Waves cue distinct behaviors and differentiate transport of congeneric snail larvae from sheltered versus wavy habitats

Heidi L. Fuchsa,1, Gregory P. Gerbib, Elias J. Huntera, and Adam J. Christmana

aDepartment of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901; and bPhysics Department, Skidmore College, Saratoga Springs, NY 12866

Edited by M. A. R. Koehl, University of California, Berkeley, CA, and approved June 25, 2018 (received for review March 16, 2018)

Marine population dynamics often depend on dispersal of lar- out of estuaries (20). Turbulence-induced stronger swimming vae with infinitesimal odds of survival, creating selective pressure also enables larvae to continue moving upward even when fluid for larval behaviors that enhance transport to suitable habitats. rotation (vorticity) tilts them away from their normal gravita- One intriguing possibility is that larvae navigate using physical tional orientation (21, 22), which can otherwise lead to net signals dominating their natal environments. We tested whether sinking or trapping in shear layers (e.g., refs. 23–25). Although flow-induced larval behaviors vary with adults’ physical environ- many larvae respond to turbulence, little is known about larval ments, using congeneric snail larvae from the wavy continental responses to wave motions. Unlike turbulence, surface gravity shelf ( trivittata) and from turbulent inlets (Tritia obsoleta). waves have inherent directionality and can induce advection, Turbulence and flow rotation (vorticity) induced both to and upward swimming under waves may enable shoreward swim more energetically and descend more frequently. Accel- transport via Stokes drift (26–28). Some of these mecha- erations, the strongest signal from waves, induced a dramatic nisms could benefit species from multiple habitats, while others response in T. trivittata but almost no response in competent T. would most benefit species whose habitats have distinct physical obsoleta. Early stage T. obsoleta did react to accelerations, ruling characteristics. out differences in sensory capacities. Larvae likely distinguished Seascapes—including the open ocean, the continental shelf, turbulent vortices from wave oscillations using statocysts. Stato- inlets and estuaries, and surf zones—have different hydrody- cysts’ ability to sense acceleration would also enable detection of namic signatures reflecting geographic variation in the intensity low-frequency sound from wind and waves. T. trivittata poten- of turbulence and waves (29). Outside the surf zone, turbu- tially hear and react to waves that provide a clear signal over lence is strongest in shallow waters and near boundaries, whereas the continental shelf, whereas T. obsoleta effectively “go deaf” to waves are largest over open waters. Because ocean turbulence wave motions that are weak in inlets. Their contrasting responses and waves have different dynamics and forcing, turbulence pro- to waves would cause these larvae to move in opposite direc- duces larger spatial velocity gradients that deform or rotate the tions in the water columns of their respective adult habitats. fluid, including strain rate (γ) and vorticity (ξ), while waves can Simulations showed that the congeners’ transport patterns would produce larger accelerations (α). Large accelerations can also be diverge over the shelf, potentially reinforcing the separate bio- generated by strong turbulence in the surf zone and estuarine geographic ranges of these otherwise similar species. Responses to turbulence could enhance settlement but are unlikely to aid Significance large-scale navigation, whereas shelf species’ responses to waves may aid retention over the shelf via Stokes drift. Many marine populations grow and spread via larvae that dis- perse in ocean currents. Larvae can alter their physical trans- acceleration | flow sensing | larval transport | wave climates | veligers port by swimming vertically or sinking in response to envi- ronmental signals. However, it remains unknown whether any signals could enable larvae to navigate over large scales. We any bottom-dwelling species rely on planktonic larvae to studied larval responses to water motions in closely related Mmaintain population cycles and distributions (1–3), but snails, one from turbulent coastal inlets and one from the large dispersal distances (4) and high larval mortality (5) make wavy continental shelf. These two species reacted similarly to it difficult to predict how populations fluctuate and spread. turbulence but differently to waves, causing their transport As larvae are dispersed in ocean currents, environmental cues patterns to diverge in wavy, offshore regions. Contrasting can induce changes in vertical swimming or sinking speeds that responses to waves could enable these similar species to affect horizontal transport over tens to hundreds of kilometers maintain separate spatial distributions. Wave-induced behav- (6–9). Although larval motions affect both transport and set- iors provide evidence that larvae may detect waves as both tlement (10–13), it remains unknown whether behaviors have motions and sounds useful in navigation. only generic benefits or represent fine-tuned adaptations for

migration among specific habitats. This question is key to under- Author contributions: H.L.F. and G.P.G. designed research; H.L.F., G.P.G., and A.J.C. standing whether species’ viability is threatened by environmen- performed research; H.L.F. contributed new reagents/analytic tools; H.L.F. and E.J.H. tal changes that could impede larvae from reaching survivable analyzed data; and H.L.F. and G.P.G. wrote the paper. habitats. The authors declare no conflict of interest. Larvae could alter their transport among and within habi- This article is a PNAS Direct Submission. tats by responding to physical signals from turbulence or waves. Published under the PNAS license. Turbulence-induced sinking may promote local retention and Data deposition: The data reported in this paper have been deposited in the Biologi- reduce horizontal transport distances (4, 11, 14), enhance cal and Chemical Oceanography Data Management Office (BCO-DMO) database (https:// onshore transport via asymmetric mixing or surf zone processes doi.org/10.1575/1912/bco-dmo.739873). (15, 16), and raise settlement fluxes in shallow tidal environ- 1 To whom correspondence should be addressed. Email: [email protected] ments (17–19). In contrast, larvae that swim faster upward in This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. turbulence should be transported farther (11) and could coor- 1073/pnas.1804558115/-/DCSupplemental. dinate their response with other tidal signals to move into or Published online July 23, 2018.

E7532–E7540 | PNAS | vol. 115 | no. 32 www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Downloaded by guest on October 1, 2021 Downloaded by guest on October 1, 2021 hl gensaig etoso agrRgoa ca oeigSse RM)mdlgi ca shading). al. (cyan et grid Fuchs and model (ROMS) Wind System up-triangles). Modeling red Ocean trivittata, Regional ( T. larger (C shelf a near downward. continental of near shelf shell square) the sections Jersey and (blue shading) on New photos) Bay (green and Delaware the these shelf down-triangles) in on in red deployed circles) page , obsoleta buoy (blue the wave (T. a buoys of NJ from (out Hook, taken upward Sandy were directed of data wave is side landward velum the ciliated ( passively, on mudsnails oriented collected threeline are Bottom () larvae adult When and long. (Top) Larval (B) estuaries. 1. Fig. than flow sis potential as release statocysts although and that sensors, cilia capsules velar egg with benthic larvae produce planktonic species Both (41). B) (Tritia mudsnails formerly threeline trivittata, and larvae”) two “inlet obsoleta; of formerly obsoleta, behaviors (Tritia this larval mudsnails test species—Eastern flow-induced congeneric To compared habitats. adult we optimal hypothesis, their dominating signals ical could (29). wavy potentially areas and offshore accelerations environments nearshore and turbulent Larvae between vorticity (40). distinguish or component pres- motion strains a particle sensing both a of and has detection component induced which enable sure sound, accelerations also low-frequency could body tilting accelerations wave-generated, or body Sensing vorticity detect waves. by could turbulent tur- statocysts by with with associated induced rates larvae strain while large external bulence, with detect Larvae could 39). cilia (38, sensory equilib- accelerometers as function or could receptors that statocysts, rium ear, inner internal (36, human have the fluid also to surrounding larvae analogous crustacean the and of Mollusc deformations 37). by stretched cilia Appendix , or (SI beating bent velum by wing-like a swim and of larvae edge distinguish Mollusc the to around waves. mechanism sensory from a turbulence need would larvae natures, be to potential the and navigation. with larval shelf cues for used physical continental creating contrast the this habitats, intensify than among can organisms wavy aggregated and less ocean, are open reduce and inlets could turbulent and and estuaries more 35) Overall, (34, Reefs accelerations. waves (30–33). wave-generated attenuate energy also kinetic vegetation turbulent the and and of stresses (ε) turbulent rates raising kelp dissipation seabed, flow and the overlying coral, over and bivalves, drag seabed Aggregated increase the organisms. by where modified distinct sig- are physical more seascapes, be within may Moreover, nals (29). seascape values each co-occurring and in of gradients ranges velocity distinct spatial have result, typically domi- a accelerations are As motions. accelerations wave elsewhere by nated but layers, boundary bottom iia,teecneesocp daethbtt ihlittle with habitats adjacent occupy congeners these similar, ehpteie htlra epn eairlyt h phys- the to behaviorally respond larvae that hypothesized We sig- hydrodynamic their by seascapes different recognize To S2 rmtdlilt and inlets tidal from obsoleta) (T. mudsnails eastern Bottom) ( adult and ( Top) Larval (A) area. study of map and study this in compared Snails ;teeclaptnilycudsnesrisa hyare they as strains sense could potentially cilia these ); .obsoleta T. laas trivittata Ilyanassa .trivittata T. ave(2.Atog hi iehsoisare histories life their Although (42). larvae A B C aveaelre tmetamorpho- at larger are larvae seflra” Fg 1 (Fig. larvae”) “shelf ; .trivittata T. ouain.Mdlrslswr ae rmDlwr a ylo hdn)adcontinental and shading) (yellow Bay Delaware from taken were results Model populations. oisS1 Movies rmtecnietlsef Saebars: (Scale shelf. continental the from trivittata) T. A and .Ma etclvlcte eena zero near were sinking velocities gravitational vertical (|w Mean offset S2). to Table force Appendix, (SI enough about with upward rcino avesnigo iigadtepousv effort propulsive the and (see diving larvae or swimming sinking of larvae the in of changes proximate fraction the unequivocal, identified more swim- using we cues of tilting, downward behavior flow-induced combination and complex from propulsion, a size, sinking reflects body velocity passive making larval direction, separate Because ming. shellward to some the difficult had in it all force sank but propulsive either downward, estimated themselves larvae propelled Sinking/diving or required motion. was passively upward the effort propulsive grav- maintain reduced more offset to that which to such available axis, sinking, force itational by propulsive body moderated of the also component vertical was of velocity is, tilting Swimming that vorticity-induced flow. velocities, the behavioral to ultimately (downward) relative sinking, too negative gravitational used in offset sometimes resulting to but force upward lar- propulsive swim Swimming little to axis. attempted body pro- always the they vae to propelled if relative they swimming if downward, sinking/diving as themselves as larvae and direction upward classified and themselves we pelled strength so the propulsion, both of in changes proximate included (competent larvae largest the for (precompetent larvae smallest details). mech- motions sensory and S1 probable 1 fluid and (Table to used anisms signals reactions the larval pinpointing while quantified experiments Our Results signals these ocean. transport to coastal larval the reactions of in patterns Different different fundamentally vorticity. to lead or could strain acceleration, to to than than vorticity or rate that whereas strain expected to we responsive Thus, waves more 45). but (29, weaker be large (29, can are turbulence small where relatively shelf, continental inlets, are the coastal waves and in strong zones 44). is subtidal turbulence to where intertidal conditions. shallow oceanographic occupies distinct and (43) overlap .I tl ae,lra eryawy rple themselves propelled always nearly larvae water, still In ). b ≤ | .trivittata T. .obsoleta T. 0.04 .trivittata T. cm·s ie utdlyi eprwtr u to (up waters deeper in subtidally lives ouain n rmNtoa aaBo etr(NDBC) Center Buoy Data National from and populations −1 u eems oiie(pad o the for (upward) positive most were but ) ol emr epniet acceleration to responsive more be would is 1adS n Table and S2 and S1 Figs. Appendix, SI is S3–S10 Figs. Appendix, SI n otnegative most and obsoleta ) T. PNAS .Ratost flow to Reactions trivittata). T. ∼100 | . dl nisae12cm 1–2 are snails Adult µm.) o.115 vol. .obsoleta T. g aslswere capsules Egg ) | o 32 no. .obsoleta T. ∼80 o other for ol be would | )of m) E7533

ECOLOGY ENVIRONMENTAL SCIENCES Table 1. Predicted responses to experimental conditions, given the signal and sensor Response expected?

Couette device Rotating cylinder Shaker flask

Signal/sensor Horizontal Vertical Horizontal Vertical Horizontal Vertical Strains/cilia Yes Yes No No No No Vorticity/statocysts Yes No Yes No No No Acceleration/statocysts Maybe* Maybe* Maybe* Maybe* Yes Yes

*Centripetal acceleration is present but may be below the response threshold.

Responses to Turbulence-Generated Signals. Larvae of both species cues include strains in the surrounding fluid, sensed with velar reacted similarly to turbulence, cued primarily by flow-induced cilia, or flow-induced body tilting or acceleration, sensed with body rotation. In a grid-stirred tank, as dissipation rates the statocysts. To pinpoint the signals used, we exposed larvae to increased, larvae sank or dove more frequently, while upward- simpler flows applied in different directions (SI Appendix, Figs. swimming larvae propelled themselves with more force (Fig. 2 S1 and S2). Cilia or statocysts should sense strain rates or accel- A–F and SI Appendix, Fig. S3). We identified threshold dissipa- eration, respectively, regardless of the direction in which they tion rates inducing behavioral changes, but some behaviors were are applied, whereas statocysts would detect flow rotation when quite variable below the thresholds, suggesting that responses to it induces tilting (horizontal vorticity) but not when it induces turbulence were not cued directly by dissipation rate. Likelier spinning (vertical vorticity) (Table 1) (22). In strain-dominated

Tritia obsoleta Tritia obsoleta Tritia trivittata (precompetent) (competent) (competent) 20 A B C 10 or diving % sinking 0 2 D E F 1.5 force of swimmers propulsive normalized 1 −9 −7 −5 −3 −9 −7 −5 −3 −9 −7 −5 −3 10 10 10 10 10 10 10 10 10 10 10 10 dissipation rate (m2 s−3) 30 20 G H I 10 or diving % sinking 0 4 3 J K L 2 force of swimmers propulsive normalized 1 −1 0 1 −1 0 1 −1 0 1 10 10 10 10 10 10 10 10 10 | vorticity | (s−1)

40 (no response) 30 M N O 20

or diving 10 % sinking 0 40 P Q R 30 20

force of 10 swimmers propulsive normalized 0 −3 −2 −1 0 −3 −2 −1 0 −3 −2 −1 0 10 10 10 10 10 10 10 10 10 10 10 10 | acceleration | (m s−2)

Fig. 2. Proximate larval responses to turbulence, tilt-inducing vorticity, and waves. Included is the percentage of larvae sinking or diving (A–C, G–I, and M–O) and the propulsive force of swimming larvae normalized by the minimum value (D–F, J–L, and P–R) vs. dissipation rate ε in grid-stirred tank (A–F), vs. magnitude of tilt-inducing vorticity ξ in the cylinder rotating about a horizontal axis (G–L), and vs. magnitude of side-to-side acceleration α in shaker flask oscillating horizontally (M–R). Turbulence experiments produced large dissipation rates, strain rates, and vorticities, but accelerations were small; rotating- cylinder experiments produced large vorticities and moderate centripetal accelerations, but strain rates were negligible; shaker flask experiments produced linear wave motions with large accelerations, but vorticity and strain rate were negligible (SI Appendix, Fig. S2). Symbols are percentages or means ±1 SE of instantaneous observations within small bins (N = 100 except N = 300 in G, H, J, K) of ε, ξ, or α at larval locations. Solid lines are the fitted piecewise model, and vertical lines and shaded regions indicate threshold signal ±1 SE identified by piecewise model fit (SI Appendix, Table S3). For propulsive force, the model was fitted to log10(|Fv |)(SI Appendix, Figs. S3, S6, and S8); here the fitted |Fv | is normalized by minimum observed |Fv |, and when converted from log10 to linear scale, the linear model fit is curved.

E7534 | www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Fuchs et al. Downloaded by guest on October 1, 2021 Downloaded by guest on October 1, 2021 uh tal. process. et dominant Fuchs the to correspond type of boldface lines) in values (dashed upper effort and (blue), swimming waves or and (purple) lines) (dotted sinking/diving trivittata T. increased for (A, ( labels rates thresholds by Dissipation indicated larval (F as lines). Bay (W) and waves Delaware or histograms of (T) BBL (blue turbulence by data generated buoy are accelerations and generated; lines) and histograms (purple (A–F Bay Delaware of (A, rate dissipation 3. Fig. Although S9). Fig. , Appendix obsoleta (SI T. reactions variable more but lar competent and in in reaction reactions no strong almost induced water, negligible shallow competent and in signal S2 ) wave Fig. predom- inant the acceler- Appendix, accelerations, We linear horizontal (SI Large produced tilting. waves. vorticity flow-induced that little ocean flask but shaker under ations a common in accelerations reactions larvae their observed larger in diverged the they to turbulence, to similarly reacted Signals. Wave-Generated to Responses by sensed as tilting turbulence body statocysts. in vorticity-induced by Collec- observed solely (Couette reactions cued cylinder). be the rates could that (rotating strain indicate accelerations results large tively, moderate both and to that flow) unresponsive demonstrate cylinders were vertical the larvae accelera- in with centripetal results Negative moderate axis Appendix tions. produced vertical (SI orientations a vorticity cylinder about spin-inducing high rotation 2 only to (Fig. about unresponsive vorticity rotation tilt-inducing relatively to high strongly with and reacted axis cylin- species horizontal rotating both single a of a larvae but in S5 ), vorticity Moreover, der, Fig. spin-inducing vorticity. Appendix, high tilt-inducing (SI and low and axis rates vertical strain rates high a strain producing about the rotated high when unresponsive was both were device they producing axis but vorticity, horizontal S4), tilt-inducing a high Fig. about rotated Appendix, was (SI device of the when stages frequently both flow, Couette .Vria ceeain nue simi- induced accelerations Vertical S8). Fig. Appendix, SI ,btprecompetent but S6), Fig. Appendix, SI .Icue are Included Analysis). Data Environmental Methods: Appendix, (SI habitats snail in signals physical behavior-inducing of distributions Frequency .Fraclrtos etclr niaeaoetrsodsga ecnae soitdwt turbulence with associated percentages signal above-threshold indicate colors text accelerations, For (G–L). shelf continental Jersey New the on .trivittata T. ece iial otruec tbt tgs they stages, both at turbulence to similarly reacted D, ; and G, .obsoleta T. upehsorm n ywvseeyhr le(C, else everywhere waves by and histogram) purple ; n precompetent and J

,vriiyS (B, SD vorticity ), signal frequency

aia)adteNwJre otnna hl (G–L; shelf continental Jersey New the and habitat) BBL water column BBL water column 0.05 0.15 0.05 0.05 0.05 0.15 .obsoleta T. 0.1 0.1 0.1 0.1 10 10 0 0 0 0 .obsoleta T. −9 −9 J G D A dissipation rate(m 10 10 lhuhtetospecies two the Although −8 −8 10 10 E, −7 −7 .obsoleta T. 10 10 and H, avesn rdove or sank larvae −6 −6 ave(i.2 (Fig. larvae 10 10 .obsoleta T. .Both S7). Fig. , −5 −5 10 10 K ,adaclrto D(C, SD acceleration and ), −4 −4 2 34 % 10 10 77 % s 2 % 1 % ave but larvae, −3 −3 −3 ) 10 10 M were G–L −2 −2 K H E B –R NJ continentalshelf 10 10 Delaware Bay and I, vorticity (s −1 −1 hl.Atog ublnei ekro h hl hni h bay, the in than shelf the on weaker is turbulence Although shelf. to bot- up above the are and in signals to turbulence altered up where threshold greatly (BBL), distributed. layer be are boundary could larvae tom aver- most behavior on where larval weak depths of is However, range turbulence turbulence the (29), over strong layer age boundary generate surface on winds the and where in turbulence, shelf, in strong Both continental generate column. the tides water where the in Bay, be reactions Delaware rarely induce would to vorticity) adult enough and strong hosting rate (dissipation sites turbulence from two Jersey 1C), New the leta (Fig. frequently and Bay shelf how Delaware estimate continental we from signals, data To physical above-threshold 3). analyzed encounter species’ (Fig. would two larvae habitats the competent of shelf environments and physical inlet the to linked appear Motions. Fluid Environmental to Relevance waves intensities. to different responded dramatically hav- congeners with Despite the signals. capacities, these sensory to similar ing sensitive equally about are species Moreover, all for and body. values 2 threshold (Fig. the groups similar at of responses induced acceleration signals these wave-induced and tilting strong that provide results evidence Combined conditions. calm to (Fig. relative by vorticities 2R), increased highest the but at 2L) doubled roughly Competent force example, propulsive For age. turbulence. from with than waves motions wave trivittata T. to unresponsive became 10 10 lehsorm) ubr niaepretgso inl exceeding signals of percentages indicate Numbers histograms). blue L; 0 0 and F, .trivittata T. −1 and I, 10 10 ) epciey o ihrseis signals species, either For respectively. trivittata, T. 21 % 1 1 87 % 1 % 5 % C, 34% averatdmc oesrnl osgasfrom signals to strongly more much reacted larvae ntewtrclm (A–C column water the in L) F, 10 10 D, Tritia and I, aia) ausaecmue rmhdoyai model hydrodynamic from computed are Values habitat). 2 2 87% 10 10 and G, ftetm for time the of .obsoleta T. −4 −4 ,sgetn httetwo the that suggesting S3), Table Appendix, SI F C L I .Aclrtosaedmntdb ublnei the in turbulence by dominated are Accelerations L). p.saoyt es ohvorticity-induced both sense statocysts spp. acceleration (ms 10 10 ftetm for time the of T T J −3 ∼40× −3 n otcte (B, vorticities and ) T 10 10 −2 −2 W nDlwr a (A–F Bay Delaware in W W ttehgetaclrtos(Fig. accelerations highest the at 10 10 W −1 −1 .trivittata T. PNAS (<1 %) (<1 %) (10 %) 10 10 −2 T (1 %) 31 % 73 % 48 % 29 % .obsoleta T. ) 0 0 and | E, hs epne oflow to responses These o.115 vol. G–I .trivittata T. and H, n B (D–F BBL and ) nteNwJersey New the on n fcompetent of and ) nDlwr Bay Delaware in | K r turbulence are ) o 32 no. swimmers’ .obso- T. and | E7535 J–L)

ECOLOGY ENVIRONMENTAL SCIENCES dissipation rate and vorticity are highly specific cues of the BBL Table 2. Weighted mean behavioral vertical velocities Wb at both sites. (cm·s−1) of competent larvae by location Unlike dissipation rates or vorticity, accelerations can be large Delaware Bay New Jersey shelf in the water columns of both habitats, but only on the con- tinental shelf do they provide a specific signal (Fig. 3 C, F, Species WC BBL WC BBL I, and L). In Delaware Bay, wave-generated accelerations in T. obsolete −0.19 −0.11 −0.03 −0.06 the water column are similar to but weaker than turbulence- T. trivittata −0.04 −0.11 +0.08 −0.01 generated accelerations in the BBL, so larvae could not use accelerations to distinguish waves from turbulence. On the New WC, water column; BBL, bottom boundary layer. Values for natal habitat Jersey shelf, however, wave-generated accelerations in both the are in boldface type. water column and BBL average at least an order of magnitude higher than turbulence-generated accelerations in the BBL, giv- (Table 2). In the BBL, both species would have more negative ing accelerations high specificity as a signal of wave motions on vertical velocities in Delaware Bay than on the shelf. In the water the continental shelf. Competent T. obsoleta larvae may ignore column, larvae would reach extremes within their natal habitats: −1 accelerations, despite sensing them, because they provide no use- T. obsoleta sank at Wb = −0.19 cm·s in Delaware Bay, whereas T. −1 ful information in their natal inlets and estuaries, whereas T. trivittata swam up at Wb = 0.08 cm·s over the continental trivittata react strongly to accelerations that clearly signal wave shelf. While dispersing in the water columns of their respec- motions over their shelf habitats. tive habitats, these two species’ larvae would move vertically in We also assessed more specifically how competent larvae opposite directions. would behave in flows typical of their adult habitats (Fig. 4 and SI Appendix, Fig. S10). We used the physical data to define the Potential Impact on Larval Transport. Even when averaged at the typical ranges of co-occurring vorticity SD and acceleration SD species level, behavioral vertical velocities varied enough among in sites hosting adult T. obsoleta and T. trivittata, respectively. inlet and shelf larvae to generate important differences in lar- Typical signals for the two habitats had little overlap in either val vertical distributions at sea. We simulated larval distributions the water column or the BBL, because the New Jersey shelf gen- in 1D using the average flow-induced vertical velocities of com- erally had weaker turbulence and larger waves—and thus lower petent T. obsoleta or T. trivittata larvae (Fig. 4 C and D). We vorticities and higher accelerations—than Delaware Bay (Fig. 4 examined two model cases: one with strong BBL turbulence and A and B). We also combined data from multiple larval exper- no surface turbulence or waves, representative of inlets, and one iments to estimate the average instantaneous behaviors within with moderate BBL turbulence and surface wind-generated tur- bins of co-occurring vorticity and acceleration, the two strongest bulence and waves, representative of the continental shelf. Inlet physical cues (Fig. 4 C and D and SI Appendix, Fig. S10). Com- larvae (T. obsoleta) were most concentrated near the bottom bining the physical and behavioral data, we calculate a weighted in both flow conditions, whereas shelf larvae (T. trivittata) were mean behavioral velocity Wb for each species in each habitat distributed like T. obsoleta in inlet conditions but were more uni- formly distributed in shelf conditions (Fig. 5). This disparity was driven mainly by T. trivittata’s propensity to swim upward with intense effort in response to waves. In open waters, the observed larval responses to turbulence and waves would produce dissim- ilar vertical distributions, likely resulting in divergent transport patterns in the coastal ocean. Discussion In this study, larvae of two closely related species from adja- cent habitats—T. obsoleta from tidal inlets and estuaries and T. trivittata from the continental shelf—responded differently to physical signals associated with their contrasting environments. When competent to settle, both species reacted to turbulence or vorticity-dominated flow, but in weak turbulence, only shelf lar- vae reacted strongly to large accelerations associated with waves. Inlet larvae did react to accelerations before becoming compe- tent, confirming that T. obsoleta larvae could sense waves but grew unresponsive to them as they aged. Results also showed that inlet larvae either cannot sense flow deformation or react only when strain rates are higher than those typical of their adult Fig. 4. Observed physical signals in snail habitats and behaviors of com- petent larvae, with reference to signals typical of their adult habitats. (A environments (e.g., ref. 29). These experiments pinpoint stato- and B) Joint frequency distributions of vorticity SD and acceleration SD cysts as the likely flow sensor and demonstrate that larvae sense in Delaware Bay (A, T. obsoleta habitat) and on the New Jersey shelf (B, vorticity-induced body tilting and wave-induced body accelera- T. trivittata habitat). Shading indicates normalized frequency of signals in tion as separate signals, enabling larvae to differentiate between the upper 75% of the water column (SI Appendix, Methods: Environmen- turbulence and waves. Despite their similar sensory capacities, tal Data Analysis); black lines indicate theoretical signal range in isotropic competent T. obsoleta ignored wave motions, while T. trivittata turbulence. Colored polygons are convex hulls enclosing the 75% most fre- responded to them by swimming upward with a massive effort. quently co-occurring signals in the water column (solid lines) and benthic As a result, the two species’ larvae would move vertically in oppo- boundary layer (dashed lines) of Delaware Bay (orange; A and C) and the site directions in the water columns of their respective habitats. New Jersey shelf (red; B and D). (C and D) Mean behavioral vertical veloci- ties of competent larvae from inlets and estuaries (C, T. obsoleta) and from These contrasting behaviors enable insights into the potential the shelf (D, T. trivittata) across gradients of co-occurring turbulence- and use of turbulence and waves as signals for larval navigation in wave-generated signals. Instantaneous observations of larval velocity are enclosed vs. exposed physical environments. combined from multiple experiments and averaged over bins of instanta- neous acceleration and vorticity magnitude at larval locations. Colored lines Implications for Larval Navigation and Settlement. Our analysis of are as in A and B. water motions demonstrates that strong turbulence could be

E7536 | www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Fuchs et al. Downloaded by guest on October 1, 2021 Downloaded by guest on October 1, 2021 hl.A eteetce togtruec a ihspecificity high continental has the turbulence on strong than for cue, Bay would settlement Delaware a species of As shal- both BBL shelf. so in the currents, in intense faster tidal more sink stronger is with turbulence water near-bed lower habitat, fluxes either settlement raise in could 4 Fig. sinking and vorticity-induced 2 in Although (Table sank BBL species the does both with and turbulence associated seabed, conditions Strong the dispersal. of proximity during indicate water cue clearly 3 the a as in (Fig. turbulence reactions habitat of induce either to of enough Moreover, column high patterns. rarely transport is con- their vorticity inlet-dwelling differentiate 2 to their (Fig. turbulence as obsoleta) turbulence (T. to geners were the responsive trivittata) outside (T. as larvae and Shelf about calmer, species. near-shore deeper, most is of range which from shelf, species a continental in (44, behavior the intense flow-induced quantify from frequently we Here species is 48). 47, on turbulence where focused habitats studies poor near-shore near-shore earlier of a but indicator be large-scale (46), a would environments with hypothe- larvae but been provide has habitats to Turbulence sized both species. shelf in for cue cue navigational settlement useful a 4 Fig. in shown velocities vertical trivittata flow-induced mean and (T. on shelves based are continental tions estuaries of and (A) inlets typical tidal scenarios: more of two typical are most obsoleta Included waves, model. (T. no 1D with a turbulence by strong predicted as larvae petent 5. Fig. tosceryidct aemtosee nteBL(i.3 (Fig. al. et BBL Fuchs the in even acceler- motions large wave and indicate weaker, by clearly is ations generated turbulence 3 however, those (Fig. habitat, from column shelf water BBL the the in in In waves species. turbulence accelerations shelf by distinguish to by generated unable could be cue would potentially larvae navigational habitats, and a inlet shelf as continental used the be over signal distinct shelf of settlement erroneous more to larvae. leading potentially tats, nietruec,wv-eeae ceeain rvd a provide accelerations wave-generated turbulence, Unlike D. .obsoleta T.

etcldsrbtosrsligfo o-nue eairo com- of behavior flow-induced from resulting distributions Vertical depth (m) oeaetruec ihmdrt waves, moderate with turbulence moderate (B) and habitat), −5 −4 −3 −2 −1 −5 −4 −3 −2 −1 0 0 0 B A aiasbtlwseict for specificity low but habitats T. trivittata T. obsoleta fraction oflarvae(m 0.05 ,csigduto h s of use the on doubt casting A–L), B C and 0.1 and H F ,lmtn h value the limiting ), aia) oe predic- Model habitat). .Over ). −1 .trivittata T. 0.15 ) .obsoleta’s T. .trivittata’s T. C and habi- D). C I owtrat swimming study, water from this to switching In while sinking. even rel- to undergoing accelerations In steadily, low and 51). slowly atively and swim 38 veligers refs. snail (e.g., contrast, locomotion high-speed cephalopods equi- during dynamic and maintaining librium in aid fish, that detectors humans, acceleration marine have smallest including select the Megafauna could of that some . in characteristic abilities habitat acceleration-sensing defining for a as waves Sensing. light Acceleration of Implications Ecological similar otherwise help these of could species. distributions habitats, separate distinct slower pat- the in transport into reinforce processes to Different sinking physical seabed. by by the limited cued terns, near be currents could trans- landward whose inlets obsoleta), or natal (T. of larvae retention out inlet local of port of that mechanism of is from This waters differ drift 50). deeper would ref. Stokes to (e.g., ocean larvae where open of the surface loss the reducing The potentially near onshore, 49). them would (26, accelerations concentrate depth wave-generated help to at larvae flow shelf return of responses offshore-directed there although an surface, be the near can shoreward Over mainly (29). is drift large con- Stokes are where the waves shelf, over continental where inner substantial ocean the be open wave and could significant shelf drift hori- of tinental Stokes induces square larval orbitals the so wave to height, drift by proportional Stokes motion transport via nonlinear zontal waves gravity This surface 27). by (26, transported be to nism are turbulence, open wavy, not in patterns waves, waters. transport disparate to produce Responses to likely column. most higher water currents the faster-moving in occupying by whereas farther seabed, transported the near currents larvae moving 5). shelf (Fig. column whereas water the bottom, obsoleta in lar- distributed the evenly Inlet more near conditions: be vertical would flow concentrate larval shelf-like would cause in vae would diverge waves to 2), to distributions that (Table responses indicate simulations different water Our these motion. still upward in in resulting effort observed those whereas to similar velocities dra- competent induces obsoleta signal in This T. responses shelf. the different on only matically signal clear a provide and ols avecuddtc o nywv oin,btalso (≤ but frequencies infrasound motions, at experiments wave accelerations shaker only produced Our not sound. low-frequency detect wave-generated, could shelf larvae of mollusk indicative motions In wave waves. detecting not of habitats. for thresholds but suited acceleration predators oyster ideally lower of of thresholds the detection acceleration contrast, enable high may the signals, larvae these 3I in lap (Fig. shelf of tinental suction-feeding accelerations include generate of waves Predators accelerations generate processes. accel- that fish physical their Instead, preda- by or so control. generated motions tors motion accelerations, fluid exogenous be to body detect likely unrelated would larvae own appears and their sensing vorticity eration feel via (∼1 to changes higher unable orientational also feel (∼0.1 are Larvae dive thresholds actively acceleration that but veligers oyster estuarine of olds h ceeainratoso hl avepoieamecha- a provide larvae shelf of reactions acceleration The h bevdratost ceeain rvd vdnethat evidence provide accelerations to reactions observed The .Wvseiti ohhbtt,btteraccelerations their but habitats, both in exist Waves L). α ol ii hi oiotltasotb cuyn slow- occupying by transport horizontal their limit could .trivittata T. ≈ r nepnieadwudhv lgtynegative slightly have would and unresponsive are 0.1 α ≤ 20 m· 0.01 z hr idadwvsaesignificant are waves and wind where Hz) s −2 epn owvswt nes propulsive intense with waves to respond m·s eairlaclrtosaehge in higher are accelerations Behavioral . n e.2) ie h ako over- of lack the Given 29). ref. and −2 Tritia elblwterbhvo thresh- behavior their below well , p.lra ceeae relative accelerated larvae spp. PNAS 1m·s ∼0.01–1 .trivittata T. 1 m·s ∼1–10 | ≤ o.115 vol. 4 .trivittata T. z nterneof range the in Hz, aveaereleased, are larvae Tritia −2 u eut high- results Our −2 | Tritia 5,5) while 54), (53, vrtecon- the over o 32 no. m·s m·s p.larvae; spp. −2 −2 ol be could p.are spp. | (28). ) (52), ) E7537 T.

ECOLOGY ENVIRONMENTAL SCIENCES sound sources (55). Although sound in air is detected via pres- successive treatments. Each treatment included a 10-min spin-up period for sure waves, sound in water can also be detected as acceleration the flow to become stationary (statistically invariant in time) followed by of particles, including heavy internal particles such as otoliths 5–20 min of recording. Due to the difficulty of obtaining T. trivittata egg or statoliths (40, 56, 57). The latter mechanism enables adult capsules from the continental shelf, only a subset of experiments could be cephalopods to use their statocysts for detecting low-frequency done with T. trivittata (SI Appendix, Table S2). sound (40, 58) and may explain sound-induced changes in valve Image Processing and Analysis. Fluid and larvae move in different direc- gape of adult bivalves (59, 60). Sound has been hypothesized tions, so we first separated the PIV images of particles and larvae using to affect larval settlement behavior (61), but it was unknown techniques for two-phase flow (e.g., refs. 28, 48, and 68). Fluid velocities whether larvae have a hearing mechanism. Although we did not were computed from the particle images with larvae masked out, and lar- explicitly test for responses to sound, this study provides evi- val translational velocities were calculated from larval trajectories. Fluid dence that larvae have a sound-sensing capacity. Moreover, T. motion and larval translation differ due to swimming or sinking movement obsoleta larvae apparently “go deaf” to wave motions that pro- relative to flow outside the larval boundary layer. In the vertical (z) dimen- vide useful information only in T. trivittata’s shelf habitat. Larvae sion, wb = wo − wf , where wb is the instantaneous behavioral velocity, wf potentially detect infrasound only as a side effect of sensing is the instantaneous flow velocity, and wo is the instantaneous translational wave motions, but their observed reactions would differentiate (observed) velocity of an individual larva. The horizontal behavioral veloc- ities were computed similarly for ub in the x dimension. Trajectories had transport of Tritia spp. from adjacent habitats with distinct wave mean durations of ∼2 s in the weakest flow conditions down to ∼0.1 s climates. in the strongest flow conditions and were too short to analyze behavioral changes over time. Materials and Methods We used the PIV data to analyze larval swimming mechanics as a response Larvae of the mud snails T. obsoleta and T. trivittata were reared from egg to the instantaneous flow environments around individual larvae (22, 28, capsules. T. obsoleta egg capsules were collected from the intertidal zone 48). The relevant hydrodynamic signals are the dissipation rate ε, strain rate at Sandy Hook, NJ (May and June, 2012–2014) (Fig. 1C). T. trivittata egg γ, horizontal component of vorticity ξ, and fluid acceleration α. We cal- capsules were collected with a beam trawl from the R/V Arabella along the culated 2D approximations of these signals from fluid velocities and their 10-m isobath east of Great Bay, NJ (June 2013) and east of Atlantic City, gradients, interpolated in space and time to the larval observations. Approx- NJ (June 2014). Each batch of egg capsules hatched over ∼10 d, producing imations for ε varied among flow tanks (28, 48). We also calculated the daily cohorts of larvae that enabled us to replicate experiments using larvae instantaneous fluid forces on individual larvae. The product of larval mass of similar ages. Egg capsules and larvae were kept in aerated, 10-L buckets and acceleration is balanced by a vector sum of forces, including gravity, ◦ of 1-µm–filtered seawater at 20 C and 33 Sp (practical salinity) and were buoyancy, drag, Basset history forces, fluid acceleration, and the force that fed daily (105 cells·mL−1 Isochrysis galbana). larvae exert to propel themselves (appendix in ref. 28). Assuming larvae to Experiments were done with T. obsoleta larvae at 7–10 d old and with be spherical, we computed all terms except propulsive force from measured both species at 21–27 d old (SI Appendix, Table S2). Early stage exper- velocities, larval size, and density (48) and then solved the force balance iments were omitted for T. trivittata due to the difficulty of obtaining equation for the propulsive force vector Fv , which indicates the magni- their egg capsules. Following each experimental replicate, larvae were tude and Cartesian direction of larval swimming effort. The propulsion collected for measurements of shell length d and terminal sinking veloc- direction was corrected to larval coordinates by estimating the vorticity- ity wT , which were used to estimate larval specific density ρp (48). We induced larval tilt angle φ (48, 69), and larvae were classified as “swim- tested later stage larvae for metamorphic competency at the beginning ming” or “sinking/diving” if their propulsive force was directed upward of most replicates by placing larvae in a petri dish with sand from the (velum direction) or downward (shell direction), respectively, relative to the field site. Typically most larvae stopped swimming and began crawling in body axis. the substrate within 3–5 h, and 50–100% of the larvae metamorphosed To estimate threshold signals inducing changes in propulsive force and within 24 h. direction, we fitted the data with piecewise linear models, ( a , log (x) < log (x ) Experiments. Larvae were observed in turbulence (e.g., ref. 48) and in sim- y = 0 10 10 cr [1] pler flows dominated by strain, vorticity, or acceleration. Signals produced a1 + a2 log10(x), log10(x) ≥ log10(xcr ), by simpler flows lack the intermittency experienced by larvae in turbulence (a −a )/a (62) but enabled us to isolate the behavioral cues (e.g., refs. 22 and 28). where x is the signal (ε, γ, ξ, or α), xcr = 10 0 1 2 is the threshold sig- Turbulence experiments were done in a 170-L tank with two oscillating nal for a change in behavior, and y is the fitted behavioral characteristic

grids; paired grids produce large regions of relatively homogeneous, nearly [fraction of larvae swimming or log10(|Fv |) of swimming or sinking/diving isotropic turbulence between the grids (63). Strain-dominated experiments larvae]. This model assumes that behavior is constant below the threshold were done in a Couette device with an outer cylinder rotating around a sta- signal and changes linearly above the threshold. The piecewise model is tionary inner cylinder; this configuration produces laminar shear at Reynolds unbounded and does not account for physical limits on larval behavior, but numbers up to ≈2,000 (64). Vorticity-dominated experiments were done in this model is reasonable here because larval responses rarely appeared to a single rotating cylinder; at steady state, this device produces nearly shear- reach a limit within the tested signal range. Piecewise fits were omitted if a free, solid-body rotation (65). Acceleration-dominated experiments were linear fit was rejected (P < 0.05) or if no threshold could be identified within done in a 250-mL shaker flask subjected to rectilinear oscillations; water the data range. SEs of the estimated xcr were computed as described in SI in this flask moves as a solid body and has minimal deformation or vortic- Appendix, Methods: Standard Error of Threshold Estimates. ity except briefly during directional reversals (66). The three simpler flow devices were operated either vertically or horizontally to isolate the sens- Environmental Data. To assess the ecological relevance of observed larval ing mechanism (Table 1 and SI Appendix, Fig. S1). In each device, multiple behaviors, we analyzed turbulence- and wave-generated signals in each forcing frequencies were used so that larvae experienced a broad range species’ local habitat, as detailed in SI Appendix, Methods: Environmental of physical signals with intensities representative of most ocean regions (SI Data Analysis. Analyses are similar to those described by Fuchs and Gerbi Appendix, Table S1 and Fig. S2). (29). Data were taken from a numerical model and buoys in Delaware Bay All aspects of the experimental design, methods, and analyses have been and on the New Jersey continental shelf (Fig. 1C) at sites with documented described previously for experiments on oyster larvae (22, 28, 48). Experi- populations of T. obsoleta (Delaware Bay) and T. trivittata (New Jersey shelf) ◦ ments were done at 21 (±0.5) C and salinities of 33–35 Sp. In each device, (43). For each habitat, we computed the joint frequency distributions of vor- larvae were gently added (see SI Appendix, Table S1 for concentrations) ticity SD and acceleration SD in the upper 75% of the water column and in along with 105 cells·mL−1 algae (∼18 µm preserved Thalassiosira weiss- the bottom ∼1 m, assumed to be within the BBL. In each region and habi- flogii; Reed Mariculture) used as flow tracers. Movements of larvae and flow tat, we defined the typical signal range as the convex hull enclosing the 75% were measured simultaneously using 2D, infrared particle-image velocime- most frequently co-occurring vorticity SD and acceleration SD. try (PIV), which has become standard for observing plankton behavior (e.g., We used these typical signals with the laboratory observations to esti- refs. 48 and 67). Image sizes and locations varied among flow tanks (SI mate weighted mean behavioral velocities for each species in the water Appendix, Fig. S1). After an initial 10- to 20-min acclimation period, larvae column and BBL of each habitat. Instantaneous behavior observations were were observed in still water for 5 min, and then four or five flow treatments combined from three experiments (turbulence, cylinder rotating about a were applied in random order with ≥10 min of no oscillation between horizontal axis, and shaker oscillating horizontally) and averaged over small

E7538 | www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Fuchs et al. Downloaded by guest on October 1, 2021 Downloaded by guest on October 1, 2021 1 age L(03 osdrtosi siaiglra ipra itne from distances dispersal larval populations: estimating marine in in Considerations self-recruitment (2003) Predicting JL (2002) Largier al. 11. et S, Sponaugle 10. 2 cmnJ,Wre E rs F(94 oeln oeefcso eairo larval on behavior of effects some Modelling (1994) TF Gross FE, Werner JE, Eckman 12. 8 uh L ednahM 21)Bohsclcntanso pia ac egh for lengths patch optimal on a constraints Biophysical (2013) into MA Reidenbach HL, transport Fuchs larval turbulence-mediated 18. larval of Effects of (2007) LS simulations Mullineaux MG, Numerical Neubert HL, (2014) Fuchs al. 17. et AG, transport Fujimura horizontal 16. A transport: mixing Asymmetric (2001) PJS Franks JM, sim- Pringle of dispersal 15. the influences behavior swimming Vertical (2008) al. et EW, North Individual- 14. (2007) MG Hadfield JR, Koseff MA, Reidenbach JA, Strother MAR, Koehl 13. 0 ec M owr B r(01 lo ietasoto lecrab, blue of transport tide Flood (2001) Jr RB, Forward JM, Welch dis- the 20. on behavior swimming larval of Effects (2015) MA Reidenbach AB, Hubbard 19. 1 coadK 21)Eris iir wmigefcsvria rnpr fplanktonic of transport vertical effects swimming ciliary Earliest (2012) KA McDonald 21. 2 uh L hita J eb P utrE,De J(05 ietoa o sensing flow Directional (2015) FJ Diez EJ, Hunter GP, Gerbi AJ, Christman HL, Fuchs 22. 4 uhmW,KslrJ,SokrR(09 irpino etclmtlt yshear by motility vertical of Disruption (2009) R Stocker JO, Kessler WM, Durham 24. Andr PR, Jonsson 23. 5 lyT,Gr TW, Clay 25. eeisniiet h nta itiuin.Smltoslse ,adthe and d, 4 results lasted hours Simulations several distributions. initial after the but to distribution, larval insensitive vertical were uniform physical simulated a with had we (70) initially model larvae, particle-tracking of representative Lagrangian competent conditions 1D a of using distributions motions vertical affect Simulations. Distribution Larval water settlement. the before for behavior for those approximate Estimates whereas BBL dispersal, shelf). the during or behavior location (inlet mean each the habitat for approximate typical and column as BBL) above or defined bins column over (water taken is sum the and ity, p subscripts where magnitudes. is acceleration velocity vertical and mean vorticity weighted The instantaneous co-occurring of bins uh tal. et Fuchs .MtxsA anesM(09 uniyn h bo”cmoet nbiophysical in components “bio-” the local Quantifying (2009) and M abilities Saunders A, larval Metaxas environments, 9. Sensory (2002) Ch CB, Paris al. 8. et MJ, Kingsford life. larval 7. of phase dispersal the during locomotion and invertebrates. Behavior bottom (1995) marine CM Young of ecology 6. larval and revisited. Reproductive distance (1950) G dispersal Thorson and duration 5. larval Pelagic (2009) connectivity. AL population marine Shanks and 4. dispersal Larval (2009) S of Sponaugle determinant RK, Cowen leading A 3. rate: settlement Larval (1985) J Roughgarden S, geo- Gaines between exchange 2. genetic of means a as dispersal Larval (1971) RS Scheltema 1. ij stenraie on inlfrequency, signal joint normalized the is caorpi data. oceanographic mechanisms. and correlates Biophysical pitfalls. and Advances invertebrates: benthic Bull marine in transport larval of models connectivity. population on Effects self-recruitment. 249–278. Larvae pp Invertebrate Marine of Ecology Rev Biol 216:373–385. Sci Mar Rev Annu zone. intertidal marine the of USA community Sci ecological an in structure gastropods. marine benthic Bull shallow-water of populations separated graphically eteeti ubln onaylayer. boundary turbulent a in settlement eteeto efbidn bivalve. reef-building a of settlement currents. tidal in 1165. settlement and supply larval on behavior zone. flows. surf rip-channeled tidal in sediment and plankton of 46:381–391. sinking model for hydrodynamic mechanism and particle-tracking coupled flow: a wave-driven in bay. turbulent, Chesapeake larvae in oyster reefs ulated coral to inducer. settlement transport dissolved to larval responses Behavioral of model based otave eairlrsosst aiiyadturbulence. and salinity to responses Behavioral postlarvae: virginica. Crassostrea oyster eastern the 535:161–176. of settlement and persal mro ntruec n ha flow. shear and turbulence in embryos ypsieysal larvae. stable passively by rgesfraino hnpyolntnlayers. phytoplankton thin of formation triggers confinement. near-bottom for Evidence Ser flow: Prog boundary-layer Ecol flume a in larvae etcltasoto avlsn olr nserflow. shear in dollars sand larval of 1292. transport vertical 216:257–272. 140:284–322. 82:3707–3711. 25:1–45. rbnL,CwnR 20)Srn,sinn,o iigfo eft reef: to reef from diving or spinning, Surfing, (2007) RK Cowen LM, erubin ´ namD(00 opooyflwitrcin edt stage-selective to lead interactions Morphology-flow (2010) D unbaum ¨ 79:67–76. i ulMrSci Mar Bull a clPo Ser Prog Ecol Mar , ,Lneat 19)Simn eaiu fmrn bivalve marine of behaviour Swimming (1991) M Lindegarth C, e ´ 1:443–466. j niaebn fvriiyadaclrto,respectively, acceleration, and vorticity of bins indicate clAppl Ecol inlOceanogr Limnol x Biol Exp J 70:309–340. .obsoleta T. 13:S71–S89. W ocmaehwosre eair would behaviors observed how compare To b a clPo Ser Prog Ecol Mar 359:99–115. = 218:2782–2792. LSOne PLoS dMEwr CCPes oaRtn FL), Raton, Boca Press, (CRC L McEdward ed , Σ x Biol Exp J ulMrSci Mar Bull p Σ epSaRsPr II Part Res Deep-Sea ij 59:1434–1447. p w and ij b w ij 8:e71506. , Science b 215:141–151. .trivittata T. ij 70:341–375. sma avlvria veloc- vertical larval mean is 347:285–300. a clPo Ser Prog Ecol Mar 323:1067–1070. inlOceanogr Limnol a Biol Mar x Biol Exp J 41:185–208. aias Particles habitats. alnce sapidus, Callinectes a clPo Ser Prog Ecol Mar inlOceanogr Limnol 139:911–918. rcNt Acad Natl Proc 335:1–18. 213:1281– 52:1156– ilBull Biol Mar Biol Biol [2] 1 aNiaeP,BnsM,DAglsG,Aglk E(00 etblrhaigdis- heading Vestibular (2010) DE Angelaki GC, DeAngelis MS, Banks PR, MacNeilage 51. by driven flow cross-shelf of R Observations 50. (2008) J by Fredericks propulsion SJ, downward Lentz Active MR, larvae (2013) Fewings RA gastropod Guazzo 49. of EL, behavior Schmitt EJ, Sinking Hunter (2004) HL, Fuchs AR 48. Solow veliger the LS, in statocysts Mullineaux the HL, of study Fuchs structural Fine 47. (1981) LR Bickell R, Koss FS, Chia 46. Observations (2009) T Kukulka AJ, Plueddemann EA, Terray JH, Trowbridge tem- GP, and Gerbi turbulence 45. to responses Larval (2010) LS Mullineaux intertidal AR, Solow England HL, www.marinespecies. New Fuchs at Available 44. species. of marine of larvae Register World Pelagic (2017) WE (1965) Board 43. AH Scheltema and phylogeny RS, The (2016) Scheltema P 42. Bouchet P, Lozouet J, Utge N, Puillandre LA, Galindo 41. pealeii (Loligo squid longfin the by detection Sound (2010) al. et TA, Mooney develop- 40. bivalve in pediveliger the of significance Functional (1990) MR in Carriker systems receptor 39. equilibrium of diversity Morphological (1988) in BU activity ciliary Budelmann of control 38. Nervous (1976) C Thiriot-Quievreux CL, responses Singla mechanical GO, and Mackie electrical 37. of Correlation (1975) K Takahashi A, reefs. coral Murakami of Hydrodynamics 36. (2007) four SG by Monismith attenuation wave 35. of evaluation preliminary A reef. (1992) oyster JA an Cahalan over MS, turbulence Fonseca and Flow the 34. (2015) into R investigation Styles field 33. A (2007) J Grover SG, Monismith JR, Koseff layer JH, Boundary Rosman (2006) 32. A Genin G, Yahel JR, Koseff SG, Monismith MA, of Reidenbach Hydrodynamics (2002) 31. JR Koseff RJ, Lowe JH, Rosman JK, Thompson JP, Crimaldi wave-generated 30. sensing and turbulence- Hydrodynamic in variation (2015) Seascape-level (2016) FJ GP Gerbi Diez HL, AJ, Fuchs Christman 29. EJ, Hunter GP, and Gerbi rock western HL, scalars of Fuchs connectivity of and drift, transport 28. Stokes potential circulation, Ocean the (2011) al. on et M, note Feng A 27. (2004) DA Fong SG, Monismith 26. a aebo aa uyGaseadaoyosrveesprovided Chant). National J. and by reviewers R. Diez) and J. provided G.P.G., F. anonymous H.L.F., and was G.P.G., (to H.L.F., OCE-1756646 and (to Funding OCE-1060622 manuscript. Grassle Grants Foundation the mea- Science Judy on and data. comments cultures helpful buoy Delaware and Pirl the larval wave provided Chant Emily Chamberlin, and Robert Bay velocities. capsules. algal Shawna sinking and egg sizes maintained Pirl, larval collecting sured Chamberlin Emily in Shawna assistance Crum, and for Kevin Gonsenhauser Petrecca, Rachel Rose crew, ACKNOWLEDGMENTS. (70). al. et Ralston by described and as velocities behavioral mixing 4 their turbulent (Fig. by species determined each were locations of vertical larvae Particle behavioral competent particle deter- for the observed vary accelerations, to as used and velocities were waves, Vorticities and turbulence wind. from the mined with equilibrium assuming the using modeled was Turbulence had ·s m conditions (∼5–10 m winds Inlet (∼0.4 stratification. tides no moderate had with m·s deep (∼0.6 m tides strong 5 was domain model rmnto n estvt olna ceeaini edadwrdcoordinates. world and head in acceleration linear Neurosci to sensitivity and crimination larvae. shelf. continental inner the on winds cross-shelf turbulence. in larvae oyster turbulence. in obsoleta) (Ilyanassa nudibranch, the of larva transport. and Energetics layer: boundary surface ocean Oceanogr the gastropods? in turbulence dispersing of by selection Habitat inlet: tidal 68:153–188. a in perature 2017. 19, June Accessed VLIZ. at org III. gastropods ). (, revisited Evol the of systematics not and motion particle low-frequency pressure. to Sensitivity potentials: evoked auditory with 267–282. pp 1986 Edinburgh Yonge, Maurice ment. 757–782. pp York), New (Springer, WN Tavolga AN, Popper invertebrates. aquatic larvae. gastropod cilia. of control nervous in seagrass. of species transport. and hydrodynamics Res coastal Geophys on pyrifera) J (Macrocystis forest kelp a of effects reef. coral fringing a 1968. over structure flow and turbulence recruitment potential at events stress turbulent of sites. influence The settlement: larval plankton. by experienced signals hydrodynamic waves. and turbulence in larvae oyster by behavior and population. cygnus) (Panulirus lobster waves. surface by organisms hsJ ta.(04 aeidcdtasotadvria iigo eai gsand eggs pelagic of mixing vertical and transport Wave-induced (2014) al. et J, ohrs ¨ 99:337–353. inlOceanogr Limnol h iava–Poednso eoilSmoimi ooro i Charles Sir of Honour in Symposium Memorial a of Proceedings – Bivalvia The inlOceanogr Limnol 30:9084–9094. x Biol Exp J 39:1077–1096. 112:C02016. asru trivittatus. −1 ilBull Biol 213:3748–3759. surCatSefSci. Shelf Coast Estuar ae nosrain rmteMdAlni Bight. Mid-Atlantic the from observations on based ) −1 47:1137–1151. d tm ,FyRR, Fay J, Atema eds Animals, Aquatic of Biology Sensory etakCp.KnRm n the and Roma Ken Capt. thank We otnapulchra. Rostanga 59:1213–1227. Nature 151:182–199. ufc urns n owns hl conditions Shelf winds. no and currents) surface x Biol Exp J inlOceanogr Limnol ·s −1 dMro Hn ogUi rs,Hn Kong), Hong Press, Univ Kong (Hong B Morton ed , 257:48–49. inlOceanogr Limnol Hydrobiologia ufc urns n elsi,moderate realistic, and currents) surface 216:1458–1469. k a ihAutSci Aquat Fish J Can − 35:565–576. PNAS  elTsu Res Tissue Cell lsr,adwvswr modeled were waves and closure, 49:1214–1217. rg Oceanogr Progr hsOceanogr Phys J | 25:321–329. nuRvFudMech Fluid Rev Annu 49:1937–1948. o.115 vol. x Biol Exp J osa Res Coastal J inlOceanogr Limnol 214:67–80. 68:1182–1196. | 141:109–129. 38:2358–2378. 218:1419–1432. o 32 no. o Phylogenet Mol 31:978–985. / Arabella R/V 39:37–55. C a Res Mar J | 51:1956– studied ) and E7539 Phys J D). J

ECOLOGY ENVIRONMENTAL SCIENCES 52. Finelli CM, Wethey DM (2003) Behavior of oyster (Crassostrea virginica) larvae in 61. Lillis A, Eggleston DB, Bohnenstiehl DR (2013) Oyster larvae settle in response to flume boundary layer flows. Mar Biol 143:703–711. habitat-associated underwater sounds. PLoS One 8:e79337. 53. Higham TE, Day SW, Wainwright PC (2006) Multidimensional analysis of suction feed- 62. Pepper R, Jaffe JS, Variano E, Koehl MAR (2015) Zooplankton in flowing water ing performance in fishes: Fluid speed, acceleration, strike accuracy and the ingested near benthic communities encounter rapidly fluctuating velocity gradients and volume of water. J Exp Biol 209:2713–2725. accelerations. Mar Biol 162:1939–1954. 54. Holzman R, Collar DC, Day SW, Bishop KL, Wainwright PC (2008) Scaling of suction- 63. Shy SS, Tang CY, Fann SY (1997) A nearly isotropic turbulence generated by a pair of induced flows in bluegill: Morphological and kinematic predictors for the ontogeny vibrating grids. Exp Therm Fluid Sci 14:251–262. of feeding performance. J Exp Biol 211:2658–2668. 64. Coles D (1965) Transition in circular Couette flow. J. Fluid Mech 21:385–425. 55. Wenz GM (1962) Acoustic ambient noise in the ocean: Spectra and sources. J Acoust 65. Jackson GA (1994) Particle trajectories in a rotating cylinder: Implications for Soc Am 34:1936–1956. aggregation incubations. Deep Sea Res Part I 41:429–437. 56. Karlsen HE (1992) Infrasound sensitivity in the plaice (Pleuronectes platessa). J Exp 66. Kiørboe T, Saiz E, Visser A (1999) Hydrodynamic signal perception in the copepod Biol 171:173–187. Acartia tonsa. Mar Ecol Prog Ser 179:97–111. 57. Sand O, Karlsen HE (2000) Detection of infrasound and linear acceleration in fishes. 67. Catton KB, Webster DR, Brown J, Yen J (2007) Quantitative analysis of tethered and Philos Trans R Soc Lond B Biol Sci 355:1295–1298. free-swimming copepodid flow fields. J Exp Biol 210:299–310. 58. Packard A, Karlsen HE, Sand O (1990) Low frequency hearing in cephalopods. J Comp 68. Khalitov DA, Longmire EK (2002) Simultaneous two-phase PIV by two-parameter Physiol A 166:501–505. phase discrimination. Exp Fluids 32:252–268. 59. Roberts L, Cheesman S, Breithaupt T, Elliot M (2015) Sensitivity of the mussel Mytilus 69. Kessler JO (1986) The external dynamics of swimming micro-organisms. Prog Phycol edulis to substrate-borne vibration in relation to anthropogenically generated noise. Res 4:257–291. Mar Ecol Prog Ser 538:185–195. 70. Ralston DK, McGillicuddy DJ, Jr, Townsend DW (2007) Asynchronous vertical 60. Charifi M, Sow M, Ciret P, Benomar S, Massabau JC (2017) The sense of hearing in the migration and bimodal distribution of motile phytoplankton. J Plankton Res 29: Pacific oyster, Magallana gigas. PLoS One 12:e0185353. 803–821.

E7540 | www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Fuchs et al. Downloaded by guest on October 1, 2021