Distribution and retention of Petrolisthes armatus in a coastal plain estuary:The role of vertical movement in larval transport

Charles E. Tilburg a,*, Jennie E. Seay b, T. Dale Bishop b, Harlan L. Miller III b, Christof Meile b

aDepartment of Marine Sciences, University of New England, 11 Hills Beach Road, Biddeford, Maine, 04005, USAbDepartment of Marine Sciences, University of Georgia, Athens, Georgia, 30602, USA

a r t i c l e i n f o

Article history:Received 31 July 2009Accepted 6 April 2010Available online 14 April 2010

Keywords:larval transportcrabslarvaezoeaemodelsPetrolisthes armatus (green porcelain crab)estuaryvertical movement

a b s t r a c t

Since transport of planktonic larvae is essential to the maintenance and expansion of many marinespecies, we examined the spatial and temporal distribution of green porcelain crab Petrolisthes armatus(Gibbes, 1850) larvae and the possible underlying physical and behavioral mechanisms using a combi-nation of !eld observations and numerical modeling. The !eld study consisted of observations of larvalabundance and distribution as well as hydrographic surveys of the Satilla River estuary on the east coastof the USA in August 2006. Larvae were found throughout the water column within the tributaries butprimarily at depth in the main river. A numerical model was used to examine the effect of "ow andpossible larval behavior responsible for the observed distribution and the consequences for larvalretention in the estuary. Model results that included downward larval movement are consistent with the!eld observations, supporting the hypothesis that P. armatus larvae vertically migrate within the watercolumn, which aids in their retention within the estuary.

! 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Many species of estuarine !sh and invertebrates depend on thesupply of planktonic larvae that are delivered to estuarine nurseryhabitats to maintain local populations. In some species, larvae arereleased in the coastal ocean and are then transported back to theestuary by coastal currents (Taylor et al., 2007). In others, larvae arereleased near the estuarine mouth and are then exported to theadjacent coastal ocean where they pass through a number ofdevelopmental stages before returning to the estuary (Epifanio,1995; Petrone et al., 2005). In yet another group, larvae arereleased within the estuary and are retained by behavioralresponses to vertical shear in currents (Forward et al., 2003).

The green porcelain crab Petrolisthes armatus (Gibbes, 1850)appears to belong to this last group. It is distributedwidely in tropicalregions of western Africa, the eastern Paci!c Ocean and the westernAtlanticOcean. IthasbeencollectedontheFlorida coast (BiscayneBayandMiami Beach) since the 1930s (Knott et al.,1999). Its discovery atSt. Catherine’s Island, Georgia in Fall of 1994marked the !rst sightingnorth of Cape Canaveral, Florida. It was subsequently found in SouthCarolina’s coastalwaters in the Springof1995 (Knott et al.,1999;Coen

and McAlister, 2001). Since the initial sightings, P. armatus hasestablished successful breeding populations in all of Georgia’s majorestuarine systems and is often the dominant crab on oyster reefs andhard substrates in shallow subtidal and intertidal waters along thecoasts of Georgia and South Carolina (Knott et al., 1999; Hollebone,2006; Hollebone and Hay, 2007a). Its small carapace width(12e14 mm; Coen and Heck, 1983) allows it to hide easily in thecrevicesof anoyster reefandescapepelagicpredators, leading topeakdensities of 4000e11,000 m!2 on some Georgia oyster reefs(Hollebone and Hay, 2007a).

Several recent studies of P. armatus along the Georgia coastfocused on the adult benthic populations (e.g., Knott et al., 1999;Hollebone, 2006; Hollebone and Hay, 2007a). Hollebone and Hay(2007b) showed that biotic resistance provided by native speciesslowed initial invasion pressure but that resistance was soon over-whelmed by the large supply of P. armatus larvae available forsettlement, suggesting that the rapid growth of dense P. armatuspopulationsmaybe related to larval dispersal. Thephysical"ow!eldand the life cycle of the animal affect the distribution and transportof larvae and hence may help explain observed abundance patterns(e.g. McConaugha, 1992; Epifanio and Garvine, 2001; Queiroga andBlanton, 2005). P. armatus has only two zoeal stages and a mega-lopal stage during its larval development and reached the juvenilecrab stage in 17e49 days during laboratory studies (Gore, 1969). Ina more recent investigation, Hollebone and Hay (2007a) reported

* Corresponding author.E-mail address: ctilburg@une.edu (C.E. Tilburg).

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Estuarine, Coastal and Shelf Science 88 (2010) 260e266

that P. armatus larvae reared in the laboratory can reach the !rstjuvenile crab stage in as quickly as 15e17 days. Such short devel-opmental periods can decrease larval exposure to predators andincrease the number of larvae available to settle in adult habitats,making the rapid establishment of dense populations more likely.

A number of studies (e.g., DiBacco et al., 2001; North et al., 2008)have shown that simple behavior by larvae can result in drasticallydifferent larval dispersal. Thus, knowledge of the "ow !eld withinestuaries and its effect on larval transport will lead to a greater under-standingof life strategies, controls on larvaldispersal and transport, andrecruitment success of invasive specieswhich impact resident"ora andfauna (Grosholz, 2002; Mooney and Cleland, 2001; Ruiz et al., 1999).

Our study examines the effects of the interaction between thebehavior of P. armatus larvae and the physical "ow !eld with regardto transport and retention within an estuary. Our objectives in thisstudy were 1) to determine if the vertical distribution of P. armatuslarvae varied between the tributaries and the main river of theSatilla River estuary; 2) to examine the effect of vertical migrationon larval distribution in the context of estuarine physical forcingand 3) to evaluate the role of vertical movement of P. armatus onlarval retention within the estuary.

We !rst conducted physical and biological surveys in the SatillaRiver estuary, measuring physical parameters and larval densities.Building on previous studies conducted on the hydrodynamics ofthe Satilla River estuarine system (Alber and Sheldon,1999; Blantonet al., 2003; Zheng et al., 2003a,b), we then used a simple larvalbehavior model coupled to a validated numerical circulation modelto simulate larval transport over a 17-day time period thatencompassed the observations. We compared the simulated andobserved larval distributions to determine if vertical movement ofthe larvae was consistent with the observed larval distribution andto what extent it affected larval retention in the estuary.

2. Materials and methods

2.1. Study area

The Satilla River estuary (Fig. 1) is located in the South AtlanticBight and represents a partially mixed estuary that can reach well-

mixed conditions in the tributaries (Blanton et al., 2003). It exhibitsstrong variations in freshwater inputs and a semi-diurnal tidal cycle.Thevolumeof the estuary is 379,000m3 and the lower 25kmstretchof the estuary is approximately 1 km wide. Average depth of theestuary is 4 m but is 10 m near the mouth, with a 1e1.5 m tidalamplitude, whose effects extend 50 km inland. The Satilla Riverdrains a watershed of 9140 km2. The average freshwater in"ow is70m3/s but varies seasonallywith peak discharge in spring (Blantonet al., 2003). Themajority of the freshwater originates at the head ofthe main river. The two sampled tributaries, Little Satilla River andJointer Creek (Fig. 1), receive most freshwater from the Satilla River,with minor precipitation input and additional small amounts offreshwater in"ow from upstream in the Little Satilla River.

2.2. Sampling procedures

Biological and physical surveys in the Satilla River and itstributaries were performed during two-day cruises in March, April,and September of 2005, andMarch andAugust of 2006 on the27-footresearch vessel R/V WaterDawg. Salinity, temperature, and depthwere measured at each station (Fig. 1) with a SeaBird SBE-25Conductivity, Temperature, and Depth (CTD) recorder. Tidal heightsand phase were determined from the nearby tidal gauge at SaintSimon’s Island,GA. Plankton sampleswere collected ateach station atthe surface (0.5e2.0 m from surface) and near bottom (0.25 m frombottom) using plankton nets (mesh size " 240 mm) equipped with"ow meters. The depth of the near bottom samples varied between4m in the tributaries to amaximumof 10m at themain rivermouth.During each cruise, samples were taken up and down the river ortributaries at approximately 45 min intervals from 7:30 AM to 7:30PM(spanning a full, daytime tidal period), resulting in13e20samplesfor each day.

Each biological sample was washed in a 180 mm-mesh sieve,transferred to aNalgene"bottle and!xedwith10%buffered formalin.In the laboratory, the samples were washed and sub-sampled witha Folsom Plankton Splitter following Grif!ths et al. (1984). P. armatuslarvae from two sub-samples were counted using a dissectingmicroscope, separated from the sample and identi!ed to stage. If thedifference in counts between the sub-samples was greater than 25%,

Fig. 1. Map of the Satilla River estuary showing the main river and the tributaries, Jointer Creek and Little Satilla River. Letters and numbers indicate the locations of CTD and larvalsampling stations.

C.E. Tilburg et al. / Estuarine, Coastal and Shelf Science 88 (2010) 260e266 261

a third sub-sample was counted. Counts of stage I, stage II, and totallarvae were divided by the volume of water sampled to obtaina density for each sample (Grif!ths et al., 1984), which were thencompared using a 3-wayANOVAto examine the effects of tidal phase,day-to-day variations, and water column location on larval densities.

2.3. Numerical model

The physical circulation model FVCOM, a primitive equation!nite-volume model in sigma (terrain-following) coordinates(Chen et al., 2006a), was used to simulate the "ow !eld. The modelis described more comprehensively in Chen et al. (2003, 2008). The"uid "ow is governed by continuity and momentum conservation,as well as temperature and salinity equations that determine thedensity structure. The model uses a Mellor and Yamada level-2.5turbulent closure scheme to determine vertical mixing. FVCOM hasbeen used extensively to study transport on coastal shelves andwithin estuaries (e.g. Chen et al., 2003; Johnson et al., 2006; Huretet al., 2007). It has been validated in the Satilla Estuary with a seriesof observations of currents and hydrographic surveys during 1999and 2004 (Chen et al., 2008). The domain consisted of anunstructured grid comprised of 20,677 elements and 10,827 nodes.It extended from the freshwater part of the Satilla River onto theinner shelf, and encompassed both subtidal and intertidal areas(Chen et al., 2008).

Riverine freshwater input, wind forcing and tidal elevation atthe outer (oceanic) boundary were used to force "uid motion. Riverdischarge was obtained from the US Geological Survey (station02228000, Satilla River at Atkinson GA). Wind speed and directionwere imposed based on observations from NOAA EnvironmentalBuoy 41008. Tidal forcing was imposed based on Foreman’s (1978)tidal forecast, which was validated by comparison to a nearby tidalgage at Saint Simon’s Island, GA (station 867344). Flow simulationswere performed for the period from July 26 to August 20, 2006 andwere spun up with 2 days of tidal forcing. The modeled "ow !eldsand eddy coef!cients were used to create trajectories of larvae.

Since the horizontal swimming speeds of the larvae aremuch lessthan the advective velocities within the estuary, the larvae weremodeled as passive particles in the horizontal. In the vertical, the roleof larval mass as well as active swimming behavior was considered.Most larvae are negatively buoyant and will sink without someswimming activity (Sulkin, 1984). However, the net effects of orien-tation, kinesis and buoyancy can result in upwardmigration, sinking,or active downward migration. Larvae may be positively phototacticor negatively geotactic after hatching (which would cause them toremain near the surface) butmay be less responsive as they get older,causing them to eventually sink in thewater column. Larvaemay alsorespond to variations inpressure, salinity, temperature, or turbulence(Epifanio, 2007). Since we are unaware of in situ studies examiningthe vertical velocities of P. armatus larvae, larval behavior was simu-latedasa randomwalkwithdirectional verticalmigration.Mimickingcommon larval behavior of brachyuran crabs, imposed verticalvelocities ranged from slightly positive to strongly negative (#1, 0,!0.5,!1,!5,!10mm/s), with the latter representing typical sinkingspeeds for these sized larvae (Capaldo, 1993; Park et al., 2004).However, as the response of P. armatus larvae to physical or chemicalcues is unknown, it does not provide a mechanistic link to triggers ofmovement (e.g. Sulkin, 1984).

In each time step, particle tracking was split into a turbulentdiffusion and an advective component. For the former, the veloci-ties and mixing coef!cients were !rst computed at the location ofeach particle. As the eddy diffusivity (K) varies with depth (z), itsvertical gradient was also obtained, which was needed to preventarti!cial accumulation of particles in zones of low diffusivities

(Hunter et al., 1993; Visser, 1997; Meile and Van Cappellen, 2005).Formally, the vertical location is calculated as

znew " zold # dKdz

$zold%dt # R

!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!2rK"zold # 1

2dKdz

#####zolddt$dt

vuut

where R is a random process with 0 mean and variance r, and thedifference between zold and znew is the vertical distance traveleddue to turbulent diffusion between the start and the end of a timestep (dt). The advective step was then performed using a 4th orderRunge-Kutta scheme as described in Chen et al. (2006b), with theimposed vertical sinking velocity added to the physical "ow !eld.Trajectories exceeding the top or bottom of the water columnwerere"ected at the boundaries (e.g. Visser, 1997).

Without any direct information on location and exact timing, wemade the assumption that female P. armatus spawn in the shallowsubtidal zone. We simulated the spawning as the introduction ofparticles at 2899 grid nodes whose tidally averaged water depthwas less than 0.75 m. Spawning was simulated as hourly release ofparticles throughout an ebb tide. For each seed location, we thenchose as the actual trajectory that one which resulted in thegreatest travel distance. Particles were released on August 2, 2006and tracking was performed for the period of August 2e20, 2006,which corresponded to the minimum time of development fromstage I zoea to a juvenile crab (Hollebone and Hay, 2007a).

3. Results

3.1. Physical conditions

During the surveys in August 2006, freshwater discharge waslow, resulting in high salinities in both the main river and thetributaries (Fig. 2). Temperature ranged from 29 to 31 &C; however,density variations were dominated by salinity, which varied by asmuch as 4 PSU in some regions of the river over a tidal cycle.Vertical salinity strati!cation varied from less than 0.01 PSU/m inthe tributaries to greater than 0.5 PSU/m within the river. Regionsof strong vertical strati!cation moved with tidal currents, down-stream during ebb tide (Fig. 2a) and upstream during "ood tide(Fig. 2b). The shallower tributaries (Fig. 2cef) tended to be moresaline than the river and less strati!ed, most likely due to the lack ofdirect freshwater sources.

3.2. Larval distribution and abundance

Larval abundance varied seasonally. No P. armatus larvae wereobserved during the two-day cruises in April 2005 and March 2006.Some P. armatus larvae were collected during August and Septemberof 2005 (not shown). Larval abundance of both zoeal stages was byfar the greatest in August 2006 and involved surface and bottomsamples in the tributaries and the main river as discussed below.

Examination of the spatial distribution of the larval densities(Fig. 3) reveals strong variations between the tributaries and themain river. In the tributaries (stations AeD; Fig. 1), larvae werepresent in signi!cant numbers in both bottom and surface samples,with higher numbers in bottom samples at 3 of the 4 stations (graybars in Fig. 3); however, the greatest larval densities were found atStation B near the connection of Jointer Creek and the Little Satilla(Fig. 1), where larvae were present in greater numbers at thesurface. In the main river (stations 1e10; Fig. 1), few if any larvaewere present in surface samples (black bars in Fig. 3). Larvaldensities were always greater in bottom samples in the main river.

Since the number of samples was relatively small (61 totalsamples for the August 2006 cruises) and ANOVA (not shown)

C.E. Tilburg et al. / Estuarine, Coastal and Shelf Science 88 (2010) 260e266262

revealed no signi!cant differences in larval densities betweenstations within the tributaries nor between stations located withinthe main river, we combined the samples into two spatial cate-gories: “tributary” (stations AeD in Fig. 1 which were collected onAugust 2, 2006) and “main river” (stations 1e10, 3ae7a in Fig. 1which were collected on August 3e4, 2006) and two temporalcategories: “"ood tide” (samples taken after the tidal bulge had

entered the estuary and velocities were observed to moveupstream) and “ebb tide” (samples taken after the tidal bulge beganto exit the estuary and velocities were downstream). Therewere 26“tributary” samples, of which 12 were “ebb tide” samples and 14were “"ood tide” samples. There were 35 “main river” samples, ofwhich 15 were “ebb tide” samples and 20 were “"ood tide”samples.

Dep

th (m

)Main Satilla River

Afte

r Ebb

!14

!12

!10

!8

!6

!4

!2

0

31

32

33

34

35

36

Distance from Mouth (km)

Dep

th (m

)

Main Satilla River

Afte

r Flo

od

!12 !10 !8 !6 !4 !2 0 2!14

!12

!10

!8

!6

!4

!2

0

31

32

33

34

35

36

Dep

th (m

)

Little Satilla River

!4

!2

0

35.6

35.8

36

36.2

Distance from mouth of tributary (km)

Dep

th (m

)

Jointer Creek

!2 !1.5 !1 !0.5 0

!4

!2

0

35.6

35.8

36

36.2

Dep

th (m

)

Little Satilla River

!4

!2

0

35.6

35.8

36

36.2

Dep

th (m

)

Jointer Creek

!4

!2

0

35.6

35.8

36

36.2

A

B

C

D

E

F

Fig. 2. Salinity pro!les in the Satilla River estuary after ebb tide (upper panels) and "ood tide (lower panels). A "Main Satilla River after ebb tide on August 3, 2006. B "Main SatillaRiver after "ood tide on August 3, 2006. Black vertical lines mark the entrance of the two merged tributaries. C " Little Satilla River after ebb tide on August 2, 2006. D " JointerCreek after ebb tide on August 2, 2006. E " Little Satilla River after "ood tide on August 2, 2006. F " Jointer Creek after "ood tide on August 2, 2006. Black dots indicate locations ofCTD casts. 0 km denotes the estuary mouth, which is at 81.4&W.

A

0

15

0

30

0

12

0

16

0

25

0

17

0

1

0

4

0

12

Fig. 3. Average larval densities (#/m3) for all August 2006 samples. A " densities found at the surface (black bars) and at the bottom (gray bars) at each station. Black dots indicatestations that lacked samples at the surface and/or the bottom. Bottom depths in the tributaries were 4 m. Bottom depths in the main river ranged from greater than 10 m at themouth to 4 m upstream. Dark gray lines represent land. Light gray lines represent the main tidal channel.

C.E. Tilburg et al. / Estuarine, Coastal and Shelf Science 88 (2010) 260e266 263

Samples from the tributaries (Table 1) showed no signi!cantdifference in larval densities between ebb and "ood tides orbetween densities at the surface and at the bottom within thetributary samples. In the main Satilla River, there was no signi!cantdifference between the densities during ebb or "ood; however,densities of both larval stages were signi!cantly higher at thebottom than at the surface during both tidal stages. Results ofANOVA revealed a statistically signi!cant effect of depth on larvaldensities for both zoeal stages in the main river (p " 0.0014 and0.0030), but no signi!cant effect of tidal phase or the interactionbetween depth and tidal phase on densities of either stage of larvae(Table 2). Since no differences were found between the distribu-tions of zoeae I and II, the two stages were combined for theanalysis of larval distribution.

3.3. Model simulations

To provide a meaningful comparison between the simulatedparticle depths and observed larval distribution, we quanti!ed thevertical distribution of the particles within the tributaries and themain river for different vertical velocities of the particles mimickingdifferent hypothetical larval net behavior (Fig. 4). We speci!edregions of the model to be “tributary” (gray square in Fig. 4a) and“main river” (black rectangle). These two regions encompass therespective sampling sites. Particle positionswere analyzed onAugust4, 2006 (2.6 days or 5 tidal periods after spawning), which corre-sponds to the time of observation, and August 20, 2006 (17 days or33 tidal periods after spawning), which corresponds to theminimumtime required for newly spawned larvae to metamorphose intojuvenile crabs. Particles were identi!ed as “bottom” particles iflocated in the bottom 20% of the water column (sigma <!0.8) and“surface” particles otherwise (the terrain-following coordinatesigma is 0 at the surface and !1 at the bottom of the water column).

Most positive or neutrally buoyant particles remained near thesurface in both the tributaries and the main river, with slightlymore particles at the surface in the main river (black lines Fig. 4b)than in the tributaries (gray lines). Such a distribution disagreeswith the majority of observations, in which the majority of thelarvae were found at depth at most stations (Fig. 3). Negativevertical velocities resulted in particles residing near bottom(Fig. 4b) in both the tributaries and the main river, although theretended to be fewer particles at the surface in the main river than inthe tributaries (Fig. 4a). For example, 30% of those particlesassigned a vertical velocity of !1.0 mm/s were found at the surfaceof the tributaries but only 20% of particles were found at the surfaceof the main river (Fig. 4b). The spatial variation of the modeledlarval distribution (Fig. 4b) for vertical velocities of !0.5 and!1.0 mm/s is consistent with the observed larval distribution(Fig. 3, Table 1), although the observed vertical variation in thelarval distribution was not as evident as the modeled variation inparticle location in the tributaries.

Examination of the trajectories of the particles indicated thatvertical movement has a strong effect on the lateral transport of theparticles, their depths, and retention in the estuary (Fig. 4).

Table 1Average larval densities (# m-3) in the Satilla River and its tributaries for August2006.

Location Depth Ebb Flood

Main River Surface 1.29 (0.76) 0.12 (0.05)Bottom 8.52 (4.91) 4.79 (2.27)

Tributaries Surface 13.84 (6.99) 11.22 (6.90)Bottom 14.28 (5.97) 12.19 (3.12)

Standard error in parentheses.

Table 2Three-way analysis of variance with larval density of Petrolisthes armatus as thedependent variable for August 3e4, 2006 samples in the Satilla River.

Source Degrees offreedom

Sum ofsquares

F-ratio P

Stage IDepth 1 929.7 10.6 0.0030Tidal Phase 1 150.8 1.7 0.2009Day 1 0.1 0.0008 0.9775Depth ' Tidal phase 1 51.4 0.6 0.4510Residual 28 2461.2

Stage IIDepth 1 945.8 12.6 0.0014Tidal Phase 1 160.7 2.0 0.1669Day 1 10.8 0.1 0.7071Depth ' Tidal phase 1 33.8 0.5 0.5070Residual 28 2095.3

81.8 81.6 81.4 81.2

32.6

32.7

32.8

32.9

33

Longitude (oW)

Latit

ude

(o N)

Dep

th (s

igm

a)

!1

!0.8

!0.6

!0.4

!0.2

0

!10 !8 !6 !4 !2 0 20

20

40

60

80

100

Vertical Velocity (mm/s)

Perc

enta

ge o

f Par

ticle

s

!10 !8 !6 !4 !2 0 20

10

20

30

Vertical Velocity (mm/s)

Perc

enta

ge o

f Par

ticle

s Lo

st fr

om E

stua

ry

04 Aug 200620 Aug 2006

Tributary ! SurfaceTributary ! BottomMain River ! SurfaceMain River ! Bottom

A

B

C

Fig. 4. A " Location and depth of particles on August 4, 2006 of particles released onAugust 2, 2006 that are assigned a vertical velocity of !1.0 mm/s. Region outlined ingray represents the “tributary” in the text. Region outlined in black represents the“main river.” B " Percentage of particles at surface (solid lines) and at bottom (dashedlines) as a function of vertical velocity in the “tributaries” (gray lines) and “main river”(black lines) on August 4, 2006. C " Percentage of particles lost from estuary by August4, 2006 (solid line) and August 20, 2006 (dashed line) as a function of vertical velocity.Particles were counted as lost from the estuary if they moved downstream of theestuary mouth (de!ned at 81.4&W).

C.E. Tilburg et al. / Estuarine, Coastal and Shelf Science 88 (2010) 260e266264

Positively or neutrally buoyant particles remained at the surface forthe duration of the simulation and were removed from the estuary(Fig. 4c). Those particles with large, negative vertical velocitiestraveled quickly to the bottom (Fig. 4b) and remained within theestuary (Fig. 4c). The effects of the vertical movement manifestthemselves quickly. Particle retention after 2.6 days (solid line inFig. 4c) is very similar to that after 17 days (dashed line) for anyvertical velocity, suggesting that those particles that do exit theestuary do sowithin the !rst few tidal cycles after their release. Thisis consistent with a lack of temporal variation in the verticalstrati!cation of particles after 2.6 days for the different velocities(not shown), indicating that the effects of vertical velocities onparticle depth occurred over a few tidal cycles.

4. Discussion

The !eld-campaign revealed strong seasonal variation ofP. armatus zoeae larvae. The absence of P. armatus in spring samplessuggests that the spawning season in the Satilla River estuaryoccurs in the summer and fall months. Since this species hasmigrated into the area from warmer climates (Knott et al., 1999;Coen and McAlister, 2001), we speculate that Satilla Rivertemperatures may hinder spawning during spring (March andApril; 18e21 &C vs. August and September: 29.5e31 &C). This latespawning is consistent with observations by Hollebone and Hay(2007a) who found an increase in gravid female P. armatus in twoGeorgia estuaries during the warmer summer months.

Data from the August 2006 !eld-campaign showed spatialvariation in the vertical distribution of P. armatus zoeae larvae.Larval densities were signi!cantly greater at the bottom than at thesurface in the main river, but the tributaries showed no signi!cantdifference. The general agreement between the observations andoutput from a numerical model that incorporated realistic down-ward vertical velocities of the larvae is consistent with thehypothesis that the P. armatus larvae move downward. There area number of explanations for the spatial variation of verticaldistribution of larvae. The shallow depth and the absence of verticalstrati!cation of salinity in the tributaries facilitate greater verticalmixing than the main river. This would result in more turbulentmovement of the larvae and tend to counteract the sinking ordownward swimming of the larvae. In contrast, weaker verticalmixing in the main river would result in less turbulent movementof the larvae and allow the larvae tomove toward the bottom of theestuary. The lack of signi!cant interaction between depth and tidalphase (Table 2) does not support the notion of larvae engaging inselective tidal stream transport (Forward et al., 2003) to remainwithin or travel throughout the estuary.

Downward movement of the larvae results in greater concen-trations of larvae in deeperwaterwhere the gravitational circulationwithin the estuary produces upstream subtidal "ow (e.g. Blantonet al., 2003). This upstream "ow would allow for greater retentionof larvae in the estuary so that, as vertical velocities become morenegative, the amount of particles lost to the coastal ocean decreases.However, even large downward velocities result in some particlesleaving the estuary,which is consistentwith the spread of P. armatusinto other estuaries on the east coast of the USA.

A notable caveat to our analysis on estimates of the role ofvertical motion on larval distribution and retention is our lack ofknowledge of spawning sites or actual larval behavior. The simu-lated release points were selected based on water depth only.However, little is known of the spatial variation of spawning sites inthe Satilla River estuary and the selected locations may notnecessarily re"ect spawning habitats. Also, vertical positioning isthe result of activities and orientations to external cues includinglight, gravity, or other stimuli. While it is not known to which cues

P. armatus larvae are responding, model and observational datasupport the following conceptual model that is consistent with thebehavior of a number of other larvae of brachyuran crabs (Sulkin,1984): Females spawn in shallow water at the beginning of ebbtide. Once spawned, larvae are characterized by downward move-ment, either due to active downward swimming by the larvae orthe cessation of swimming and passive sinking. Vertical mixingresults in some larvae remaining distributed throughout the watercolumn during both ebb and "ood tide, particularly in thetributaries. However, within the main Satilla River, the downwardmovement tends to overcome the weaker vertical mixing and mostlarvae move to deeper water during both tidal phases, hinderingtheir movement out of the estuary.

Our !ndings are relevant to other estuarine larvae with similarvertical migration velocities (e.g. Cronin, 1982). Although themodeling approach reinforces the limited observations, morefrequent sampling (during both day and night) as well as laboratorystudies that examine both the larval response to different cues andthe rates of vertical movement are needed to assess in situ migra-tory patterns, to constrain the potential impact of the timing oflarval spawning on recruitment, and to determine the spread of theinvasive P. armatus in the Satilla River and other estuaries along theSouth Atlantic Bight.

Acknowledgments

This is contribution number 29 of the Marine Science Center atthe University of New England. We would like to thank Dr.Changsheng Chen and Dr. Geoffrey Cowles for providing FVCOM.Wewould also like to thank Dr. RandyWalker for allowing us to usethe Marine Extension Service as well as Captain Paul Christian ofthe R/V WaterDawg, Captain Lindsey Parker and Marty Higgins ofthe R/V Bulldog, Heather Reader, Marcia Hsu, Barakah Jamison, andChristine Tilburg for their help in the !eld. Comments on an earlierversion by Drs. Rick Tankersley, Chuck Epifanio and Phil Yundhelped to substantially improve the manuscript. This publicationwas supported by Georgia Sea Grant of the National Sea GrantCollege Program of the U.S. Department of Commerce’s NationalOceanic and Atmospheric Administration under NOAA Grant#NA04OAR4170033 to CT and CM and by the National ScienceFoundation Georgia Coastal Ecosystems Long Term EcologicalResearch grant # OCE 06-20959 (DB and CM). The views expressedherein do not necessarily re"ect the views of any of thoseorganizations.

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