Downloaded by guest on September 25, 2021 www.pnas.org/cgi/doi/10.1073/pnas.1804558115 a Fuchs L. Heidi habitats wavy versus from sheltered larvae congeneric of differentiate transport and behaviors distinct cue Waves acceleration drift. Stokes via shelf aid the to over waves retention unlikely to aid responses are may ’ but shelf whereas settlement navigation, enhance large-scale Responses could species. bio- similar turbulence separate otherwise to the these habitats. reinforcing of adult potentially ranges geographic shelf, respective the direc- their over would opposite of patterns diverge transport in congeners’ columns the move that water showed to Simulations the larvae these in cause tions over responses would contrasting signal Their waves clear inlets. to in a weak are provide that motions that wave waves whereas to shelf, continental react the and waves. hear and tially of wind detection from enable also sound would low-frequency acceleration Stato- sense statocysts. to using ability distinguished oscillations cysts’ likely wave from Larvae vortices capacities. turbulent sensory in differences dramatic out a stage induced Early obsoleta. Accel- waves, frequently. from in more signal response strongest descend the to and species erations, energetically both more induced obsoleta). (vorticity) swim ( rotation inlets flow continental turbulent and wavy from Turbulence the and from trivittata ) (Tritia larvae shelf snail environ- congeneric physical using adults’ with ments, vary whether physical behaviors tested using We larval environments. navigate flow-induced natal larvae their habitats. that dominating suitable is signals to possibility transport intriguing enhance lar- One that of behaviors pressure 2018) selective dispersal larval 16, creating March survival, for on review of for odds depend (received infinitesimal 2018 with often 25, vae June dynamics approved and population CA, Berkeley, Marine California, of University Koehl, R. A. M. by Edited 12866 NY iaeterrsos ihohrtdlsgast oeit or into move to signals tidal coor- other in could with and upward response (11) faster environ- their farther swim tidal transported dinate that shallow be larvae in should enhance contrast, fluxes turbulence In settlement 14), (17–19). raise processes ments 11, zone and surf 16), (4, or mixing (15, asymmetric distances via and transport transport retention onshore local horizontal waves. promote or reduce turbulence may from sinking signals physical Turbulence-induced to responding by tats survivable reaching from larvae impede could habitats. environmen- that by changes threatened for tal is under- viability to adaptations key species’ is whether fine-tuned question standing This represent have habitats. specific behaviors or among set- migration whether benefits and unknown generic transport remains only both it affect kilometers (10–13), motions of tlement hundreds larval that to Although speeds tens sinking (6–9). over spread. or cues transport swimming and environmental horizontal vertical currents, affect fluctuate in ocean changes populations in induce dispersed can how make are predict (5) larvae mortality As to larval high difficult and it (4) distances dispersal large M eateto aieadCatlSine,RtesUiest,NwBusik J091 and 08901; NJ Brunswick, New University, Rutgers Sciences, Coastal and Marine of Department avecudatrtertasotaogadwti habi- within and among transport their alter could Larvae ananpplto ylsaddsrbtos(–) but (1–3), distributions and to larvae cycles planktonic population on maintain rely species bottom-dwelling any | .trivittata T. o sensing flow a,1 rgr .Gerbi P. Gregory , .obsoleta T. | u lotn epnei competent in response no almost but avltransport larval .obsoleta T. i ec oaclrtos ruling accelerations, to react did b la .Hunter J. Elias , | aeclimates wave fetvl g ef to deaf” “go effectively .trivittata T. | veligers a n dmJ Christman J. Adam and , poten- T. 1073/pnas.1804558115/-/DCSupplemental. at online information supporting contains article This 1 aadpsto:Tedt eotdi hspprhv endpstdi h Biologi- the in deposited (https:// been database (BCO-DMO) have Office paper doi.org/10.1575/1912/bco-dmo.739873 Management Data this Oceanography in Chemical and reported cal data The deposition: Data the under Published Submission. Direct PNAS a is article This interest. of E.J.H. conflict no A.J.C. and declare H.L.F. authors and paper. The the tools; G.P.G., wrote G.P.G. H.L.F., reagents/analytic and H.L.F. new research; and data; contributed analyzed designed H.L.F. G.P.G. research; and performed H.L.F. contributions: Author eeae ysrn ublnei h ufzn n estuarine and zone surf the in turbulence strong be also by can accelerations generated Large (α). the accelerations rotate larger (γ produce or rate deform strain that including pro- gradients fluid, turbulence velocity turbulence forcing, spatial ocean and larger turbu- dynamics Because duces different waters. zone, have open waves surf over and the largest whereas boundaries, are near Outside and waves waters (29). shallow in strongest waves is hydrody- lence intensity and the different turbulence in zones—have variation of geographic surf reflecting and signatures namic estuaries, and inlets mecha- these physical distinct of have habitats others Some whose characteristics. while shoreward species habitats, benefit (26–28). multiple enable most from would drift species may benefit could Stokes waves advection, nisms under via induce can swimming transport and gravity upward directionality surface and inherent turbulence, larval Unlike about have net known motions. waves is to Although wave little 23–25). to lead turbulence, refs. responses to otherwise (e.g., respond layers can larvae shear gravita- many in which normal trapping 22), or their sinking (21, from away orientation fluid when them tional even tilts upward swimming (vorticity) moving continue stronger rotation to Turbulence-induced larvae enables (20). also estuaries of out owo orsodnesol eadesd mi:[email protected] Email: addressed. be should correspondence whom To ospoieeiec htlra a eetwvsa both as waves navigation. in detect to useful may sounds larvae species and motions that similar evidence provide these behav- iors Wave-induced enable Contrasting distributions. spatial regions. could separate offshore maintain waves wavy, to transport in responses their diverge causing the to waves, from patterns to one to differently similarly and but reacted species turbulence inlets two These related coastal shelf. closely continental turbulent wavy in from motions We one water scales. , to large responses over navigate larval to envi- studied larvae to enable response could any in signals whether unknown sinking remains it trans- or However, physical signals. vertically ronmental their swimming alter can by Larvae port currents. dis- ocean that larvae in via perse spread and grow populations marine Many Significance esae—nldn h pnoen h otnna shelf, continental the ocean, open the Seascapes—including b a hsc eatet kdoeClee aaoaSprings, Saratoga College, Skidmore Department, Physics NSlicense. 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ENVIRONMENTAL ECOLOGY SCIENCES bottom boundary layers, but elsewhere accelerations are domi- overlap (43) and distinct oceanographic conditions. T. obsoleta nated by wave motions. As a result, spatial velocity gradients and occupies shallow intertidal to subtidal zones in coastal inlets, accelerations typically have distinct ranges of co-occurring values where turbulence is strong and waves are relatively small (29, in each seascape (29). Moreover, within seascapes, physical sig- 44). T. trivittata lives subtidally in deeper waters (up to ∼80 m) of nals may be more distinct where the seabed and overlying flow the continental shelf, where turbulence can be weaker but waves are modified by organisms. Aggregated bivalves, coral, and kelp are large (29, 45). Thus, we expected that T. obsoleta would be increase drag over the seabed, raising turbulent stresses and the more responsive to strain rate or vorticity than to acceleration, dissipation rates (ε) of turbulent kinetic energy (30–33). Reefs whereas T. trivittata would be more responsive to acceleration and vegetation also attenuate waves (34, 35) and could reduce than to strain or vorticity. Different reactions to these signals wave-generated accelerations. Overall, estuaries and inlets are could lead to fundamentally different patterns of larval transport more turbulent and less wavy than the continental shelf and in the coastal ocean. open ocean, and aggregated organisms can intensify this contrast among habitats, creating physical cues with the potential to be Results used for larval navigation. Our experiments quantified larval reactions to fluid motions To recognize different seascapes by their hydrodynamic sig- while pinpointing the signals used and probable sensory mech- natures, larvae would need a sensory mechanism to distinguish anisms (Table 1 and SI Appendix, Figs. S1 and S2 and Table turbulence from waves. Mollusc larvae swim by beating cilia S1). In still water, larvae nearly always propelled themselves around the edge of a wing-like velum (SI Appendix, Movies S1 upward with about enough force to offset gravitational sinking and S2); these cilia potentially could sense strains as they are (SI Appendix, Table S2). Mean vertical velocities were near zero −1 bent or stretched by deformations of the surrounding fluid (36, (|wb | ≤ 0.04 cm·s ) but were most positive (upward) for the 37). Mollusc and crustacean larvae also have internal statocysts, smallest larvae (precompetent T. obsoleta) and most negative analogous to the human inner ear, that could function as equilib- for the largest larvae (competent T. trivittata). Reactions to flow rium receptors or accelerometers (38, 39). Larvae with external included proximate changes in both the strength and direction sensory cilia could detect large strain rates associated with tur- of propulsion, so we classified larvae as swimming if they pro- bulence, while larvae with statocysts could detect body tilting pelled themselves upward and as sinking/diving if they propelled induced by turbulent vorticity or body accelerations induced themselves downward, relative to the body axis. Swimming lar- by waves. Sensing accelerations could also enable detection of vae always attempted to swim upward but sometimes used too wave-generated, low-frequency sound, which has both a pres- little propulsive force to offset gravitational sinking, ultimately sure component and a particle motion component (40). Larvae resulting in negative (downward) behavioral velocities, that is, sensing strains or vorticity and accelerations potentially could relative to the flow. Swimming velocity was also moderated by distinguish between turbulent nearshore environments and wavy vorticity-induced tilting of the body axis, which reduced the offshore areas (29). vertical component of propulsive force available to offset grav- We hypothesized that larvae respond behaviorally to the phys- itational sinking, such that more propulsive effort was required ical signals dominating their optimal adult habitats. To test this to maintain upward motion. Sinking/diving larvae either sank hypothesis, we compared flow-induced larval behaviors of two passively or propelled themselves downward, but all had some congeneric species—Eastern mudsnails (, formerly estimated propulsive force in the shellward direction, making obsoleta; “inlet larvae”) and threeline mudsnails (Tritia it difficult to separate passive sinking from downward swim- trivittata, formerly Ilyanassa trivittata; “shelf larvae”) (Fig. 1 A and ming. Because larval velocity reflects a complex combination of B) (41). Both species produce benthic egg capsules that release body size, propulsion, and flow-induced tilting, we identified the planktonic larvae with velar cilia and statocysts as potential flow behavior cues using more unequivocal, proximate changes in the sensors, although T. trivittata larvae are larger at metamorpho- fraction of larvae sinking or diving and the propulsive effort sis than T. obsoleta larvae (42). Although their life histories are of swimming larvae (see SI Appendix, Figs. S3–S10 for other similar, these congeners occupy adjacent habitats with little details).

A B C

Fig. 1. Snails compared in this study and map of study area. (A) Larval (Top) and adult (Bottom) eastern mudsnails (T. obsoleta) from tidal inlets and estuaries. (B) Larval (Top) and adult (Bottom) threeline mudsnails (T. trivittata) from the continental shelf. (Scale bars: ∼100 µm.) Adult snails are 1–2 cm long. When larvae are oriented passively, ciliated velum is directed upward (out of the page in these photos) and shell downward. (C) Egg capsules were collected on the landward side of Sandy Hook, NJ (T. obsoleta, red down-triangles) and on the continental shelf (T. trivittata, red up-triangles). Wind and wave data were taken from a wave buoy deployed in Delaware Bay (blue square) near T. obsoleta populations and from National Data Buoy Center (NDBC) buoys (blue circles) on the New Jersey shelf near T. trivittata populations. Model results were taken from Delaware Bay (yellow shading) and continental shelf (green shading) sections of a larger Regional Ocean Modeling System (ROMS) model grid (cyan shading).

2 of 9 | www.pnas.org/cgi/doi/10.1073/pnas.1804558115 Fuchs et al. Downloaded by guest on September 25, 2021 Downloaded by guest on September 25, 2021 uh tal. et Fuchs log log signal to threshold fitted indicate was regions model shaded the and lines vertical and model, .Smosaepretgso means or percentages are Symbols S2). Fig. Appendix, (SI negligible were (N produced rate experiments bins strain flask small shaker and rotating- within negligible; vorticity small; observations were but were rates instantaneous accelerations, accelerations strain of large but but with vorticities, accelerations, and motions centripetal moderate rates, wave and strain linear vorticities rates, large dissipation produced large experiments produced cylinder (D–F, experiments Turbulence value (M–R). minimum horizontally the oscillating by normalized vorticity larvae tilt-inducing swimming of of magnitude force propulsive the and M–O) 2. Fig. Likelier rate. dissipation by directly cued to not responses that were suggesting turbulence thresholds, were the behaviors below some variable but rates quite changes, behavioral 2 dissipation inducing (Fig. rates tion force as more upward- with while tank, A–F themselves frequently, propelled more grid-stirred larvae dove swimming or a sank larvae In flow-induced increased, by rotation. primarily cued body turbulence, to similarly reacted Signals. Turbulence-Generated to Responses 10 olna cl,telna oe ti curved. is fit model linear the scale, linear to and rxmt avlrsosst ublne itidcn otct,adwvs nlddi h ecnaeo avesnigo iig(A–C, diving or sinking larvae of percentage the is Included waves. and vorticity, tilt-inducing turbulence, to responses larval Proximate .W dnie hehl dissipa- threshold identified We S3). Fig. Appendix, SI ceeainsaoyt ab*Mye ab*Mye e Yes Yes Maybe* Maybe* Maybe* Maybe* Acceleration/statocysts al .Peitdrsosst xeietlcniin,gvntesga n sensor and signal the given conditions, experimental to responses Predicted 1. Table Cnrptlaclrto speetbtmyb eo h epnethreshold. response the below be may but present is acceleration *Centripetal Vorticity/statocysts Strains/cilia Signal/sensor 10 (|F normalized normalized v

;hr h fitted the here S8); and S6, S3, Figs. Appendix , (SI |) normalized propulsive propulsive propulsive force of ξ force of % sinking % sinking % sinking

,adv.mgiueo iet-ieacceleration side-to-side of magnitude vs. and (G–L), axis horizontal a about rotating cylinder the in force of swimmers or diving or diving swimmers or diving 1.5 10 20 30 10 20 10 20 30 40 10 20 30 40 swimmers 10 0 0 1 2 0 0 1 2 3 4 −9 P M J G D A 10 10 (precompetent) −1 10 Tritia obsoleta −3 aveo ohspecies both of Larvae −7 10 oiotlVria oiotlVria oiotlVertical Horizontal Vertical Horizontal Vertical Horizontal = 10 −2 0 except 100 10 e oYsN oNo No No No No No Yes No No Yes Yes Yes oet device Couette 10 0 −5 −1 10 10 10 0 1 −3 N = 0 in 300 10 .Frpousv force, propulsive For S3 ). Table Appendix, (SI fit model piecewise by identified SE ±1 −9 dissipation rate(m Q N K H E B 10 | acceleration(ms 10 −1 10 G, Tritia obsoleta (no response) −3 | vorticity(s (competent) −7 pnig(etclvriiy Tbe1 2) nstrain-dominated induces In it (22). when 1) not (Table but vorticity) vorticity) (vertical when (horizontal spinning they rotation tilting which flow induces detect in would it direction statocysts accel- whereas the or applied, rates of are strain regardless sense should respectively, Figs. statocysts Appendix, eration, or (SI Cilia S2). directions and different to S1 with larvae in exposed applied sensed we flows used, acceleration, signals simpler velar the or pinpoint with tilting To sensed statocysts. body the fluid, flow-induced surrounding or the cilia, in strains include cues H, 10 epneexpected? Response 10 −2 J, oaigcylinder Rotating 10 |F K 10 0 v −5 of ) | −1 snraie ymnmmobserved minimum by normalized is 10 10 10 −1 ε, 2 and J–L, ) 0 1 −3 ξ s −2 or , −3 ) ) α 10 s ispto rate dissipation vs. P–R) tlra oain.Sldlnsaetefitdpiecewise fitted the are lines Solid locations. larval at −9 R O L I F C 10 10 −1 −3 10 (competent) 10 −7 10 −2 hkrflask Shaker 10 0 10 −1 −5 10 10 0 1 10 |F ε −3 v ngi-tre ak(A–F tank grid-stirred in NSLts Articles Latest PNAS n hncnetdfrom converted when and |, α nsae flask shaker in and G–I, | SE ±1 f9 of 3 ,vs. ),

ENVIRONMENTAL ECOLOGY SCIENCES Couette flow, both stages of T. obsoleta larvae sank or dove became unresponsive to wave motions with age. Competent frequently when the device was rotated about a horizontal axis T. trivittata larvae reacted much more strongly to signals from (SI Appendix, Fig. S4), producing both high strain rates and waves than from turbulence. For example, T. trivittata swimmers’ high tilt-inducing vorticity, but they were unresponsive when the propulsive force roughly doubled at the highest vorticities (Fig. device was rotated about a vertical axis (SI Appendix, Fig. S5), 2L) but increased by ∼40× at the highest accelerations (Fig. producing high strain rates and high spin-inducing vorticity but 2R), relative to calm conditions. Combined results provide strong low tilt-inducing vorticity. Moreover, in a single rotating cylin- evidence that Tritia spp. statocysts sense both vorticity-induced der, larvae of both species reacted strongly to rotation about tilting and wave-induced acceleration of the body. Moreover, a horizontal axis with high tilt-inducing vorticity (Fig. 2 G–L these signals induced responses at similar threshold values for all and SI Appendix, Fig. S6), but precompetent T. obsoleta were groups (Fig. 2 and SI Appendix, Table S3), suggesting that the two relatively unresponsive to rotation about a vertical axis with species are about equally sensitive to these signals. Despite hav- only high spin-inducing vorticity (SI Appendix, Fig. S7). Both ing similar sensory capacities, the congeners responded to waves cylinder orientations produced moderate centripetal accelera- with dramatically different intensities. tions. Negative results in the vertical cylinders demonstrate that larvae were unresponsive to both large strain rates (Couette Relevance to Environmental Fluid Motions. These responses to flow flow) and moderate accelerations (rotating cylinder). Collec- appear linked to the physical environments of the two species’ tively, results indicate that the reactions observed in turbulence inlet and shelf habitats (Fig. 3). To estimate how frequently could be cued solely by vorticity-induced body tilting as sensed by competent larvae would encounter above-threshold signals, we statocysts. analyzed physical data from Delaware Bay and the New Jersey continental shelf (Fig. 1C), two sites hosting adult T. obso- Responses to Wave-Generated Signals. Although the two species leta and T. trivittata, respectively. For either species, signals reacted similarly to turbulence, they diverged in their reactions from turbulence (dissipation rate and vorticity) would rarely be to the larger accelerations common under ocean waves. We strong enough to induce reactions in the water column. Both in observed larvae in a shaker flask that produced linear acceler- Delaware Bay, where tides generate strong turbulence, and on ations but little vorticity (SI Appendix, Fig. S2) and negligible the continental shelf, where winds generate strong turbulence flow-induced tilting. Large horizontal accelerations, the predom- in the surface boundary layer (29), turbulence is weak on aver- inant wave signal in shallow water, induced strong reactions in age over the range of depths where most larvae are distributed. competent T. trivittata and precompetent T. obsoleta larvae, but However, larval behavior could be greatly altered in the bot- almost no reaction in competent T. obsoleta larvae (Fig. 2 M–R tom boundary layer (BBL), where turbulence signals are above and SI Appendix, Fig. S8). Vertical accelerations induced simi- threshold up to 87% of the time for T. obsoleta in Delaware Bay lar but more variable reactions (SI Appendix, Fig. S9). Although and up to 34% of the time for T. trivittata on the New Jersey T. obsoleta reacted similarly to turbulence at both stages, they shelf. Although turbulence is weaker on the shelf than in the bay,

Delaware Bay 0.1 A 1 % B 5 % C 29 % T W (<1 %) 0.05

water column 0 0.15 77 % 87 % 48 % D E F (1 %) 0.1 W T BBL 0.05 0 −9 −8 −7 −6 −5 −4 −3 −2 −1 0 1 2 −4 −3 −2 −1 0 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 NJ continental shelf 0.15 G 2 % H 1 % I 73 % signal frequency 0.1 W (<1 %) T 0.05

water column 0 0.1 34 % 21 % W 31 % J K L (10 %) 0.05 T BBL

0 −9 −8 −7 −6 −5 −4 −3 −2 −1 0 1 2 −4 −3 −2 −1 0 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 dissipation rate (m2 s−3) vorticity (s−1) acceleration (m s−2)

Fig. 3. Frequency distributions of behavior-inducing physical signals in snail habitats (SI Appendix, Methods: Environmental Data Analysis). Included are dissipation rate (A, D, G, and J), vorticity SD (B, E, H, and K), and acceleration SD (C, F, I, and L) in the water column (A–C and G–I) and BBL (D–F and J–L) of Delaware Bay (A–F; T. obsoleta habitat) and the New Jersey continental shelf (G–L; T. trivittata habitat). Values are computed from hydrodynamic model (purple histograms and lines) and buoy data (blue histograms and lines). Dissipation rates (A, D, G, and J) and vorticities (B, E, H, and K) are turbulence generated; accelerations are generated by turbulence (T) or waves (W) as indicated by labels (C, F, I, and L). Accelerations are dominated by turbulence in the BBL of Delaware Bay (F; purple histogram) and by waves everywhere else (C, I, and L; blue histograms). Numbers indicate percentages of signals exceeding larval thresholds for increased sinking/diving (dotted lines) or swimming effort (dashed lines) of T. obsoleta in Delaware Bay (A–F) and of competent T. trivittata on the New Jersey continental shelf (G–L). For accelerations, text colors indicate above-threshold signal percentages associated with turbulence (purple) and waves (blue), and upper values in boldface type correspond to the dominant process.

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ENVIRONMENTAL ECOLOGY SCIENCES Downloaded by guest on September 25, 2021 f9 of 6 tosceryidct aemtosee nteBL(i.3 (Fig. BBL 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 specificity tats, 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. 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

www.pnas.org/cgi/doi/10.1073/pnas.1804558115 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 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 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 at 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 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 h bevdratost ceeain rvd vdnethat evidence provide accelerations to reactions observed The mecha- a provide larvae shelf of reactions acceleration 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·s 0.01 z hr idadwvsaesignificant are waves and wind where Hz) −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. 1m·s ∼0.01–1 .trivittata T. 1 m ∼1–10 ≤ 4 .trivittata T. z nterneof range the in Hz, ·s aveaereleased, are larvae Tritia −2 u eut high- results Our −2 Tritia 5,5) while 54), (53, vrtecon- the over m·s m·s p.larvae; spp. −2 −2 uh tal. et Fuchs ol be could p.are spp. (28). ) (52), ) T. Downloaded by guest on September 25, 2021 aveo h u snails mud the of Larvae Methods and Materials sensing of differentiate effect climates. would reactions side observed of a transport their as but motions, only wave infrasound detect potentially in only evi- information Moreover, useful provides vide capacity. study sound-sensing this a obsoleta have sound, larvae to unknown that not responses was dence did for it we Although hypothesized test but mechanism. been explicitly hearing (61), a has behavior have Sound larvae settlement whether 60). larval (59, affect valve bivalves in to changes adult sound-induced adult of explain low-frequency may enables gape detecting and mechanism 58) for latter (40, statocysts sound otoliths their The use as 57). to such 56, cephalopods particles acceleration (40, as internal statoliths detected heavy or pres- be including via also can detected particles, water is of in air sound in waves, sound sure Although (55). sources sound eeapidi admodrwith treatments flow order (SI five or random tanks four larvae in then flow and period, applied min, among acclimation 5 20-min were for varied to water locations still 10- in initial and observed an were sizes After S1). Image Fig. 67). (e.g., Appendix, behavior and plankton observing 48 for standard refs. become velocime- has particle-image which infrared (PIV), 2D, try using simultaneously measured were flogii 10 (see with added Experi- along 48). gently 28, were (±0.5) (22, larvae 21 larvae at oyster done were on ments experiments for previously described (SI range regions broad S2). ocean Fig. a most and of experienced S1 representative Table larvae Appendix, intensities with that signals so physical used of sens- were the frequencies isolate flow to and forcing simpler 1 horizontally (Table vortic- three or mechanism or The vertically ing deformation (66). either minimal operated reversals has water were directional and oscillations; devices during body rectilinear briefly solid to a except as subjected ity moves flask flask shaker this were 250-mL in experiments a Acceleration-dominated shear- in nearly (65). done produces rotation device this solid-body state, steady free, at cylinder; rotating single a sta- Reynolds to a at up around shear laminar rotating numbers produces cylinder configuration outer this an cylinder; with inner device tionary Couette experiments oscillating a Strain-dominated in two 28). (63). done were grids nearly with and homogeneous, the 22 tank relatively between of refs. turbulence 170-L regions isotropic (e.g., large a produce cues in grids behavioral paired done grids; the were isolate experiments to turbulence in Turbulence us larvae enabled by experienced produced but intermittency Signals (62) the acceleration. lack or flows vorticity, simpler strain, by by dominated flows pler Experiments. the from sand 50–100% in and with crawling h, dish h. began 24 3–5 and petri within swimming within a stopped substrate beginning in larvae the the larvae most Typically at placing site. competency by field metamorphic replicates for most larvae of stage were later larvae tested exper- replicate, length stage shell experimental ity of Early each measurements S2). Following for Table collected capsules. Appendix, egg (SI for their old omitted d were 21–27 iments at species both buckets 10-L (10 aerated, daily in 20 fed kept at were seawater larvae 1-µm–filtered City, and larvae of using capsules Atlantic experiments Egg replicate of ages. to similar east over us of enabled hatched and that capsules larvae 2013) egg of (June of cohorts daily batch NJ Each Bay, 2014). Great (June NJ 1 of the (Fig. east from trawl 2012–2014) isobath beam 10-m June, a with and collected (May were NJ capsules Hook, Sandy at capsules. uh tal. et Fuchs l set fteeprmna ein ehd,adaaye aebeen have analyses and methods, design, experimental the of aspects All with done were Experiments w edMrclue sda o rcr.Mvmnso aveadflow and larvae of Movements tracers. flow as used Mariculture) Reed ; T hc eeue oetmt avlseicdensity specific larval estimate to used were which , .obsoleta T. aveaprnl g ef owv oin htpro- that motions wave to deaf” “go apparently larvae 5 avewr bevdi ublne(.. e.4)adi sim- in and 48) ref. (e.g., turbulence in observed were Larvae cells·mL 5 Tritia ,0 6) otct-oiae xeiet eedn in done were experiments Vorticity-dominated (64). ≈2,000 cells·mL g aslswr olce rmteitria zone intertidal the from collected were capsules egg p.fo daethbtt ihdsic wave distinct with habitats adjacent from spp. −1 −1 scrssgalbana). Isochrysis .obsoleta T. .trivittata T. la (∼18 algae .I ahdvc,multiple device, each In S1). Fig. Appendix, SI ◦ n aiiiso 33–35 of salinities and C al S1 Table Appendix, SI .obsoleta T. ◦ n 33 and C .trivittata T. and 0mno ooclainbetween oscillation no of min ≥10 u otedfclyo obtaining of difficulty the to due preserved µm .trivittata T. ftelra metamorphosed larvae the of S avea –0dodadwith and old d 7–10 at larvae d p patclslnt)adwere and salinity) (practical n emnlsnigveloc- sinking terminal and ssefhbtt Larvae habitat. shelf ’s / Arabella R/V eerae rmegg from reared were C hlsisr weiss- Thalassiosira o concentrations) for ). S 0d producing d, ∼10 p .trivittata T. nec device, each In . ρ p ln the along 4) We (48). egg T. ieto,w te h aawt icws iermodels, linear piecewise with data the fitted we direction, upward directed the to was relative respectively, axis. force direction), body (shell propulsive downward their or direction) vorticity- if (velum the “sinking/diving” propulsion estimating or The by angle ming” effort. coordinates tilt swimming larval larval to larval induced corrected balance of was force direction direction the vector Cartesian solved force and then propulsive tude and the (48) for density measured equation and from to size, force larvae propulsive larval Assuming except terms velocities, 28). all ref. computed gravity, in we that (appendix including spherical, force be themselves the forces, propel and of to acceleration, sum exert fluid larvae vector forces, mass history a larval Basset by of drag, buoyancy, balanced product The is larvae. acceleration individual and on forces fluid instantaneous their Approx- and observations. larval velocities for the fluid to imations time from and space signals in these interpolated gradients, of approximations 2D culated 28, rate (22, dissipation the larvae are γ individual signals hydrodynamic around relevant environments The 48). flow instantaneous the to behavioral analyze to short too were time. and over conditions changes flow strongest the in of veloc- durations for behavioral mean similarly horizontal computed The larva. were individual ities an of velocity (observed) and velocity, flow (z instantaneous vertical the the is In layer. boundary movement larval Fluid sion, sinking the or outside trajectories. swimming flow to larval to due relative lar- from differ translation and calculated velocities larval out, and using Fluid were masked motion 68). larvae larvae velocities with and and translational images 48, particles particle val 28, of the refs. from images (e.g., computed PIV were flow the two-phase separated for first techniques we so Analysis. tions, and Processing Image be could experiments of subset obtaining a of only with difficulty by shelf, done continental the followed the to time) from Due in capsules recording. invariant of (statistically min stationary for 5–20 become period to spin-up 10-min flow a the included treatment Each treatments. successive oiotlai,adsae siltn oiotly n vrgdoe small a over about averaged and rotating horizontally) oscillating cylinder shaker water and (turbulence, axis, the experiments horizontal were in observations three behavior species from Instantaneous each habitat. combined each for of BBL velocities and behavioral column mean weighted mate SD. 75% acceleration the and enclosing SD hull vorticity convex co-occurring the as frequently range most signal typical the defined we tat, 75% upper the bottom in vor- the SD of acceleration distributions and frequency joint SD the ticity computed we habitat, each For Bay (43). 1C Delaware (Fig. in shelf Gerbi buoys continental of and and populations Jersey model Fuchs New numerical the by a on described from and those taken to were Data similar each (29). are in Analyses in Analysis. signals detailed Data wave-generated as habitat, and local turbulence- species’ analyzed we behaviors, Data. Environmental Estimates. Threshold of Error estimated Standard the Methods: of Appendix, SEs a if range. omitted data were the fits to Piecewise (P appeared rejected range. was rarely signal fit tested responses linear the larval within is because but limit behavior, a here model larval reach reasonable on piecewise limits is The physical model for threshold. this account threshold the not the does above and below linearly unbounded constant changes is behavior and that signal assumes model log This or larvae]. swimming and larvae behavior, of in [fraction change a for nal where oiotlcmoeto vorticity of component horizontal , oetmt hehl inl nuigcagsi rpliefreand force propulsive in changes inducing signals threshold estimate To response a as mechanics swimming larval analyze to data PIV the used We eue hs yia inl ihtelbrtr bevtost esti- to observations laboratory the with signals typical these used We w x b = stesga (ε, signal the is .trivittata T. w ,asmdt ewti h B.I ahrgo n habi- and region each In BBL. the within be to assumed m, ∼1 o ε − .obsoleta T. y aidaogflwtns(8 8.W locluae the calculated also We 48). (28, tanks flow among varied w = f where , ( ntewaetflwcniin onto down conditions flow weakest the in s ∼2 oass h clgclrlvneo bevdlarval observed of relevance ecological the assess To a a ). S2 Table Appendix, (SI 0 1 , + < γ φ Dlwr a)and Bay) (Delaware a 5 ri otrsodcudb dnie within identified be could threshold no if or 0.05) , 2 w ξ 4,6) n avewr lsie s“swim- as classified were larvae and 69), (48, log or , b steisatnosbhvoa velocity, behavioral instantaneous the is 10 li n avemv ndfeetdirec- different in move larvae and Fluid α), (x u y ,log ), b 10 IApni,Mtos Environmental Methods: Appendix, SI x stefitdbhvoa characteristic behavioral fitted the is x nthe in cr (|F ξ w cr log n udacceleration fluid and , = o v eecmue sdsrbdin described as computed were fsimn rsinking/diving or swimming of |) steisatnostranslational instantaneous the is 10 10 10 F v (x (x (a x hc niae h magni- the indicates which , .trivittata T. 0 ) ) −a ieso.Taetre had Trajectories dimension. < ≥ NSLts Articles Latest PNAS ftewtrclm n in and column water the of tstswt documented with sites at ) log log 1 )/a 10 10 2 (x (x stetrsodsig- threshold the is cr cr NwJre shelf) Jersey (New ) ), .trivittata T. tanrate strain ε, ecal- We α. dimen- ) | s ∼0.1 f9 of 7 egg w [1] SI f

ENVIRONMENTAL ECOLOGY SCIENCES bins of co-occurring instantaneous vorticity and acceleration magnitudes. model domain was 5 m deep with no stratification. Inlet conditions had The weighted mean vertical velocity is strong tides (∼0.6 m·s−1 surface currents) and no winds. Shelf conditions had moderate tides (∼0.4 m·s−1 surface currents) and realistic, moderate Σp w −1 ij bij winds (∼5–10 m·s ) based on observations from the Mid-Atlantic Bight. Wb = , [2] Σpij Turbulence was modeled using the k −  closure, and waves were modeled assuming equilibrium with the wind. Vorticities and accelerations, deter- where subscripts i, j indicate bins of vorticity and acceleration, respectively, mined from turbulence and waves, were used to vary the particle behavioral p is the normalized joint signal frequency, w is mean larval vertical veloc- velocities as observed for competent larvae of each species (Fig. 4 C and D). ij bij ity, and the sum is taken over bins defined above as typical for each location Particle vertical locations were determined by their behavioral velocities and (water column or BBL) and habitat (inlet or shelf). Estimates for the water turbulent mixing as described by Ralston et al. (70). column approximate the mean behavior during dispersal, whereas those for the BBL approximate behavior before settlement. ACKNOWLEDGMENTS. We thank Capt. Ken Roma and the R/V Arabella crew, Rose Petrecca, Kevin Crum, Emily Pirl, Shawna Chamberlin, and Larval Distribution Simulations. To compare how observed behaviors would Rachel Gonsenhauser for assistance in collecting egg capsules. Emily Pirl and Shawna Chamberlin maintained algal and larval cultures and mea- affect vertical distributions of competent larvae, we simulated larval sured larval sizes and sinking velocities. Robert Chant provided the Delaware motions using a 1D Lagrangian particle-tracking model (70) with physical Bay wave buoy data. Judy Grassle and anonymous reviewers provided conditions representative of T. obsoleta and T. trivittata habitats. Particles helpful comments on the manuscript. Funding was provided by National initially had a uniform vertical distribution, but after several hours results Science Foundation Grants OCE-1060622 (to H.L.F., G.P.G., and F. J. Diez) and were insensitive to the initial distributions. Simulations lasted 4 d, and the OCE-1756646 (to H.L.F., G.P.G., and R. J. Chant).

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