Scaling Marine Fish Movement Behavior from Individuals to Populations

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Article: Griffiths, C.A., Patterson, T.A., Blanchard, J. et al. (4 more authors) (2018) Scaling marine fish movement behavior from individuals to populations. Ecology and Evolution, 8 (14). pp. 7031-7043. ISSN 2045-7758 https://doi.org/10.1002/ece3.4223

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Received November | Revised February | Accepted March DOI: 10.1002/ece3.4223

ORIGINAL RESEARCH

Scaling marine fish movement behavior from individuals to populations

1Schoo of Mathematics and Statistics University of Sheffied Sheffied Abstract UK Understanding how where and when animas move is a centra probem in marine 2 Institute for Marine and Antarctic ecoogy and conservation Key to improving our knowedge about what drives anima Studies University of Tasmania Hobart TAS Austraia movement is the rising depoyment of teemetry devices on a range of free roaming 3Centre for Environment Fisheries and species An increasingy popuar way of gaining meaningfu inference from an ani Aquacuture Science Lowestoft Laboratory mas recorded movements is the appication of hidden Markov modes HMMs Lowestoft UK 4CSIRO Marine and Atmospheric Research which aow for the identification of atent behaviora states in the movement paths Hobart TAS Austraia of individuas However the use of HMMs to expore the popuation eve conse 5 Department of Bioogy University of York quences of movement is often imited by mode compexity and insufficient sampe York UK sizes Here we introduce an aternative approach to current practices and provide Correspondence evidence of how the incusion of prior information in mode structure can simpify the Christopher A Griffiths Schoo of Mathematics and Statistics University of appication of HMMs to mutipe anima movement paths with two cear benefits a Sheffied Sheffied UK consistent state aocation and b increases in effective sampe size To demonstrate Emai cagriffithssheffiedacuk the utiity of our approach we appy HMMs and adapted HMMs to over muti Funding information variate movement paths consisting of conditionay dependent daiy horizonta and Natura Environment Research Counci GrantAward Number NEL vertica movements in two species of demersa fish Atantic cod Gadus morhua; n and European paice Pleuronectes platessa; n We identify atent states corresponding to two main underying behaviors resident and migrating As our ana ysis considers a reativey arge sampe size and states are aocated consistenty we use coective mode output to investigate state dependent spatiotempora trends at the individua and popuation eves In particuar we show how both species shift their movement behaviors on a seasona basis and demonstrate popuation space use patterns that are consistent with previous individua eve studies Tagging studies are increasingy being used to inform stock assessment modes spatia management strategies and monitoring of marine fish popuations Our approach provides a prom ising way of adding vaue to tagging studies because inferences about movement behavior can be gained from a arger proportion of datasets making tagging studies more reevant to management and more cost effective

This is an open access artice under the terms of the Creative Commons Attribution License which permits use distribution and reproduction in any medium provided the origina work is propery cited The Authors Ecology and Evolution pubished by John Wiey Sons Ltd

Ecology and Evolution. 2018;8:7031–7043. www.ecolevol.org | 7031 | GRIFFITHS ET AL.

KEYWORDS Atantic cod data storage tags European paice hidden Markov modeing movement behavior popuationeve patterns priors

|INTRODUCTION Kranstauber et a it woud appear that the most viabe route toward robust popuation eve inferences is approaches that The spatia management of the marine word requires in depth in make the most of the tagging data we aready have formation about how animas move when they move and where Among the many methodoogica deveopments that utiize they move to Key to increasing our understanding of species space movement data to answer ecoogica questions hidden Markov use movement patterns and how individuas interact with the en modes HMMs and hidden semiMarkov modes have taken cen vironment they inhabit is the rising depoyment of sma and rei ter stage eg DeRuiter et a McKear Langrock Waters abe data oggers and transmitters on free roaming marine animas Keser Micheot Langrock Patterson Towner et Costa Breed Robinson Hays et a Hussey et a a Favored because they match our initiative understanding Capabe of recording a range of movement metrics incuding that movement is governed by switches in an animas motivation horizonta and vertica movement aongside basic environmenta in Patterson et a HMMs provide a computationay efficient formation such as water temperature sainity and ambient dayight means of objectivey cassifying movement into discrete states with these devices have revoutionized our understanding of fundamen different statistica properties indicating differences in underying ta ecoogy Hussey et a documented oceanwide dispersa behavior Langrock et a events Bock et a highighted areas that are essentia for HMMs have been fitted to mutipe individua pathways simu species surviva Raymond et a and even aowed us to test taneousy in both the frequentist Langrock et a McKear the effectiveness of current conservation poicies Pittman et a et a and Bayesian statistica paradigms Jonsen Scott et a McCintock et a However these approaches are typicay One of the main motivations for anima borne teemetry studies impemented by speciaist statisticians and require the couping of is that by understanding individua movement behavior we might HMM and hierarchica structures producing a hierarchica Hidden infer the popuation species and community eve consequences Markov mode HHMM The aternative is the use of HMMs or other of movement Bock et a Hinde et a Raymond et a state space approaches that fit on an individua by individua basis Wakefied et a This is especiay true in marine sys Jonsen Myers James Micheot et a This atter tems as individua observations provide our ony insight into the more frequenty used approach has its advantages the most notabe otherwise unobservabe Achieving this scaing of inference from being an ease of use for statisticians and bioogists aike Fitting per individua movement patterns to popuation dynamics requires two individua aso has its disadvantages The first is that it requires indi important components The first is an adequate sampe size num vidua movement paths that are suitaby data rich to achieve mode ber of individuas to address the ecoogica question of interest convergence imposing even stricter restrictions on sampe size The Hebbewhite Haydon and second a statistica means by second is a distinct ack of any forma process by which state one in which we gain meaningfu inference at the individua and popua anima A is ensured consistency with state one in anima B This ack tion eve from a finite sampe of individuas Jonsen Langrock of consistency means that estimated parameters can readiy inform et a McCintock Russe Matthiopouos King individua eve movement studies but wi resut in tricky interspe The issue of sampe size has been extensivey discussed espe cific and intraspecific comparisons imiting a researchers abiity to ciay when considering how movement studies can inform marine ask post hoc popuation eve questions of their data conservation and spatia management Hebbewhite Haydon Our objective is to introduce an aternative framework that uses McGowan et a Nguyen et a Ogburn et a HMMs to overcome the described imitations of individuay fitted Tags can be expensive McGowan et a are iabe to HMMs whie maintaining their heraded ease of use advantages Our occasiona faiure or oss and often resut in individua pathways approach combines an N state HMM and severa hierarchica struc that are data poor or have a ow number of observations As a re tures but bypasses the need to integrate over the random effects sut meeting the minimum sampe size of individuas when as in HHMMs Langrock et a by using information we gain making simpe statistica comparisons between popuations is un from our data rich pathways as a priori approximations of each states common Hebbewhite Haydon with even greater num movement parameters Doing so not ony aows us to achieve co bers needed when testing for the effects of age sex and species herent individua and popuation eve state cassification but aso identity Lindberg Waker In the absence of a coabora ensures that we maximize our sampe size by gaining meaningfu in tive effort across mutipe institutions Bock et a Hinde ference from our data poor and data rich movement paths et a a significant increase in funding or a communitywide To iustrate our approach we appy it to a rea ecoogica prob shift to data sharing eg via onine data repositories ike Movebank emquantifying seasona space use patterns in Atantic cod Gadus GRIFFITHS ET AL. | morhua and European paice Pleuronectes platessa in the North Sea and June Fish were broady separated into substocks based on and Engish Channe Both Atantic cod and European paice have reease ocation see Figure and dispayed considerabe variation significant commercia and conservation vaue and as a resut have in movement path duration Supporting information Tabe S been the subject of severa ong term tagging programs Hobson Each DST was programmed to record depth m at min in Righton Metcafe Hays Hunter Metcafe Arnod tervas for the duration of depoyment The first weeks and the Reynods Hunter Metcafe OBrien Arnod Reynods ast day of every time series were excuded to remove any errone Righton Metcafe Connoy Drawing on this the ous or irreguar measurements associated with reease and recap rest of this paper considers a case study of individua bivari ture events as per Hobson et a For detais of tag type fish ate movement paths many of which n have imited observa catchment tag impantation and measurement accuracy see Righton tions andor ack cear bioogica signas Our findings demonstrate et a Gadus morhua or Hunter Metcafe Arnod et a cear spatiotempora patterns in the movement behavior of either Pleuronectes platessa species that are consistent with individua eve studies Hobson Each movement path is a bivariate time series of horizonta and et a Hunter Metcafe Arnod et a Hunter vertica movement per day Net vertica movement mday of each Metcafe OBrien et a Neat et a Furthermore by fish was taken directy from the raw DST data by cacuating the anayzing a reativey arge dataset we provide a unique insight into absoute difference between corresponding min depth measure how differing substocks of cod and paice shift their behavior on a ments and summing the vaues for each day at iberty Horizonta seasona basis with cear consequences for fisheries management movement mday in comparison was inferred indirecty from the and conservation depth data in a two step approach First daiy geoocation estimates were produced via a FokkerPanck based method that combines Metcafe and Arnods tida ocation method and a Bayesian |MATERIALS AND METHODS state space mode see Pedersen Righton Thygesen Andersen Madsen for mode detais The straightine distance between |Case study data daiy geographic estimates commony referred to as step ength Movement paths were taken directy from the depoyment of data was then cacuated using the Great Circe equation Both vertica storage tags DSTs on free roaming fish in the North Sea or Engish v and horizonta h movement metrics were og natura og trans Channe The dataset incudes individuas from two species of formed prior to mode impementation Ony time series that were European demersa fish Atantic cod n and European paice onger than days and had compete depth recordings were used n A fish were tagged and reeased between December in this study For descriptions of horizonta and vertica movement in

FIGURE Reease ocations of a tagged fish Atantic cod Gadus morhua n are shown in red fish are either separated into the Engish Channe substock trianges n or the southern North Sea substock circes n European paice Pleuronectes platessa n are shown in purpe fish are grouped into three substocks Centra North Sea circes n German Bight trianges n and Southern North Sea crosses n | GRIFFITHS ET AL.

Atantic cod and European paice see Hunter Metcafe Arnod et a agorithm Zucchini MacDonad Langrock Framing the Hunter Metcafe OBrien et a and Hobson et a mode in this way enabes us to conduct parameter estimation using a Bayesian approach by numericay maximizing the posterior density The cassification probabiity of each state at t is then de termined using the backward smoothing agorithm Zucchini et a |The mode More detais for how the efficient HMM machinery can be Previous individua eve studies demonstrate that Atantic cod and used to conduct statistica inference are given in Zucchini et a European paice dispay periods of high activity whie in the water for the particuar case of anima movement modeing see coumn punctuated by periods of reativey ow activity whie on the Patterson et a For our case study we used the R optimiza seabed Metcafe Hunter Buckey Righton et a tion routine optim to numericay maximize the og posterior density Thus we consider a discrete state HMM We abe state one as State aocation is carried out by seecting the most ikey state at resident R representing periods of time with ow movement each time point separatey rates We abe state two as migrating M representing a much Periods of reative inactivity ow h and v movement rates can more active phase where movement rates in the horizonta and persist for months in either species Metcafe et a vertica dimension are greaty increased As in a attempts to infer Righton et a To accommodate this persistence within state behavior from movement observations state abes must be inter we have imposed a prior penaty term on the transition probabiities preted with care as they provide simpified proxies of unobserved such that behaviora modes not direct equivaents Patterson et a γ11 ∼β(α,β) For a movement path of ength T it is assumed that an under and ying nonobserved state sequence S1 ST taking vaues in R M} describes the persistence within and stochastic switching between γ22 ∼β( ,β) states The time varying evoution of this state process takes the where α and β This prior termed hereafter as the transition form of a first order Markov chain with transition probabiity ma probabiity prior is designed to ensure that states R and M corre trix Γ spond to strong seasona shifts in movement behavior and not day

γR→R γR→M to day fuctuations Γ= γM→R γM→M and |Cassifying fish movements γj→k = Pr (St+1 = k St = j) We appy the mode described in section to a individ for any j k in R M Given a state j at time t the observation xt is ua movement paths such that each fish gets its own parameter assumed to be drawn from a mutivariate norma distribution MVN set Each parameter set consists of estimated parameters

xt ∼ MVN μj,Σj two transition probabiities and sets of parameters describ with ing the mean μj and covariance Σj of each state A tota num ber of days Atantic cod days European paice μjH μj = days were considered As expected the resuting state μ V j sequences are predominatey made up of two ceary defined and behaviora modes one more active and one ess active see

2 Supporting information Figures S and S for exampe output σ ρ σ σ jH j jH jV Σj = 2 However the parameters describing the numerica structure of ρ σ σ σ j jH jV jV these modes showed great variation among fish with no cear and H and V represent movements made in the horizonta and ver consistency Moreover a handfu of movement paths faied to tica dimension respectivey Thus the compete data ikeihood achieve mode convergence as an upper threshod of observa S S given a state sequence 1 T is tions is needed for robust parameter estimation Patterson Basson Bravington Gunn ωS ϕS x1 γS →S ϕS x2 …γS →S ϕS xT 1 1 1 2 2 T−1 T T To avoid the wastefu remova of vauabe data or a tedious post where the row vector ω is the Markov chain initia state probabiity hoc description of the individua variation that exists in the HMMs

which we assume to be uniform at t = and ϕj refers to the muti output we adopted an aternative approach Based on the seection variate norma density stated in equation We aow distinct pa criteria outined in Supporting information Figure S we seect rameters for each fish indexed by i = and write these as mode output from fish Atantic cod n European paice i i i Γ μj and Σj. n spread eveny across the five substocks Supporting informa In practice standard HMM agorithms aow us to cacuate the tion Tabe S We then cacuate summary statistics means m and actua ikeihood when the states are unobserved very efficienty variances δ that describe the numerica structure of the two states by integrating over a possibe state sequences using the forward Supporting information Figure S These summary statistics are GRIFFITHS ET AL. |

FIGURE Estimated state dependent distributions bars for vertica eft and horizonta right movements of a seected fish Back ines iustrate the movement parameter prior distributions N (m, ) that were constructed based on coective mode output Prior distributions are state resident soid ine migratory dashed ine species Atantic cod top European paice bottom and dimension horizonta or vertica specific

used to construct Gaussian distributions Figure N (m, ) where m states are across mutipe fish Supporting information Figure S and and δ are dimension h or v d state j and species specific given the differences between mode fit for one of the data poor movement seected sampe These informative distributions per species paths are provided Supporting information Figure S termed hereafter as priors on the modes movement parameters A HMMs were coded and impemented in R R Deveopment are then introduced directy into the HMMs ikeihood function such Core Team see Supporting Information document for ex that Equation is mutipied by ampe code A pots were generated using the ggplot2 Wickham ϕ(μ m ,δ ) and ggmap Kahe Wickham packages in R R jd jd jd j d Deveopment Core Team Bathymetric data was samped where ϕ m δ is the Gaussian density with mean m and vari from the Genera Bathymetric Chart of the Oceans onine repository ance δ Thus our informative priors act to constrain the mean pa GEBCO wwwgebconet which is a goba topographic data rameters of each state during the cassification process set with a oneminute spatia resoution This adapted approach is appied to the cassification of the re maining individua pathways Atantic cod n European paice |Prior sensitivity anaysis n outputting state sequences that comprise comparabe states across a fish This enabes post hoc comparisons to be made at the in When imposing prior distributions in statistica modes it is aways dividua and popuation eve with reative ease For an exampe of how important to test what infuence those priors have on the modes prior incusion infuences the cassification process see Supporting in predictions in our case the modes estimated state sequences formation Figure S Furthermore demonstrations of how comparabe To test the sensitivity of our mode to changes in the transition | GRIFFITHS ET AL. probabiity prior we varied the α and β vaues that characterize the October and ocations cassified to a migrating state between priors beta distribution and reran the HMM for a seected November and May were used In European paice ocations cas fish In test α β we sti expect a behaviora switch sified to a resident state between Apri and September and oca to occur at an order of every days However we approximatey tions cassified to a migrating state between October and March doube our priors variance In test α β the expected rate were used of switching is haved To test the modes sensitivity to changes in the movement pa |RESULTS rameter priors we varied the variances δs that describe the spread of each state and reran the adapted HMM for randomy seected |Individua fish movement fish from each species In test A we increased a δ vaues by re fecting a prior expectation of greater variabiity between the param Mapping the posterior probabiity of being in a particuar state in eters of individua fish and in test B we decreased a δ vaues by dicated that individua fish from either species switch between pe refecting an expectation of reduced variabiity During a reruns of riods of highy directed movement when in a migratory state and the adapted HMM Test A and Test B the state transition prior is kept periods of random and highy ocaized movements when in the ess constant therefore ensuring that any change in state is a direct con active resident state Figure Time spent in either state and the sequence of the changes to the modes movement parameter prior transitions between states were shown to vary in space and time and can be inked to certain habitats For exampe cod spent days JuneNovember consecutivey in the resident state within |Univariate modeing the deeper waters of the Cetic Sea and ony shifted into a migratory To assess the advantages of using bivariate responses state when transiting through the Engish Channe In comparison we aso carried out an anaysis using a univariate obser paice undertook ong distance directed movements after its vation mode considering ony movements made in the reease in the German Bight spending days consecutivey in the horizonta dimension The same mode for transition prob migrating state before switching to the resident state in the shaow abiities is used as described above We appy this approach waters of the Centra North Sea to the fish Atantic cod n European paice n The majority of individua time series had observations that previousy characterized as data rich movement paths shifted between resident and migratory states n Atantic cod Reported comparisons refect the percentage change if any in n European paice However a sma number of individuas the resutant state sequences for each individua fish n persisted in a singe state for the duration of their time se ries one European paice and four Atantic cod remained in a resi dent state throughout whereas the movements of one Atantic cod |Inferring popuation patterns were consistenty cassified to the migratory state A singe state As popuation dynamics emerge as the sum of the individuas that movement paths had short duration times average movement path comprise the popuation we used individua movement behaviors duration days and were reeased throughout the year to expore spatiotempora patterns Annua tempora patterns of NovemberMay movement behavior were cacuated for each species in two ways First the daiy individua probabiities of each fish being in each state |Popuation patterns were averaged across a individuas and over each week of the year Second the proportion of fish cassified to each state was cacuated The mean probabiity of observing a resident state and the pro by averaging the daiy number of fish in each state and smoothing portion of observations cassified to a resident state varied it again to the weeky time step Week refers to weeks of the year throughout the year Figure In both species migratory behavior starting on the st January and ending on the st December and is dominated throughout the winter and into spring with the onset independent of year of summer signifying a shift in movement behavior to the resident Patterns of space use whie in either state were quantified state This shift in state occurred earier in European paice than in using utiization distributions Kie et a Wombe Gende Atantic cod with movements of paice having a higher probabiity Worton For each species and substock utiization of cassification to the sower ess active resident state between distributions were cacuated by pooing a daiy horizonta geoo ate Apri and September compared to June through to November cations for specified time periods and spatiay binning them into in cod km2 grid ces Maxwe et a Wombe Gende The mode predicted arge variation in average movement rates Specified time periods were state dependent and based on a within each state Tabe Horizonta movement rates of paice tagged weeky averaged probabiity of observing a given state across a and reeased in the Southern North Sea and German Bight were sig individuas exceeding Successive weeks cassified to the same nificanty ower than those tagged in the Centra North Sea resident behaviora state were then grouped In Atantic cod this meant Students t test p migrating Students t test p In ocations that were cassified to a resident state between June the resident state paice from the Southern North Sea and German GRIFFITHS ET AL. |

Bight moved on average kmday horizontay and between and priors resuted in a percentage change in state that was on average mday verticay compared to kmday horizontay and be in cod and in paice Such findings demonstrate that the tween and mday verticay in the migratory state In com precise detais of these priors are not crucia with state cassifica parison paice tagged in the Centra North Sea exhibited much higher tions and bioogicay important resuts being robust to fairy arge horizonta movement rates moving on average and kmday in changes in prior parameters the resident and migratory states respectivey Predicted spatia utiization distributions showed that migration oc |Distribution of state dwe times curred throughout the spatia domain with no cear concentration of migratory activity in either species Figure Supporting information In an HMM the ength of time that an individua spends in one state Figure S In comparison periods of time spent in a resident state pro before switching to the other necessariy foows a geometric distri duced cear geographic patches of space use whie in certain habitats bution Pooing across individuas we find that these distributions These habitats varied with species Figure and substock Supporting are indeed geometric see Supporting information Figures S and information Figure S however Southern North Sea cod and paice S and so the dynamics of the fitted changes in state are consist both aggregated in the coasta waters off the Engish mainand Cod in ent with the Markov nature of the mode Further mode assessment the Engish Channe shift to a resident state when in the western mouth is provided by residua pots in Supporting information Figure S of the Channe In the German Bight of paice spent most of their and S time at iberty within the area dispaying itte or no dispersa Of those paice tagged in the Centra North Sea were estimated to be in |Comparison to univariate modeing the resident state within the Northern North Sea whie a further fish undertook southern migrations before shifting to a resident mode State aocation was found to be different across the two tested ob in the shaow waters of the Centra North Sea servation modes The bivariate mode resuted in state sequences that differed from the univariate mode in and of cases in Atantic cod and European paice respectivey This resut con |Prior sensitivity anaysis firms the need for the bivariate anaysis Minima change in the cassification of states was found dur ing prior sensitivity anaysis Supporting information Tabe S Rerunning the HMM with changes to the transition probabiity |DISCUSSION prior reveaed an average percentage change in state across a individuas of in cod and in paice In comparison rerun One of the main objectives of anima movement studies is the sca ning the adapted HMM with changes to the movement parameters ing of inference about movement behaviors from individuas to

FIGURE State dependent movement behavior of two individua fish Shown in a coor scae from red to yeow is the movement behavior of one Atantic cod tagged on the March duration days Red points represent a migrating state yeow a resident state and those points shown in orange iustrate times when the mode was uncertain of state cassification ie the daiy probabiity of state cassification was Shown in a scae from purpe to cyan is the movement behavior of one European paice tagged on the November duration days Purpe points represent a migrating state cyan a resident state and those points shown in roya bue iustrate times when the mode was uncertain of state cassification The start point and end point of each individuas movement path are shown as a green triange and a red diamond respectivey | GRIFFITHS ET AL.

FIGURE Annua tempora distributions of the resident state in Atantic cod red and European paice bue The potted ine in either graph iustrates the mean probabiity of observing a resident state SEgray shading The underying barpots demonstrate the proportion of individua fish that are in a resident state during each week Periods of time when the mean probabiity of observing a resident state is continuay are iustrated in either species

TABLE State dependent movement Resident state Migrating state rates horizonta kmday vertica mday Horizonta Vertical Horizonta Vertical by substock in Atantic cod and European Substock movement km movement m movement km movement m paice

Atantic cod Gadus morhua) Southern 31.5 158.3 North Sea Engish 53.5 13.4 125.4 Channe European paice Pleuronectes platessa Southern 6.4 20.0 115.6 North Sea German Bight 6.6 26.1 125.8 Centra North 26.2 121.0 Sea

Note A vaues are taken from coated mode output and are averaged across a individuas GRIFFITHS ET AL. |

FIGURE Annua state dependent space use patterns of Atantic cod a b and European paice c d in the North Sea and Engish Channe Pots are spit into periods of resident dominant a c and migrating dominant b d defined by a mean probabiity of observing a given state at a given time being A grid ces km2 are iustrated in a coor gradient so as to iustrate the sum tota number of days spent in a certain state in a given grid ce within a specified time period

popuations Bock et a Hays et a Hinde et a behaviors are identified consistenty across mutipe individuas Raymond et a Wakefied et a HMMs McKear et a Here we have achieved this consistency by borrowing information Micheot et a Patterson et a or their Bayesian from a finite sampe of individuas and using it to provide our mode equivaents Jonsen et a McCintock et a provide a with data driven approximations of each state Using this nove ex powerfu way of achieving this objective but ony when movement tension to HMM methodoogy we investigated spatia and tempora | GRIFFITHS ET AL. shifts in movement behavior from a arge sampe size of bivariate paice Hunter Metcafe Arnod et a Hunter Metcafe movement pathways We demonstrated where and when shifts be OBrien Arnod and Reynods noting strong seasona de tween two ecoogicay meaningfu states are most ikey to occur pendence in the movement patterns of individua fish Here we add and add further confidence to observations of seasona dependence confidence to these findings by providing a mechanistic view of in the movements of commerciay important demersa fish Our how fish switch between two movement modes during their annua bioogica findings compement and advance current understanding cyce In particuar we show that cod and paice are more ikey to oc and highight how our approach has significant utiity in the fieds of cupy a resident state during the summer months ApriSeptember movement ecoogy and conservation in paice JuneNovember in cod These periods are dominated by Our approach to behavior cassification has two major advan ow horizonta and vertica movement rates therefore our findings tages First it enabed us to gain meaningfu inference from support the hypothesis that both species spend their summer in a of the dataset additiona movement pathways many of which are sedentary state with minima activity eves Metcafe et a data poor and woud otherwise be subject to post hoc remova This Righton et a Movement rates then ramp up during the win retention of a individua eve information is favorabe because it ter and eary spring OctoberMarch in paice DecemberMay in maximized our sampe size and ends more information to our ana cod resuting in a coective shift in state As in previous studies ysis Second our approach ensures that state abes are aocated Hobson et a Hunter et a b we interpret this shift to consistenty across mutipe individuas without resorting to arge be refective of prespawning migrations the onset of spawning and increases in mode compexity As a direct consequence of these two subsequent postspawning migrations One imitation of the two advantages we were abe to ask popuation eve post hoc questions state mode considered here is that we cannot directy infer foraging of our movement data and provide answers that are meaningfu for or spawning behavior Foraging and spawning events are ikey to conservation and spatia management represent an immediate activity eve with both behaviors invoving Studies that cassify behavior based on horizonta and verti notabe vertica dispacement to and from the water coumn Hobson ca movements are rare but see Breed Bowen Leonard et a The incusion of a third immediate state woud be a re Bestey Jonsen Hinde Harcourt Gaes DeRuiter et a ativey straightforward extension to mode structure see Vermard

Here we have assumed that ht and vt are conditionay depen Rivot Mahvas Marcha Gascue Pee Good dent given atent states which is a nove addition to the movement Micheot et a for exampes of HMMs that consider states ecoogy iterature Our reasons for doing so are inked to a priori in However it is unikey that the scae of these vertica excursions is formation about how the species of interest ater their activity eves arge enough to aow cassification at the daiy time step Therefore within an annua cyce Hobson et a However we intuitivey we suggest that future studies either depoy more sophisticated tags expect other species occupying three dimensiona environments to which are capabe of recording more refined information about the exhibit simiar degrees of couping For exampe Bestey et a underying movement process eg acceerometers Leos Barajas revea that the directed horizonta movements in mutipe Antarctic Photopouou et a or consider a nested hierarchica HMMs in pinniped species are associated with onger dive durations whereas which vertica and horizonta movements are recorded and cassified an inverted reationship is noted in bue whaes Balaenoptera muscu- at differing time scaes Leos Barajas Gangoff et a lus with perceived shaow foraging behaviors being characterized Over the ast years andings data for the North Sea and by shaow dives and short horizonta movements DeRuiter et a Engish Channe demonstrate that catch per unit effort CPUE for Future studies may find simiar observation modes a power demersa species is higher during the summer months Righton fu too for investigating the dependences of horizonta and vertica Townhi Van Der Kooij Such increases in CPUE are un movement rates Carter Bennett Embing Hosegood Russe doubtedy inked to changes in the popuations underying move ment behavior as time spent on the seabed resuts in an increased Our estimates of average movement rates are consistent with vunerabiity to commercia expoitation Righton et a By previous work In cod horizonta movement rates whie in the migra assuming that time spent in a resident state is inked to sea bottom tory state are shown to be approximatey kmday which is com dweing we show that cod and paice aggregate in certain habitat parabe to past observations Hobson et a and aboratory types For exampe cod in the Engish Channe have greatest density studies Bainbridge Videer Warde In paice previ in the deeper waters at the western mouth of the Engish Channe ous research reports that seven tagged individuas swam on average In contrast cod and paice in the Southern North Sea aggregate in km during prespawning migrations Hunter Metcafe coasta waters off the Engish mainand We aso demonstrate that Reynods Assuming an average migration time of weeks paice in the German Bight remain excusivey within this region sug as noted in Hunter et a our estimates of horizonta move gesting the presence of a sedentary resident popuation in which fish ment rates between and kmday seem reasonabe Therefore spawn and forage in the same ocaity previousy noted in paice by we are confident that our choice of state abes is bioogicay mean Hunter et a b and in cod by Neat et a Such spatia ingfu for the species in question information is essentia for defining mutispecies management mea Much work has considered the horizonta and vertica move sures as strategies typicay invove gear restrictions Moustakas ments of Atantic cod Hobson et a and European Sivert Dimitromanoakis aimed at imiting the expoitation GRIFFITHS ET AL. | of certain speciesife stages and spatia fisheries cosures aimed Jeroen van der Kooij as we as two reviewers for discussions and at protecting areas of particuar importance for species surviva comments that have improved the manuscript for exampe foraging and spawning grounds Hunter et a b Righton Quaye Hetherington Burt CONFLICT OF INTEREST One imitation of our method is the way in which we dea with individua variation Currenty we assume that by anayzing the Authors decare no confict of interests movements of a finite sampe of data rich pathways n we gain sufficient information about how the mean movement of each AUTHORS CONTRIBUTIONS state is distributed throughout the popuation We then expect the movements of a other individuas to be drawn from one of these CAG TAP and PGB designed the methodoogy CAG distributions and make no attempt to expain any deviance away PGB JLB and DAR interpreted and anayzed the modes from this expected process One way to improve our approach and output movement paths were derived and anayzed by DAR and make it more generic woud be the incusion of covariate informa SRW CAG JLB PGB DAR and JWP ed the writing of tion Phiips Patterson Leroy Piing Nico For exampe the manuscript CAG and SRW designed the figures A au four Atantic cod were unexpectedy cassified soey to a resident thors contributed criticay to the drafts and gave fina approva state even though their movements occurred throughout the win for pubication ter NovemberApri Post hoc investigations revea an average body ength of cm which ies within the predicted range of ength at DATA AND R CODE first maturity cm Froese Pauy It is ikey that im mature fish act differenty to their mature conspecifics Sippe et a The coated datasets for each fish species incuding estimated and that tagging programmes ike the one considered here in state sequences geoocation estimates atitude and ongitude cude fish of differing sex and age Carter et a Consideration and date stamps can be found on the CEFAS Data Hub httpsdoi of these factors is beyond the scope of this paper However we orgcefasdatahub Exampe R code to run our HMM is beieve that the incusion of body ength see Towner et a incuded in Suppementary Information document or can be down for an ecoogica exampe or other individua covariates within the oaded from GitHub httpsgithubcomcagriffithsFishHMM HMMs ikeihood function woud provide a fruitfu avenue for future research ORCID Technoogica advancements in teemetry devices have ed to huge efforts to track the movements of free roaming marine ani Christopher A. Griffiths httporcidorg mas Hays et a Hussey et a Tagging data are now Julia L. Blanchard httporcidorg seen as a vauabe information source for stock assessment modes David A. Righton httporcidorg Sippe et a monitoring the effectiveness of conservation efforts eg McGowan et a Raymond et a and un Serena R. Wright httporcidorg derstanding popuation dynamics across vast spatia scaes Bock et a Hinde et a However there is no avoiding the REFERENCES fact that tags are expensive McGowan et a iabe to occa siona faiure and often produce individua pathways that are of im Bainbridge B Y R The speed of swimming of fish as reated to size and the frequency and ampitude of the tai beat The Journal ited use data poor or a ow number of observations Here we have of Experimental Biology 35 httpsdoiorg introduced a methodoogy that makes the process of scaing up in rspb ference about movement behaviors from individuas to popuation Bestey S Jonsen I D Hinde M A Harcourt R G Gaes N more readiy achievabe Moreover we iustrate how the adoption J Taking anima tracking to new depths Synthesizing of our approach can make tagging studies more cost effective as horizonta vertica movement reationships for four marine pred ators Ecology 96 httpsdoiorg inference can sti be gained from data poor movement paths with Bock B A Jonsen I D Jorgensen S J Winship A J Shaffer S A out resorting to redepoyment or a renewed effort to secure further Bograd S J Costa D P Tracking apex marine predator funding movements in a dynamic ocean Nature 475 https doiorgnature Breed G A Bowen W D Leonard M L Behaviora signa ACKNOWLEDGMENTS ture of intraspecific competition and density dependence in coony breeding marine predators Ecology and Evolution 3 Work was funded by a NERC studentship awarded to CAG JLB httpsdoiorgece PGB DAG and JWP through the ACCE doctora training part Carter M I D Bennett K A Embing C B Hosegood P J Russe D J F Navigating uncertain waters A critica re nership Grant No NEL CAG was aso supported by a view of inferring foraging behaviour from ocation and dive data Tasmania graduate research schoarship We thank Yuan Pan in pinnipeds Movement Ecology 4–25 httpsdoiorg Michae Spence Ewan Hunter Simon Wotherspoon Aison Parton s | GRIFFITHS ET AL.

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Movements and distribution of cod Gadus morhua in the southern North Sea and Engish Channe Resuts from conventiona and eec httpsdoiorgece tronic tagging experiments Journal of the Marine Biological Association