am bient (w 2 C) to w 50 C (Girguis and Lee, 2006). Fluid chem istry is generally correlated w ith tem perature at hydrother- * Tel.: þ 1 252 504 7655. m al vents, w ith higher tem peratures associated w ith a greater E-mail address: [email protected]. proportion of typically sulfide- and m etal-rich and oxygen- http://dx.doi.org/10.1016/j.m arenvres.2014.03.008 0141-1136/Ó 2014 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecom m ons.org/licenses/by-nc-nd/3.0/). 60 C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 depleted vent fluids (Johnson et al., 1988; Zielinski et al., 2011). The 3. Natu ral distu rban ce in deep-sea hydroth erm al ven t specific nature of these relationships can vary from one site to ecosystem s another (Beinart et al., 2012; Podowski et al., 2010). Vent ecosystem s are typically dom inated by benthic inver- Natural physico-chemical disturbances at hydrotherm al vents tebrate taxa (e.g., vestim entiferan tubew orm s, bathym odiolin range in severity from periodic tidal fluctuations in fluid flow and m ussels, vesicomyid clam s, provannid snails, rim icarid shrim p, plum e fall-out that have negligible im pact on the ecosystem , to yeti crabs) that host sym biotic, chem oautotrophic m icroorgan- chronic disturbance regim es associated w ith m ineralization and ism s. These sym bionts require a source of electron donors (e.g., clogging of conduits, to system atic disturbances associated w ith the sulfide in vent fluid), a source of electron acceptors (e.g., O2 in hydrotherm al cycle. Unpredictable and catastrophic disturbance seawater), and a source of inorganic carbon (e.g., CO2 or CH4 in regim es result from collapse of structures either through inherent vent fluids, CO2 in seawater). These so-called ‘holobiont’(host- instability of m ineralized structures or as a result of tectonic ac- sym biont) taxa often exhibit unusual m orphological, physio- tivity and infrequent catastrophic volcanism that paves over vent logical, and biochem ical adaptations to characteristics of vent fields and result in local extinctions (Fig. 1). environm ents, including loss of the digestive system in vesti- Deep-sea vents have been understood to be ephem eral habitat m entiferan tubew orm s, novel photoreceptors in sw arm ing islands from the m om ent of their discovery (Macdonald et al., shrim p on black sm oker chim neys, and sulfide-binding proteins 1980). Vent-restricted taxa are characterized by rapid grow th in vesicomyid clam s (Van Dover, 2000). Holobiont taxa are also rates, early m aturation, large reproductive output, and w ell- often foundation species, creating com plex 3-dim ensional developed dispersal capabilities (Grassle, 1986), characteristics habitat (e.g., w orm aggregations, bivalve beds, snail aggrega- shared by opportunistic m arine invertebrate species that persist tions) that serves as substratum for m icrobial grow th and as despite frequent local extinctions and divergent from those of refugia for juvenile invertebrates and habitat for associated or- deep-sea species in low-disturbance regim es (Grassle and Sanders, ganism s, including prim ary consum ers (e.g., lim pet grazers on 1973). The docum ented im pact of natural disturbances on vent m icrobial biofilm s) and secondary and tertiary consum ers (e.g., ecosystem s is review ed here, to provide context for understanding scavenging and predatory crustaceans and fishes). im pacts of hum an activities at deep-sea vents. Levels of im pacts are Zonation at vents can be rem iniscent of intertidal zonation, w ith assessed based on both the am ount of change to vent ecosystem s holobiont taxa typically dom inating the biom ass of habitable and the duration of change (Table 1). diffuse flow regions and w ith abrupt transitions from one species to another that relate to differing tolerances am ong species for ther- 3.1. Tidal fluctuations and plume fall-out m al and chem ical regimes and to biotic interactions (facilitation, com petition, predation). Total biom ass of benthic organism s is Diffuse vents exhibit continuous m icroscale tem perature and typically very high at vents; beyond the periphery of a vent field, chem ical fluctuations due to turbulent m ixing, and larger scale living biom ass is relatively inconspicuous, punctuated occasionally fluctuations (several degrees Celsius, several orders of m agnitude by solitary large anem ones, gorgonian corals, or other m egafaunal in sulfide concentration) related to tidally induced changes in organism s. bottom flow (Tivey et al., 2002) and tidal pum ping (Luther et al., Diversity (species richness) at deep-sea hydrotherm al vents is 2008; Scheirer et al., 2006). The alvinellid polychaete Paralvinella relatively low, on a par w ith that observed in tem perate and boreal sulfincola and other m obile invertebrate types m ay adjust their rocky intertidal system s (Van Dover and Trask, 2000), w ith nu- position in response to these fluctuations to m aintain an optim al m erical dom inance (thousands of individuals per m 3) by a sm all position (Robert et al., 2012). Tidal excursions of 10 C or m ore are num ber of species (< 10) and w ith a large percentage (25%) of rare com m only tolerated by sessile or attached vent taxa (e.g., the taxa (occurring as singletons or doubletons) in suites of replicate m ussel Bathymodiolus puteoserpentis; Zielinski et al., 2011). While quantitative sam ples (Van Dover, 2002). Cryptic taxa (m orpholog- tidal periodicities in shallow water are linked to a variety of peri- ically sim ilar, genetically distinct) and phenotypic plasticity odicities in physiological processes of shallow-water invertebrates, (genetically sim ilar, m orphologically distinct) are com m only including reproductive activities, this kind of linkage has so far not observed. Species com position is often differentiated by habitat been docum ented for vent invertebrates. What seem s clear is that w ithin a geographic region (e.g., species-abundance m atrices of m any invertebrate species at vents are naturally exposed to and m ussel beds are different from those of tubew orm aggregations) tolerate variable fluid chem istry and tem perature regim es. What is and varies substantively across ocean basins, w ith up to 11 usually not clear for m ost taxa is the optim al set of conditions that biogeographic provinces recognized to date (Moalic et al., 2012; m axim ize grow th and reproductive output. Rogers et al., 2012; Van Dover et al., 2002). Iron- and m anganese-rich particulate plum es generated by Grow th rates of holobiont taxa at vents are am ong the fastest black sm okers typically rise 100 m or m ore vertically and disperse reported for m arine invertebrates (Lutz et al., 1994; Shank et al., horizontally; m ost (99%) sedim entation of particulate iron and 1998). Reproductive m aturation is early and gam etogenesis in m anganese m ay occur away from the vent field (e.g., Feely et al., vent taxa is generally continuous, w ithout a strong seasonal signal 1994) and have little im pact on benthic ecosystems through pro- and little if any evidence for gam etogenic synchrony in m any vent cesses such as burial or clogging of feeding system s. Volcanoclastic taxa analyzed (Tyler and Young, 1999). Surprisingly, there is good fragm ents are also produced at spreading centers during deep-sea anecdotal evidence of cohort phenom ena occurring in at least som e volcanic eruptions (Barreyre et al., 2011). To date, evidence for vent taxa (e.g., vestim entiferan tubew orm s, rim icarid shrim p), im pacts of hydrotherm al or volcanic plum e fallout on hydrotherm al w here enorm ous num bers of juveniles have been observed in a vent organism s is scarce in the prim ary literature. given location (Short and Metaxas, 2010). Fertilization strategies of vent invertebrates are diverse, ranging from sperm transfer, stor- 3.2. Mineralization and conduit dynamics age, and internal fertilization [e.g., in scaleworm (polynoid) poly- chaetes] to broadcast spaw ning (e.g., bathym odiolin m ussels), w ith Tim e-series studies of sulfide structures at vents sites on the nearly all taxa undergoing a dispersive larval phase w ith either Juan de Fuca Ridge, Mid-Atlantic Ridge, and elsew here em phasize lecithotrophic or plankotrophic developm ent (Adam s et al., 2011; the role that m ineralization and clogging of conduits play in Tyler and Young, 1999). destroying and creating habitat. Cuvelier et al. (2011) describe the C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 61

Fig. 1. Natural and anthropogenic disturbance at hydrotherm al vents. Levels of disturbance are defined in Table 1. Natural disturbance occurs on a continuum of frequency and intensity of im pact on vent biota. ‘?’indicates uncertainty associated w ith the classification of im pact.

variability of hydrotherm al activity on the Eiffel Tower edifice w here clogging of the conduit becom es com plete, the tubew orm s, (Lucky Strike field, Mid-Atlantic Ridge) over a 14-year period and lim pets, and other colonists are replaced by scavengers and detri- note the decline of hydrotherm al activity at the sum m it and tivores. Because new chim lets open as other chim lets clog, a large increased activity peripherally, w ith som e corresponding reorga- sulfide edifice becom es a patchwork m osaic of assem blages rep- nization of m ussel beds but w ith overall constancy in their areal resenting different phases of the colonization cycle. coverage. In the above exam ples of very localized and abrupt natural A sim ilar pattern of diversion of hydrotherm al activity to the disturbance caused by changes in the location of fluid flow, the periphery of sulfide m ounds and central clogging has also been suite of biological responses include m igration, facilitation, suc- reported for northeast Pacific vent sites (Sarrazin et al., 1997). In cession, recruitm ent, and trophic interactions. These disturbances this Pacific setting, com m unity structure is m ore dynam ic than it is do not typically result in local extinction, but com m unity history at the Eiffel Tower structure, w ith distinct faunal assem blages that and legacy effects can influence succession characteristics occur during colonization of new ‘chim lets’ that form on large (Mullineaux et al., 2009). Biological responses to this scale of sulfide structures (Sarrazin et al., 2002): As early colonization of a disturbance take place over periods of days to m onths and can chim let takes place by a pioneer alvinellid polychaete species, the prom ote locally enhanced species diversity as a consequence of tubes of the polychaete allow a m arcasite crust to m ineralize un- m osaics of m icrohabitats in different phases of faunal succession at derneath, w hich in turn m odulates the therm o-chem ical m ilieu vents. Decadal-scale invariance in dom inance, general distribution, and allows a second, less tolerant species of alvinellid polychaete to and abundance of species at the TAG m ound (Copley et al., 2007) colonize the site. As fluid flow decreases further, other taxa m ove and the Eiffel Tower edifice (Cuvelier et al., 2011) on the Mid- in, including lim pets and tubew orm s. In the senescent phase, Atlantic Ridge rem ind us that processes occurring in one system m ay differ in others.

Table 1 Levels of potential im pacts to hydrotherm al vent ecosystem s. Modified from Cardno 3.3. Tectonic activity TEC Inc., 2013).

Im pact level Definition Vent fields occur on tectonically active regions of the seafloor, and tectonic activity can result in perturbation of fluid flow at vents Negligible No m easureable im pact Minor Detectable change that is sm all, localized, through collapse of black sm oker chim neys (e.g., Delaney et al., of little consequence 1992) and swarm -induced rearrangem ent of the perm eability Moderate Readily apparent change over a relatively w ide area zone (Crone et al., 2010). Docum ented disturbances include Major Substantial change to the ecosystem over a large extended duration (weeks to m onths) tem perature anom alies of area (i.e., a vent field) 10 C or m ore in diffuse flow zones occupied by vent invertebrates 62 C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 that, prior to seism ic activity, had tem perature records below 5 C; creating a longer-lasting (years), chronic effect that influences the the consequences of this scale of perturbation on the biological com m unity com position of vents. In this cycle, heat flux in the com m unities rem ains uncertain (Johnson et al., 2000). hydrotherm al system increases im m ediately follow ing the up- Where chim neys collapse, there is loss of habitat, but new sur- w elling or eruption of m agm a (Butterfield et al., 1997; Von Dam m , faces m ay form and becom e recolonized. Changes in fluid flow 1995). This triggers phase separation of fluids and delivery of low resulting from seism ic activity could have m any biological conse- chlorinity fluids, heat, volatiles (e.g., sulfide, carbon dioxide, quences, including m ortality of taxa intolerant of the altered ther- hydrogen), and dissolved m etals to the seafloor. As the system m ochem ical conditions and enhanced grow th, reproduction, and cools, vent fluids m ay go through a brine phase, followed by decay recruitm ent of taxa adapted to the altered conditions. Tectonic back to chlorinities of seawater. This hydrotherm al cycle affects the events m ay also generate plum es of suspended sedim ents that biological productivity, habitat quality, and com m unity com posi- m ight cause burial of organism s, clog filtering m echanism s of tion of diffuse flow system s. suspension-feeding invertebrates, or otherw ise interfere w ith bio- At the 9N vent field on the East Pacific Rise, w here the hydro- logical activity (Binns and Decker, 1998), but such an event and its therm al cycle was reset by a 1991 eruption, com m unity response to consequences are so far not docum ented. changing physico-chemical conditions was docum ented during a m ulti-year period (Shank et al., 1998). Subseafloor bacterial pro- 3.4. Volcanic eruptions and hydrothermal cycles ductivity increased im m ediately follow ing the eruption (a phe- nom enon observed on other ridge system s as w ell; Marcus et al., Hydrotherm al vents are associated w ith volcanic system s and as 2009; Tunnicliffe et al., 1997) and bacterial m ats and grazers on such are periodically subjected to volcanic eruptions and overrun. bacterial m ats predom inated im m ediately follow ing the eruption The frequency and duration of volcanic events vary depending on (Marcus et al., 2009; Shank et al., 1998). The vestim entiferan factors such as seafloor spreading rate and thickness of the crust tubew orm Tevnia jerichonana blanketed the study sites w ithin one (Rubin et al., 2012). Subm arine volcanic eruptions m ay be explosive year and was inferred to be a pioneer species that tolerates higher and continuous events, as evidenced by m ulti-year eruptions at tem perature and sulfide conditions than giant tubew orm s (Riftia subm arine subduction zones (Em bley et al., 2006; Deardorff et al., pachyptila). Sulfide concentrations at study sites decreased 50% 2011; Rubin et al., 2012), or m ore effusive events (som etim es w ithin two years of the eruption, and T. jerichonana was replaced by w ith explosive com ponents; Chadw ick et al., 2012; Dziak et al., dense aggregations of R. pachyptila (Shank et al., 1998). Sulfide 2009; Gregg et al., 1996) that take place relatively frequently concentrations continued to decline in subsequent years and (decadal or even sub-decadal tim e scales) and in a punctuated m ussels began to colonize the seafloor diffuse flow vents along m anner (durations of days to w eeks) on fast- and interm ediate w ith increasing num bers of associated invertebrate taxa (Shank spreading centers (e.g., East Pacific Rise, Juan de Fuca Ridge). et al., 1998). A sim ilar hydrotherm al cycle was observed in the Chronic explosive volcanic activity generates an unstable sam e area follow ing a 2005e 2006 eruption (Luther et al., 2012; benthic habitat that is colonized by only a few species. At ‘Brim - Nees et al., 2008. Biological responses to eruptions at Co-Axial stone Pit’, a volcanically active crater at the NW Rota-1 seam ount, Volcano (Tunnicliffe et al., 1997) and Axial Volcano on the Juan de m icrobial m ats and populations of m obile vent shrim p and crabs Fuca Ridge (Marcus et al., 2009) have also been m onitored, and a are the only persistent organism s (Em bley et al., 2006). Acute relatively rapid succession of taxa responding to biotic and abiotic effusive volcanic eruptions have acute catastrophic effects on hy- factors is reported. drotherm al vent com m unities. Lava flows, m ass wasting, and Significant changes in larval supply before and after a m ajor explosive eruptions destroy vent com m unities, and there is typi- volcanic eruption have been reported using larval traps cally a redistribution of venting activity associated w ith an eruption (Mullineaux et al., 2010). The 2006 eruption on the East Pacific Rise (Haym on et al., 1993). These events create a ‘tim e zero’, a Krakatau- near 9500N resurfaced an area of nearly 15 km 2 along w 18 km of like reset of the system (Whittaker et al., 2010), w ith w ell- ridge crest (Soule et al., 2007). Loss of resident populations was docum ented ‘recovery’ of vent com m unities to pre-disturbance correlated w ith dim inished larval supply after the eruption conditions taking place w ell w ithin a decade (Marcus et al., 2009; (Mullineaux et al., 2010), a correlation consistent w ith population Shank et al., 1998; Tunnicliffe et al., 1997). m aintenance through processes that allow for larval retention. One Very infrequent eruptive events (repose intervals of a thousand species that was all but absent prior to the eruptiond the lim pet years or m ore) are inferred for slow-spreading ridges (e.g., Mid- Ctenopelta poriferad increased in supply (Mullineaux et al., 2010), Atlantic Ridge; Rubin et al., 2012), w here vent sites are long-lived consistent w ith high gene flow facilitated by infrequent exchange and spaced at intervals of 100 km and m ore (Cherkashov et al., of individuals am ong populations. Continued studies w ill docu- 2010). Despite the apparent longevity of venting activity in a m ent w hether the changes observed in larval supply and coloni- given location, invertebrates living at Mid-Atlantic Ridge vents also zation represent a phase of a successional process or w hether there display life-history characters associated w ith opportunistic spe- has been an ecological regim e shift (Mullineaux et al., 2010). cies (Llodra et al., 2000; Tyler and Young, 1999), w hich suggests Physico-chem ical environments of diffuse flow habitats at hy- that factors other than volcanic eruptions m ay influence these life- drothermal vents evolve during the hydrotherm al cycle and history characters. different taxa m ay be optimally adapted to or tolerate different Genetic data can provide insight into the occurrence of cata- phases of this cycle. Because there are m ultiple vent sites strophic events, but any link to a singular volcanic event is so far not com prising a vent field at 9N and on the eruptive segment of the tenable. As an exam ple, there is prelim inary genetic evidence based Juan de Fuca Ridge, and because these sites are not all linked to the on a single gene sequence for a recent bottleneck or founder event sam e hydrothermal system and not all affected by a given eruption followed by dem ographic expansion in the shrim p Rimicaris exo- event, there is always an array of habitats in different phases of the culata, a typical dom inant species at vents south of the Azores hydrothermal cycle that facilitates persistence of populations in the (Teixeira et al., 2011), but this genetic ‘event’extended from 36N to face of local extinctions through dispersal and colonization events. 4S, far beyond the reach of a single eruptive event as w e currently This demographic instability m ay be recorded in genetic data as loss understand them . of rare alleles during frequent extinction and recolonization events In addition to the physical disturbance of lava overrun, eruptions (Coykendall et al., 2011), w ith shallow, star-like genealogical net- reset the hydrotherm al cycle for fluid physic-chem ical param eters, works indicating recent population expansion (Vrijenhoek, 2010). C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 63

3.5. Placing deep-sea hydrothermal vent ecosystems in an discovery in 1976 (Corliss et al., 1979). Scientific research has been ecological-disturbance-resilience framework the prim ary source of hum an disturbance at vents (Glowka, 2003), w ith m ore than 600 scientific research expeditions to hydrother- As sum m arized above, hydrotherm al-vent ecosystem s are sub- m al vents since 1976 (Godet et al., 2011). The num ber of expeditions ject to a variety of spatio-tem poral scales of natural disturbance and has been doubling every five years globally. Scientific research and as such, they arguably occupy one extrem e of a disturbance- m ineral exploration activities at vents has the beneficial im pact of resilience gradient relative to other deep-sea ecosystem s (Fig. 1), increasing our knowledge of geophysical and hydrotherm al pro- an extrem e sim ilar to that of tem perate and boreal rocky intertidal cesses, biodiversity, adaptation to extrem e environm ents, and zones that experience chronic disturbance through wave action m any other fields. The ‘knowledge value’ of hydrotherm al-vent and that are periodically scoured by ice (Kelly and Metaxas, 2010). ecosystem s as ‘living libraries’d as m easured by both the num ber Characteristic taxa colonizing hydrotherm al vents tend to be of publications resulting from this research and their im pact abundant, w ith high biomass, rapid grow th rates, and high repro- factorsd is high (Godet et al., 2011). ductive output. The fauna of other deep-sea reducing environm ents Where expeditions use rem ote sensing system s such as m ulti- (seeps and w hale falls) are interm ediate in this disturbance-resilience beam sonar and a variety of water-colum n sensor system s (e.g., continuum (Glover et al., 2010), experiencing, for example, tectonic backscatter, Eh and other chem ical sensors, m agnetics), there is shifts in fluid flux (seeps: Hornbach et al.,2007; Tryon et al.,2012) and likely negligible im pact on hydrotherm al-vent com m unities. But successional sequences (seeps: Bergquist et al., 2003; Cordes et al., m ost scientific or m ineral exploration research uses a com bination 2009; w hale falls: Smith and Baco, 2003). Taxa that live in sedi- of autonom ous, tethered, or hum an-occupied vehicles, tow ed m ents of the abyssal plain and manganese nodule beds are arguably cam era sleds, and cabled observatories to engage in observation, at the other extreme of the disturbance-resilience context in the deep sam pling, and instrum ent deployments and recoveries. These tools sea (Fig. 2). At this m ore stable extreme, natural disturbances tend to and activities have varying types of im pacts on vent ecosystem s be biogenic and subtle compared to those experienced by vent or- (discussed below ). Know n im pacts of scientific or m ineral explo- ganism s. Such disturbances include periodic pulses of phytodetritus ration activities to date are deem ed to be negligible or m inor and deposition (Gooday, 2002), bioturbation (Smith et al., 1997), boome short-term , w ith the possible exceptions of scientific drilling bust cycles of echinoderms (Billett et al., 2010), and climatic effects (w here it extends 10s of m eters and m ore below the seafloor in an (Ruhl, 2007). In these low-disturbance, low-resilience regimes there active vent system ) and dam age to photoreceptors by high- is generally relatively low abundance, biomass, grow th rates, and intensity illum ination (see discussions below ). reproductive output of benthic invertebrates (McClain et al., 2012). Cold-water coral reefs and gardens experience biogenic reef cycles 4.1.1. Interference with vent ecosystems by tools of scientific and are m ore productive than abyssal plain ecosystems (Roberts et al., research and mineral exploration 2006; Thiem et al., 2006; Murray et al., 2006); as such, they are at an At the largest spatial scales, scientific and com m ercial explora- intermediate level in the disturbance-resilience space. tion interference w ith vent ecosystem s is incurred during geophysical m apping, including active m ulti-channel seism ic 4. An th ropogen ic distu rban ce in hydroth erm al ven t studies that use air guns and other sound sources to study the ecosystem s subsurface structure of the seabed (e.g., Carbotte et al., 2012) and sonar m ethods that yield bathym etric m aps w ith 1-m scale reso- 4.1. Impact of scientific research and mineral exploration activities lution (e.g., Caress et al., 2012). These activities are undertaken from surface ships and, in the case of m ultibeam sonar m apping, from The presence of hum ans at deep-sea hydrotherm al vents has a autonom ous, tethered, and hum an-occupied vehicles as w ell. relatively short historyd m easured in decadesd since their initial Insonification during m ultibeam m apping is at low frequencies (e.g., the Reson m ultibeam system has dual frequencies at 200 and 400 kHz) that, together w ith sounds generated by the vehicle itself, could potentially alter behaviors and m ask com m unication reper- toires of, for exam ple, vent-dw elling fish (see Codarin et al., 2009; Popper, 2003). To date there has been no study or evidence of im pact of biologically relevant am bient and introduced sound in vent ecosystem s. Large-scale m apping is also undertaken w ith m agnetom eters to identify m agnetic anom alies associated w ith volcanic rocks, but the m agnetic recordings are passive. Sensor surveys (e.g., conductivity, temperature, Eh, transm issivity) in the water colum n are benign to benthic com m unities. Im aging surveys are com m only undertaken at m ultiple spatial scales and require high-intensity light that can tem porarily alter behavior of fish and invertebrates. These behavioral m odifications m ay result in census biases resulting from attraction or avoidance (Stoner et al., 2008), but the im pact of lighting during photosurveys on benthic vent com m unities is deem ed to be m inim al, the light being infrequent and of short duration, albeit of high intensity.

Fig. 2. Hydrotherm al-vent ecosystem s in an ecological (e.g., abundance, biom ass, Rock dredge activities in support of scientific and com m ercial grow th rate, reproductive output), disturbance (likelihood and spatiotem poral scale), exploration of m id-ocean ridge system s result in relatively indis- and resilience fram ew ork. Vents are exposed to frequent and som etim es locally crim inate, destructive ‘bites’from the seabed (the m outh of a rock catastrophic natural disturbances and vent taxa have ecological attributes consistent dredge is typically on the order of 0.5 m in w idth). Scientists leading w ith resilience (high abundance, biom ass, grow th rate, reproductive output); biodi- rock dredge activities generally aim to avoid hydrotherm al vent versity at vents is relatively low. Vents on slow-spreading centers such as the Mid- Atlantic Ridge (MAR) experience less frequent volcanic eruptions than those on fast- sites. There is at least one celebrated exam ple, however, w here a spreading centers like the East Pacific Rise (EPR). White text: shallow-w ater ecosystem . rock dredge recovered sulfide deposits and live m ussels 64 C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 characteristic of vent com m unities, providing the first indication of stages from one site to another. Ballast tanks on HOVs designed to a previously unknow n vent field on the Mid-Atlantic Ridge, sub- hold water at am bient seafloor pressures are often filled or dum ped sequently nam ed ‘Lucky Strike’(Langm uir et al., 1997). Traw lers in the vicinity of vents, w here they can take on and expel larvae and (com m ercial or scientific) avoid m ost hydrotherm al vent settings m icrobes. Where study sites are w ithin a day or two-day transit because of the hard rock nature of the seabed and the rugged from one another, it is easy to im agine ballast system s of deep-sea terrain. vehicles as effective vectors, just as they are in coastal waters. The Plankton net tow s and pum ps m ay be m ade in the vicinity of potential role of scientific gear and vehicles in unintentional hydrotherm al vents in studies of larval distributions, pelagic food transport was also highlighted in the case of an epizootic fungal w ebs, and biodiversity; the ‘take’of plankton nets is generally very infection in m ussels from sites in Fiji Basin (Van Dover et al., 2007) low. Typical biom ass recovered is low, although there has been at and for other pathogens and parasites (Voight et al., 2012). least one record of a 226 alvinocarid post-larval shrim p in 33 tow s High-intensity illum ination associated w ith HOVs and ROVs has (Herring and Dixon, 1998). Given their short duration and lim ited been im plicated in photoreceptor dam age in shrim p that aggregate sam pling swath, plankton tows and pum p sam ples are inferred to on black sm okers at vents the Mid-Atlantic Ridge, and by inference, have negligible im pact on vent ecosystem s. their cognates at vents on the Central Indian Ridge and Mid- Scientific drilling in hydrotherm al settings is used to study the Caym an Spreading Center. Thoracic eyes in adult vent shrim p (R. structure of the ocean crust, hydrotherm al circulation, and other exoculata) contain visual pigm ent (rhodopsin) that is light sensitive deep-crustal processes and provide a subsurface dim ension useful and the structure of the eyes suggests they are adapted to detecting for understanding the distribution of vent faunas (Grehan and dim light generated by high-tem perature venting as a near-field Juniper, 1996). Sedim ent deposition occurs during activities of the rem ote-sensing m eans of avoiding therm al stress and m ortality Ocean Drilling Program (ODP), w here drill rigs deployed from (Van Dover et al., 1989). Initial description of these thoracic pho- surface ships penetrate to depths of 100 m and m ore below the toreceptors noted degraded rhabdom eral segm ents inferred to seafloor. At the TAG hydrotherm al m ound on the Mid-Atlantic result from exposure to light (Van Dover et al., 1989). Functional Ridge, ODP drilling activities in 1994 resulted in transient arhabdom eral segm ents in juveniles and attenuated arhabdom eral displacem ent of shrim p and burial of anem ones (Copley et al., segm ents in adult specim ens suggest that the cellular m achinery to 1999). Disturbances caused by this drilling w ere localized and the support rhabdom eric turnover (recovery from light dam age) dis- overall ecology and productivity of the vent site has been stable on appears during ontogeny (Cham berlain, 2000). Herring et al. (1999) a decadal tim escale (Copley et al., 2007). Bore holes can alter local brought forward further associative evidence of light-induced hydrotherm al circulation and create new ‘artificial’hydrotherm al dam age to eyes of vent shrim p, but to date, there is little to no vents that are often cased and capped w ith an outlet for subsequent understanding of the behavioral consequences of light-dam aged study of the evolution of hydrotherm al fluids and of m icro- and photoreceptors in vent shrim p. There has also been no evidence m acrofaunal developm ent (e.g., Takai et al., 2012). of a decline in shrim p populations at the TAG m ound during a Hum an-Occupied Vehicles (HOVs) and Rem otely Operated Ve- decade of repeated exposure to scientific research, suggesting that hicles (ROVs) likely do the m ost dam age to hydrotherm al-vent there is no im m ediate conservation threat to shrim p populations com m unities through m aneuvers, light pollution, intensive and resulting from high-intensity illum ination (Copley et al., 2007). destructive sam pling, intentional and unintentional transplants, Other taxa w ith light-sensitive organs are likely susceptible to abandoned m aterials, and potential for transport of propagules to dam age from subm ersible illum ination, including bythograeid non-native areas and spread of disease. By virtue of their relatively crabs (Jinks et al., 2002). large size and ability to take on water ballast and achieve w eighted Scientific research activities intentionally and unintentionally stability on the seabed, HOVs have the greatest potential to dam age abandon m aterials on the seafloor in the vicinity of hydrotherm al vent com m unities by crushing seabed fauna and bashing anim als vents, including subm ersible ballast (iron shot or plates), ‘ghost’ living on sulfide deposits and other seafloor features w ith vertical traps (deployed to capture crabs, fish, and other m obile scavengers relief (basalt pillars, graben walls, etc.). In the past, HOVs w ere and predators and abandoned on the seafloor), plastics of various intentionally used to ram sulfide chim neys for sam ples, but this kinds (m ilk crates, navigational m arkers, polypropylene line), brute tactic is now discouraged (Devey et al., 2007). Tops of m ooring chains and anchors, etc. This scientific ‘trash’has so far had chim neys are, however, often rem oved as part of a precision negligible or possibly m inor im pact on vent ecosystem s, but it can strategy to collect paired fluid/rock sam pling from vent orifices and have a long-term im pact on viewsheds of scientific research areas to excavate orifices to enable sam pling of undiluted end-m em ber and the ability of docum entary artists to capture im ages of pristine vent fluids. Unintentional destruction seem s likely to be lim ited vent habitats. Cultural artifacts are occasionally purposefully placed to fractional areas of vent com m unities; the im pact of uninten- on the seafloor at hydrotherm al vents. Perhaps the best exam ples tional habitat disturbance is rarely m easured. Im pacts of sam pling are installations of glass ‘Planets’created by artist Josh Sim pson at or other hum an-induced disturbances that displace anim als are hydrotherm al vents in Pacific, Atlantic, and Indian Oceans (Fornari, m ost severe w here the disturbed anim als are attached holobiont 2001) and ashes of the late Professor John Edm ond, a pioneer in the taxa (such as vestim entiferan tubew orm s) and relatively sessile study of the chem istry of hydrotherm al vents, at ‘Moose’(Snake Pit holobiont taxa, including bathym odiolin m ussels and provannid vent field) on the Mid-Atlantic Ridge (Van Dover, pers. obs.). gastropods (Tunnicliffe,1990), all of w hich depend on their position In addition to HOVs, ROVs, and AUVs, the scientific com m unity is in diffuse flow to sustain their sym bionts. building cabled observatories, including the US Regional Scale Scientific sam pling equipm ent on HOVs and ROVs has the po- Network (RSN) that instrum ents a tectonic plate, w ith a node at tential for unintentional transport of anim als from one site to hydrotherm al sites on Axial Seam ount (Juan De Fuca Ridge). The another, as observed in the case of Gorda Ridge lim pets transported funding agency for the RSN (National Science Foundation) required to the Juan de Fuca Ridge in a suction sam pling device (Voight et al., a site-specific Environm ental Assessm ent of potential im pacts to 2012). It is not clear w hether the Gorda lim pet species was in fact the natural environm ent for a num ber of resources during instal- introduced to the Juan de Fuca locale, but there is convincing evi- lation, operations, and m aintenance of the RSN cabled observatory, dence that it was a contam inant in sam ples ostensibly from the in com pliance w ith the US National Environm ental Protection Act. Juan de Fuca sam pling site, highlighting the potential for intro- Deploym ent and recovery of cables, nodes, and instrum ents w ere duction. Ballast water also has the potential to transport larval deem ed to result in short-term , m inor changes in water quality and C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 65 occupancy of very sm all patches of seabed (Cardno TEC Inc., 2013; Derivatives of vent m icroorganism s include enzym es developed by TEC Inc., 2011) and that the threshold of im pact that w ould Diversa Corporation (PyrolaseÔ 60, Valley Ultra-ThinÔ), Invitrogen require an Environm ental Im pact Statem ent (EIS) was not reached. Corporation (Therm alAceÔ DNA Polymerase), and New England Ò While the installation of the cabled observatory itself m ay have no Biolabs Inc. (Deep VentR DNA Polym erase, am ong others) (Leary, im pact, the im pact of long-term and intensified scientific studies of 2004). The Valley Ultra-ThinÔ enzym e lowers the viscosity of Axial Seam ount and other vent ecosystem s (e.g., the Endeavour cornstarch, operates at high tem perature and lower pH, and allow s vents, w w w.oceannetworks.ca) facilitated by the operation of the for m ore efficient ethanol production than other enzym es (PR cabled infrastructure is of interest, but likely to be m inor, i.e., New sw ire, 28 February 2006), and was estim ated to have an annual resulting in detectable but sm all, localized, changes to vent eco- sales value of US$150 m illion (Leary et al., 2009). system s w ith little environm ental consequence. To date, interest in genetic resources from vents has involved therm ophilic and hypertherm ophilic prokaryotic m icroorganism s 4.2. Impact of commercial (exploitation) activities (Bacteria and Archaea) collected in lim ited quantities during sci- entific research for initial gene or product discovery (Leary et al., Im pacts of com m ercial activities are inform ed by our know ledge 2009; Pettit, 2011). Downstream product developm ent often re- of vent ecosystem s, but m ost w ill rem ain theoretical until the ac- lies on laboratory cultivation, especially for m icrobes (Martins et al., tivities begin and im pacts are experienced and m onitored. Where 2013; Pettit, 2011; Thornburg et al., 2010). As such, the environ- the tem po and scale of hum an activities at hydrotherm al vents in a m ental im pacts of genetic resource activities on deep-sea hydro- given region are intense, cum ulative im pacts w ill need to be therm al vents are currently considered to be negligible or m inor. assessed and m anaged as appropriate to ensure there are not For natural products that m ight eventually be derived from vent regional losses of brood stock, genetic diversity, species, trophic invertebrates (e.g., Andrianasolo et al., 2011), initial harvest w ill interactions and com plexity, and resilience, together w ith changes likely be sm all (Thornburg et al., 2010), but subsequent and m ore in com m unity structure, genetic isolation, and the possibility of substantial harvests m ay be required (Arrieta et al., 2010). In the species extinctions, and species invasions. absence of environm ental regulations, large harvests of w ild vent Am ong the com m ercial activities proposed for hydrotherm al invertebrate species to sustain a com m ercial enterprise are unde- vents, the m ost benign m ay be tourism and docum entary arts, sirable (Arrieta et al., 2010) and, if undertaken, m ay exceed the size already underway. Genetic resources have already been developed of collections m ade during scientific sam pling and have m oderate from vent organism s in tandem w ith scientific research; com m er- to m ajor im pacts on both the target species and the vent ecosystem , cial harvest of vent organism s for secondary m etabolites that m ay including m odified recruitm ent, size-class structure, diversity, serve as therapeutic agents or other com m ercial products are so far trophic interactions, and ecosystem services. Large harvests un- not w idely reported, if they have taken place at all. Hydrotherm al dertaken periodically (e.g., on an annual basis) as part of a com - and geotherm al energy sources have been considered since vents m ercial production schem e w ould likely have a m ajor im pact on w ere first discovered and are still under study. One recent concept the vent ecosystem . paper envisions offshore gigawatt pow er stations that extract m inerals from hydrotherm al fluids using therm o-electric genera- 4.2.3. Energy and mineral harvesting tors (Parada et al., 2012), w ith potential for hydrogen fuel produc- Military interest in tapping into deep-sea hydrotherm al vents to tion as w ell (Bubis et al., 1993). Conventional, open-cut m ineral pow er seafloor listening devices and other equipm ent began soon extraction of seafloor m assive sulfide deposits, associated w ith after the discovery of vents on the seafloor. Interest in using power hydrotherm al vents, seem s the m ost likely com m ercial activity to from vents is grow ing (e.g., Hiriart et al., 2010), and pilot generators take place in the near future (Aldhous, 2011; Hoagland et al., 2010). for scientific research are nearing the testing phase. For exam ple, Each of these activities is considered below. Mercury, ‘a solid-state, m odular, and scalable hydro-therm oelectric generator’is planned for Axial Seam ount as a pow er source for 4.2.1. Adventure tourism and documentary arts research sensors and AUVs (MAPC: w w w.m apcorp.com ). A m ore The UK-based Deep-Ocean Expeditions LLC (inactive since 2012) am bitious, com m ercial approach to a ‘deep-sea energy park’in- has taken m ore than 40 fee-paying tourists to Atlantic and Pacific cludes a therm oelectric pow er-generating station com bined w ith deep-sea hydrotherm al vents in the MIR subm ersibles (Leary, m etal and m ineral extraction from hydrotherm al fluids, desalina- 2007). HOVs and ROVs have been used in the production of tele- tion, and hydrolysis and hydrogen storage (Parada et al., 2012). At vision, film , and video docum entaries, including titles produced by least one U.S. patent has been awarded for a ‘hydrotherm al energy Stephen Low and Jam es Cam eron (Leary, 2007; Van Dover pers. and deep-sea resource recovery system ’(Marshall, 2010). Energy obs). Tourism and docum entary arts activities are relatively infre- and m ineral harvesting system s do not resurface the vent quent and are usually integrated into m arine scientific research ecosystem as m ineral extraction of sulfide deposits w ill do, but they program s; their im pacts are indistinguishable from those cited m ay involve activities (e.g., establishing stable conduits), that above for scientific research (Section 4.1). Tourism and docum en- w ould cause physical dam age (Parada et al., 2012) and likely alter tary arts have the beneficial im pact of educating the public about the diffuse fluid flows that support hydrotherm al-vent ecosystem s. the deep ocean and hydrotherm al system s and, in the case of tourism under the auspices of Deep-Ocean Expeditions, helped to 4.2.4. Mineral extraction fund scientific research (Leary, 2007). Technologies currently proposed for extraction of m ineral de- posits at hydrotherm al vents involve bulk rem oval of m inerals akin 4.2.2. Genetic resources to an underwater equivalent of terrestrial open-cut m ining. One Deep-sea hydrotherm al vents are extreme environm ents, w here proposed m ethod is m echanical cutting and slurry transportation organism s are adapted to tem peratures, chem istries, sym biotic of ore through a riser system to a support vessel and a return water relationships, and other circum stances that m ake vent organism s of pipe w hich returns the seawater separated from the ore after interest to drug, enzym e, cosm etic, biofuel, and other product de- removal of particles > 8 mm (Coffey Natural System s, 2008), to 25e velopers (Arrieta et al., 2010; Leary, 2004; Leary et al., 2009; 50 m above the seafloor (Coffey Natural System s, 2008; Hoagland Thornburg et al., 2010). These products are of benefit to society as et al., 2010; Masuda, 2011; Sm ith and Sm ith, 2010-2011). Other therapeutic agents and in a variety of industrial applications. concepts for com m ercial m ining under consideration include a 66 C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72

‘grab’system (rem oval and transport of m ineral deposits in a grab m obile organism s that m ay avoid or be attracted to light and/or to a surface vessel), m agnetic separation at the seabed, and solution noise. m ining or bio-leaching (Scott, 2007). In a region w here there is only a single geographically con- The im pacts of m ineral extraction rem ain theoretical in the strained m ining event, vent com m unities are predicted to re- absence of a pilot m ining operation or experim ent although m uch establish w ithin years, as they do following volcanic eruptions can be estim ated based on other seafloor operations such as (Van Dover, 2011a), although they m ay have structure and function dredging, trenching and diam ond m ining. There continues to be different from w hat existed prior to m ining. uncertainty about w hether m ineral extraction w ill be undertaken at active hydrotherm al-vent ecosystem s (Hein et al., 2013), partic- 4.2.4.1. Impact of mineral extraction on recolonization processes. ularly given that high temperature and caustic characteristics of Once an im pact has occurred, recovery of a vent ecosystem is vent fluids of vigorously active black sm okers m ay be incom patible dependent on both im m igration of m obile species and successful w ith extraction technologies (Yam azaki, 2011). If extraction takes colonization by larvae (Adam s et al., 2012). Literature that provides place at non-active, ‘old‘ vent system s, there is likely to be a insight into factors that m ay influence the recovery of a vent system different set of, potentially m ore deleterious, im pacts (Van Dover, is reviewed here in the context of extraction activities, but apply as 2011a). w ell to any hum an activity that results in a sim ilar quality and in- Potential im pacts of a m ineral extraction activity on a tensity of habitat alteration. hydrotherm al-vent ecosystem fall into two broad categories: causal 4.2.4.1.1. Maintenance of local populations: self-recruitment and physico-chemical changes and biological response or consequence near-bottom larval densities. There is gathering evidence that, at (Table 2). The m ain physical im pacts expected are loss of habitat least for som e hydrotherm al-vent systems, invertebrate pop- through removal of ore and associated organism s, degradation of ulations are m aintained by local larval supply and retention during habitat quality through reshaping of the seabed, and m odification periods of habitat stability (Adam s and Mullineaux, 2008; Metaxas, of fluid flux regim es. The intensity of im pacts is expected to be 2004, 2011), even w hile gene flow m ay be high from one site to m ajor at the site scale (Fig. 1). While vent ecosystem s are naturally another (Vrijenhoek, 2010). Characteristics that facilitate local exposed to fallout of m inerals from black-sm oker plum es and larval supply include behavioral or other processes that retain possibly from plum es of nearby volcanoes, the intensity of sedi- larvae near the seafloor, effectively m inim izing dilution and m ent plum es generated during m ining activities m ay be in excess transport (e.g., Kim and Mullineaux, 1998; Mullineaux et al., 1995). of natural exposures at the local scale during certain phases of For exam ple, topographic basins form ed by deep axial valleys (e.g., operations. Juan de Fuca Ridge, NE Pacific) constrain circulation and trap and Im pacts to biological system s resulting from m ining activities m ix larvae (McGillicuddy et al., 2010; Thom son et al., 2003). Larval include loss of local populations w here ore and organism s are distributions estim ated from net tow s w ithin axial valleys m ay be rem oved together and the potential local extinction of rare species. hom ogeneous i.e., no difference in larval abundance near vents The ecological significance of the rare species is uncertain, but the (w ithin tens of m eters) or away from vents (up to 5 km ; Metaxas, im pact of their local loss is likely to be m inor. Likely m inor to 2004) or heterogeneous, w ith higher abundances found near m oderate im pacts m ay result from pum ping water from near the vents (w ithin tens of m eters) than away from vents (hundreds of seabed at vents w here larvae of vent invertebrates tend to be m ost m eters; Mullineaux et al., 2005). concentrated (Section 4.2.4.1). Minor (likely short term ) im pacts 4.2.4.1.2. Timing of larval supply. A few studies have used larval m ay also be evident in altered behaviors of vent fish and other traps on m oorings to characterize the tem poral dynam ics of larval

Table 2 Types of environm ental im pacts resulting from m ineral exploitation at deep-sea hydrotherm al vents and exam ples of references that m ention these im pacts.

Im pact References

Ph ysico-ch em ical im pacts (cau se) Loss of habitat Baker et al., 2010; Coffey Natural System s, 2008; Glover and Sm ith, 2003; Glow ka, 2000; Halfar and Fujita, 2007; Hein et al., 2013; Ram irez-Llodra et al., 2011; Van Dover, 2007; Van Dover, 2011a,b Degradation of habitat quality Coffey Natural System s, 2008; Halfar and Fujita, 2002, 2007; Van Dover, 2007, 2011a,b (altered topography, substrata) Modification of fluid flux regim es Baker et al., 2010; Coffey Natural System s, 2008; Glow ka, 2000, Halfar and Fujita, 2007, (flow rates, distribution, chem istry) van den Hove and Moreau, 2007; Van Dover, 2007, 2011a Sedim ent plum e and sedim entation Baker et al., 2010; Coffey Natural System s, 2008; Glow ka, 2000; Halfar and Fujita, 2002, 2007; Ram irez-Llodra et al., 2011; Thiel, 2003; Van Dover, 2007; Van Dover, 2011a Light, noise Baker et al., 2010; Coffey Natural System s, 2008; Van Dover, 2011a; Yam azaki, 2011 Poten tial biological im pacts (respon se) Elim ination or reduction of local populations Baker et al., 2010; Gena 2013; Glover and Sm ith, 2003, van den Hove and Moreau, 2007, and decreased reproductive output Van Dover 2007, 2011a; Van Dover et al., 2011 Loss of larvae/zooplankton in lift system Coffey Natural System s, 2008; This paper Local, regional, or global extinction of rare species Van Dover, 2007, 2011a Decreased seafloor prim ary production Van Dover, 2007 Modification of trophic interactions Van Dover, 2007 Decreased local diversity (genetic, species, habitat) Coffey Natural System s, 2008; van den Hove and Moreau, 2007; Van Dover 2007, 2011a Mortality or im pairm ent due to toxic sedim ents Coffey Natural System s, 2008; Halfar and Fujita, 2007, Van Dover, 2007, 2011a; Woodw ell, 2011 Altered behaviors This paper Oth er Potential Cum ulative effects (regional losses of: Van Dover, 2007, 2011a,b; Van Dover et al., 2011; Vrijenhoek, 2010; this paper brood stock, genetic diversity, species, trophic interactions and com plexity, resilience; changes in com m unity structure, genetic isolation, species extinctions, species invasions) C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72 67 supply in the vicinity of hydrotherm al vents (e.g., Khripounoff et al., approaching that of the life cycle of the dom inant taxad is a m odel 2008; Mullineaux et al., 2005). These studies suggest that supply of for vent ecosystem s in other geological settings w ith different larvae is discontinuous and that tim ing of m axim al supply of larval frequencies of catastrophic disturbance, rem ains to be determ ined. taxa varies from one taxon to another. While seasonal periodicity in Although volcanic eruptions are indiscrim inant and do not reproduction is suggested as one m echanism that could account for em ploy strategies to m inim ize im pacts such as establishing set- discontinuous larval supply, alternative (non-exclusive) explana- aside areas nor do they em ploy strategies to restore, volcanic tions have also been suggested, including behavioral interactions eruptions m ay be the closest natural analog to the scale of im pact of w ith turbulence produced by black sm okers that could increase m ineral extraction at an active hydrotherm al system . Lessons residence tim e (Mullineaux and France, 1995; Mullineaux et al., learned from larval studies follow ing eruptions include: 2005), flow conditions m odulated by tidal variations and tectonic activity (Crone et al., 2010), or settlem ent cues (Khripounoff et al., Where larval retention occurs near natal sites, larval supply w ill 2008). be at least tem porarily dim inished follow ing an eruption or 4.2.4.1.3. Settlement cues and gregarious settlement. Larvae of other disturbance that rem oves benthic adult populations m arine invertebrate taxa are selective in w here they settle and they (Mullineaux et al., 2010); larval supply is likely correlated w ith respond to inducem ent and deterrent cues, including those asso- benthic population density (Metaxas, 2011). ciated w ith chem ical and physical characters of the environm ent Changes in substratum , fluid chem istry, and other vent prop- and odors from conspecifics or other organism s (m icrobial and erties concom itant w ith seabed eruptions and other m assive otherw ise) in the environm ent (review ed in Hadfield, 2011; disturbances can select for subsets of species w ith tolerances to Hadfield and Paul, 2001; Steinberg et al., 2002; am ong others). the changed and changing conditions, at least tem porarily Observations of gregarious settlem ent in tw o species of vesti- changing the nature of the vent com m unity (Mullineaux et al., m entiferan tubew orm s [Lamellibrachia sp. on the Monowai Volca- 2010) nic Com plex (Tonga-Kerm adec Arc; Short and Metaxas, 2010), R. Tem poral variability (Mullineaux et al., 2005) and stochasticity pachyptila on the southern East Pacific Rise (G Rouse, R Vrijenhoek, (Mullineaux et al., 2010) in larval supply w ill influence post- CLVan Dover, unpublished)] and in m ussels (Van Dover et al., 2001) disturbance colonization options and outcom es. indicate that there can be pulsed, gregarious settlem ent of larvae in Colonization success by previously rare or absent species m ay be vent habitats. facilitated by natural or anthropogenic resets of the hydrother- Habitat degradation has been im plicated in altered settlem ent m al cycle that alter com petitive interactions in the earliest cues and changes in the pattern of replenishm ent of coral-reef fish stages of succession relative to established system s (Mullineaux com m unities (Feary et al., 2007; McCorm ick et al., 2010). Anthro- et al., 2010). pogenic activities that interfere w ith inductive settlem ent cues or The relative im pact of m ining or sim ilarly-scaled hum an activity generate deterrent settlem ent cues at hydrotherm al vents w ill on a vent ecosystem from the perspective of larval supply de- interfere w ith colonization and succession processes. We under- pends on the size of the local adult population that rem ains in stand little about how to predict the strength and duration of such the vicinity and continues to produce propagules, the degree of interference effects, but expect that changes in characters such as isolation of the site relative to larval dispersal capabilities, the fluid chem istry, substratum texture, m icrotopography, and m icro- degree of change in the geochem ical and geophysical setting bial biofilm regeneration resulting from m ineral extraction activ- (Metaxas, 2011), and on the consequences of stochastic and ities m ay not differ quantitatively from changes in these characters determ inistic processes related to succession and developm ent that take place follow ing a volcanic eruption or other circum stances of the vent com m unity. that cause new vents to form , followed by rapid colonization. 4.2.4.1.4. Major disturbances and changes in larval supply. 4.2.5. Indirect effects of human activities Significant changes in larval supply before and after a m ajor vol- Global clim ate change w ould seem decoupled from any direct canic eruption have been reported (Mullineaux et al., 2010). The im pact on the ecology of hydrotherm al-vent ecosystem s (Glover 0 2006 eruption on the East Pacific Rise near 9 50 N resurfaced an and Sm ith, 2003). Variable and elevated pCO2 and low pH fluids area of nearly 15 km 2 along w 18 km of ridge crest (Soule et al., inhabited by som e benthic vent organism s can provide insight into 2007). Supply of four gastropod larval types (m easured in sedi- the m etabolic cost of shell deposition (Tunnicliffe et al., 2009) and m ent traps at 6- to 7-day intervals) declined significantly after the com pensation m echanism s for acidosis (Fabry et al., 2008) under eruption, and one species that was all but absent prior to the these conditions. Larvae of vent organism s disperse in the pelagic eruptiond the lim pet C. poriferad increased in supply (Mullineaux environm ent and som e m ay even rely on developm ent periods in et al., 2010). C. porifera was a successful colonist in this system relatively shallow water, w here the biological effects of decreasing (first report for the locale) and species-abundance m atrices derived pH are expected to be evident (Doney et al., 2009) but the signifi- from colonization experim ents docum ent differences in pre- and cance to vent ecosystems of a changing surface ocean is obscure at post-eruption gastropod assem blages. The authors suggest that a this tim e. Anthropogenically induced and shifting patterns in the com bination of altered larval supply and tolerance to altered tim ing, duration, and strength of deep-reaching m esoscale surface environm ental conditions are not m utually exclusive and could eddies that m ay transport propagules hundreds of kilom eters from account for the observed patterns. Loss of resident populations was their source (Adam s et al., 2011) could change the dynam ics of correlated w ith dim inished larval supply, a correlation consistent long-distance dispersal and larval retention at vents. But un- w ith population m aintenance through processes that allow for certainties associated w ith any assessm ent of the im pact of clim ate larval retention. Introduction of a species previously unreported for change on vent ecosystem s are substantial. the area is consistent w ith high gene flow facilitated by infrequent exchange of individuals am ong populations. Continued studies w ill 5. Poten tial m itigation m easu res docum ent w hether the changes observed in larval supply and colonization represent a phase of a successional process or w hether While a detailed review of m itigation m easures is outside the there has been an ecological regim e shift (Mullineaux et al., 2010). scope of this paper, it is im portant to recognize that there m ust be a The extent to w hich the 950’N East Pacific Rise system d w here balance between resource extraction and acceptable environ- m ajor volcanic resets of vent habitats occur on tim e frames m ental im pact, and that environm ental im pacts can be m itigated. 68 C.L. Van Dover / Marine Environmental Research 102 (2014) 59e 72

Approaches to m itigation of environm ental im pacts include the ecosystem to recover at an im pacted vent field before activity at avoidance, m inim ization, restoration, and offset m easures. This another vent field is perm itted. m itigation hierarchy was established for w etlands m itigation (US Risk m anagem ent and m itigation efforts related to m ineral EPA and DA, 1990) and has since been m ore broadly adopted as a extraction include establishm ent of un-m ined biological corridors fram ework for environm ental m anagem ent (McKenney and (temporary refuges) w ithin a m ine site to aid in recovery of the Kiesecker, 2010). Underlying m itigation fram ew orks for biota and site rehabilitation, as described in the voluntary Code for hydrotherm al-vent ecosystems m ust be know ledge of the natural Environm ental Managem ent of Marine Mining (International ecosystem s, including its biogeographic context, biodiversity, Marine Minerals Society, 2011). These and additional approaches com m unity and trophic structure, connectivity, ecosystem services, to m inim ize im pacts of m ineral extraction and their application to a disturbance regim es and com m unity dynam ics, etc. This know l- future extractive operation are presented in Coffey Natural System s edge can be acquired through scientific research and through (2008). These approaches include i) establishm ent of an un-m ined baseline data collected as part of Environm ental Im pact Assess- area that can serve as both a reference site for com parative studies m ents (EIAs) (e.g., Van Dover, 2007; Collins et al., 2013). Monitoring and as a source of colonists (Collins et al., 2012), ii) netw orks of program s at appropriate spatial and tem poral scales yield addi- perm anent and tem porary set-aside areas w ithin the m ine site that tional know ledge and inform adaptive m anagement (Boschen et al., can also serve as sources of colonists, iii) deploym ent of 3- 2013). dim ensional structures (artificial substrates) to provide topo- Avoidance is a key first step in the m itigation hierarchy and it is graphic relief and structural stability for developing sulfide de- the approach advocated by the scientific com m unity for m itigating posits following m ining, and relocation of anim als w ithin the site to the im pacts of deep-sea research. Over-sam pling and unintentional facilitate re-establishm ent of characteristic invertebrates. Minim i- and intentional dam age to sulfide structures are am ong the im pacts zation approaches m ay also be applied to engineering design to vent ecosystems resulting from scientific research. Concern (Coffey Natural System s, 2008; Boschen et al., 2013), including, in about these im pacts prom pted developm ent of a voluntary code of the case of deep-sea m ining, system s and approaches that m ini- conduct for scientific research at vents that em phasizes avoidance m ize noise and sedim ent plum es, biodegradable lubricants, etc. of activities that m ight have long-lasting and deleterious effects Restoration or rehabilitation of vent ecosystem s and other (Devey et al., 2007). Actions to m itigate im pacts of other activities, degraded deep-sea habitats should be considered to address re- such as scientific drilling deep into the seabed, also include sidual im pacts as part of any m itigation hierarchy, undertaken only avoidance of sensitive areas w here vent anim als are particularly after all effort has been m ade to avoid and m inim ize im pacts (Van abundant (Juniper et al., 1992). Dover et al., 2014). Given the apparent natural resilience of vent Marine Protected Areas (MPAs) contribute to m itigation by ecosystem s, the scope for unassisted recoveryd som etim es establish avoidance zones. To date, a num ber of countries have referred to as ‘passive restoration’d should also be assessed and created Marine Protected Areas (MPAs) for hydrotherm al vent considered. There is scope for developing m itigation actions that ecosystem s (Van Dover et al., 2011), including Canada (Endeavour tim e activities (e.g., to reproductive periodicity, tidal periodicity) to Hydrotherm al Vents MPA), Mexico (Guaymas Basin and Eastern m inim ize im pacts, in addition to spatial set-asides. We do not yet Pacific Rise Hydrotherm al Vents Sanctuary), Portugal (Azores Hy- have a sophisticated understanding of rates of natural recovery for drotherm al Vent MPAs, and the United States (Mariana Trench m ost vent system s or of tem poral variability in larval supply at National Monum ent). There are currently no hydrotherm al-vent vents, but building this know ledge w ill help to determ ine w hether MPAs in international waters, but hydrotherm al-vent ecosystem s m itigation opportunities exist that m ay be tim ed to, for exam ple, are frequently cited as m eeting several of the criteria of ecologically periods of m inim al larval supply. or biologically significant areas (EBSAs) in areas beyond national Biodiversity offset frameworks do not yet exist for hydrotherm al jurisdiction and in need of protection (e.g., Ardron et al., 2009; systems and should be an area of active discussion and engagem ent Taranto et al., 2012). am ong stakeholders in the context of deep-sea m ining. In land- Marine protected areas that include hydrotherm al vents and based system s, offset benefits should accrue to the affected area that m anage hum an activities can im plem ent avoidance m easures (e.g., watershed) and should provide benefits in addition to any w ith obligatory com pliance (Van Dover et al., 2012). Establishm ent existing conservation value (McKenney and Kiesecker, 2010); such of netw orks of chem osynthetic ecosystem reserves as part of benefits could be challenging to develop in a deep-sea context. An m ining regulations has been recom m ended to the International alternative (or additional) offset fram ework has recently been Seabed Authority as a m easure to address issues of population proposed follow ing a polluter-pays principle that w ould fund deep- m aintenance and gene flow for system s w here m ineral extraction sea ecosystem reserves, research, and restoration (Barbier et al., or other hum an activities m ight put vent ecosystem s at risk (Van 2014). Dover et al., 2011, 2012). Such an approach is m odeled after the proposal for protection of Areas of Particular Environm ental In- 6. Su m m ary terest (APEIs) for m anganese nodule beds under the jurisdiction of the International Seabed Authority (Wedding et al., 2013). Hydrotherm al-vent ecosystem s have been hubs for scientific The potential for self-recruitm ent of populations at vents sug- activities since the m om ent of their discovery and they have been gests larval supply is at risk w here anthropogenic disturbance in- of com m ercial interest since alm ost the sam e m om ent because cludes rem oval of brood stock. In such cases, the local abundance of vents form m etal-rich sulfide deposits. For decades, scientific ac- eggs and larvae of vent invertebrates and suitable colonization tivities dom inated, occasionally resulting in readily apparent im - conditions w ould be dim inished. The scale of this im pact rem ains pacts over a localized area (i.e., w ithin a vent field). From this to be assessed for any hum an activity at the seabed, but m itigation scientific w ork, and especially from studies related to responses of m easures that protect brood stocks through avoidance m ay prove vent com m unities to a variety of natural disturbances, vent eco- to be an im portant m anagem ent tool. Because hydrotherm al vent systems are inferred to be am ong the m ost resilient ecosystem s in ecosystem s m ay prove to be relatively resilient to extractive ac- the deep sea. Despite this resilience, scientific and civil com m u- tivities, strategies that stagger hum an activities through both tim e nities have paid increasing attention to detrim ental im pacts of and space could reduce the likelihood and degree of cum ulative scientific sam pling and other activities on vent ecosystem s, im pacts w ithin a region. Such a tem poral strategy w ould require resulting in a code of conduct for scientific research and in C.L. 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