Journal of Experimental Marine Biology and Ecology 461 (2014) 102–106

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Journal of Experimental Marine Biology and Ecology

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Spine reorientation influences drift particle capture efficiency insea urchins

Matthew N. George ⁎, Emily CarringtonDepartment of Biology and Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, WA 98250, USA

⁎ Corresponding author. Tel.: +1 360 378 2165.E-mail address: mngeorge@u.washington.edu (M.N. G

http://dx.doi.org/10.1016/j.jembe.2014.08.0010022-0981/Published by Elsevier B.V.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 4 November 2013Received in revised form 30 July 2014Accepted 1 August 2014Available online xxxx

Keywords:StrongylocentrotusStreamlining behaviorDragKelpUrchin grazingEcomechanics

Many marine organisms use behavior to navigate hydrodynamic landscapes. The subtidal sea urchinStrongylocentrotus franciscanus reorients its spines aswater velocity increases to reducedrag and remain attachedto the substratum. Streamlining may be advantageous in this regard, but it is unclear how this change in dragprofile will affect particle capture, a feeding strategy employed by these organisms. Streamlining in urchinsresults in a “spines down” posture while particle capture benefits from spines remaining erect, a differencethat could potentially lead to decreased feeding rates in high water velocities. To investigate this we ran flowtank experimentswith three species of urchin (Strongylocentrotus droebachiensis, Strongylocentrotus franciscanus,and Strongylocentrotus purpuratus) which differ in size and spine length. All urchins studied displayed some de-gree of streamlining, although the thresholdwater velocity atwhich the behavior occurred varied among species.Particle capturewas highly dependent on urchin size, with S. franciscanus, the largest of the three species studied,capturing the highest total mass across water velocities. However, taking into account urchin size and thechanges in particle flux at eachwater velocity, S. purpuratuswas significantlymore efficient at capturing particleswith “spines up” — an advantage which disappeared once spines were lowered. These results show that size andspine orientation affect how particles interact with urchins in flow and imply that spinemorphology plays a rolein whether or not an individual adopts a streamlined posture.

Published by Elsevier B.V.

1. Introduction

Life in the subtidal zone is driven by water motion. Underwater cur-rents interactwith benthic topography to produce hydrodynamic forcesthat fluctuate in both time and space (Denny, 1987a). Hydrodynamicforces can remove individuals from the substratum (Denny, 1987b;Bell and Gosline, 1997; Blanchette, 1997), cause physical damage tothosewhich remain attached (Shanks andWright, 1986), and influencecommunity structure (Leichter andWitman, 1997; Siddon andWitman,2003). This challenge that marine organisms face influences theirsize (Gaylord et al., 1994; Blanchette, 1997; Denny, 1999), shape(Friedland and Denny, 1995; Koehl, 1996), and the performance ofbiomaterials (Denny and Gaylord, 2002; Boller and Carrington, 2007;Demes et al., 2011).

For suspension feeders, underwater currents present a trade-off. Themovement of water makes suspension feeding possible by deliveringsuspended particles to the feeding structures of sessile organisms(Rubenstein and Koehl, 1977). However, as water velocity increases,drag and lift forces increase as water interacts with the shape andsize of feeding structures (Denny et al., 1985). Mitigation of theseforces requires that organisms living in high current areas employ

eorge).

morphological (Friedland and Denny, 1995; Carrington, 2002) andbehavioral (Koehl, 1976; Maude and Williams, 1983) strategies tosurvive (Denny, 1994).

For sea urchins, water movement plays a fundamental role in theirbehavioral ecology. Inhabiting both the intertidal and subtidal, seaurchins are voracious, mobile herbivores, often credited with the de-struction of the entire algal communities (Mann, 1977; Hagen, 1983).However, urchins move little when algal drift is abundant, take refugein crevices, and lift their spines into currents to feed (Lawrence, 1975;Duggins, 1981; Harrold and Reed, 1985; Lowe et al., 2014). This behav-ioral switch in feedingmode increases the amount of drift algae presentin the local environment (Vanderklift and Kendrick, 2005) and pullsnutrients out of the water column, feeding the individual, other urchinspecies, and the benthic invertebrate communities below them(Duggins, 1981; Nishizaki and Ackerman, 2004; Britton-Simmonset al., 2009; Kelly et al., 2012). As such, it has been hypothesized thatthis flux of carbon from photic zones may allow invertebrate communi-ties to live in high current subtidal habitats where light levels are low(Bustamante et al., 1995; Vanderklift and Wernberg, 2008).

Recently it has been shown that Strongylocentrotus franciscanus(Agassiz, 1863)moves its spines into streamlined positions aswater ve-locity increases to reduce drag forces and stay attached to the substra-tum (Stewart and Britton-Simmons, 2011). A form of streamlining,spine movement dynamically alters the urchin's drag coefficient and

103M.N. George, E. Carrington / Journal of Experimental Marine Biology and Ecology 461 (2014) 102–106

cross-sectional area. This work compliments a previous study whichcompared the probability of dislodgment of three species of urchinswith different spine morphologies (Denny and Gaylord, 1996). Whilethese studies highlight that shape change can reduce dislodgementrisk, it remains unclear how feeding performance is affected by spineposture. One possibility is, with spines up, particles are forced to flowthrough the gaps between spine rows, increasing the probability ofencountering tube feet. Another possibility is, with spines down, ur-chins actually increase particle capture rate by reducing boundarylayer thickness (Frechette et al., 1989).

In this study we investigate the effect of spine reorientation onparticle capture using three species of sea urchin with different bodysizes and spine morphologies. S. franciscanus, a relatively large, subtidalurchin, has long spines and readily adopts a streamlined posture in lab-oratory manipulation of water velocity (Stewart and Britton-Simmons,2011). Other commonly occurring species that inhabit the subtidaland intertidal zones of the Pacific Northwest, Strongylocentrotuspurpuratus (Stimpson, 1857) and Strongylocentrotus droebachiensis(Müller, 1776), are smaller by comparison, have different spine lengths,and have no previously recorded streamlining behavior. Using thesethree species in flow tank experiments, we askwhether spinemorphol-ogy plays a role in streamlining behavior andwhat effect, if any, changesin spine posture have on particle capture.

2. Materials and methods

Three species of sea urchin (S. droebachiensis, S. purpuratus, andS. franciscanus) were collected from subtidal field sites near FridayHarbor Laboratories on San Juan Island, WA, USA (48°32′39.92″N,123°00′39.60″W) and held in aquaria with flowing seawater. Urchinswere kept at 10 °C for two weeks and were fed drift kelp particles adlibitum. Pictures of each individual and a length standard were takenwith an Olympus FE-47 digital camera in the coronal (side) andtransverse (top) planes. Using Image J software (NIH, Bethesda, MD,USA), average spine length (n = 50 per individual), test diameter(transverse plane), and test height (coronal plane) were measured tothe nearest millimeter. Test surface area (A, m2) was computed usingthe generalized equation for an oblate spheroid using test diameterand test height. Adult urchins of approximately the same diameterwere selected within species (see Table 1).

2.1. Spine angle

Each urchin was placed in a 350 l, high-speed flume (Boller andCarrington, 2006) under aweighted plastic basket to restrictmovement.A Sanyo VPC-E2waterproof camcorder was placed downstream of eachurchin and focused upon their resting position. After a 15 minuteacclimation period the basket was removed and water velocity was in-creased from 0 to 79 cm s−1 in nine increments (0, 8, 20, 32, 40, 46, 57,73, and 79 cm s−1), stopping at each water velocity for 2 min. Watervelocity was measured in real time using an electromagnetic flowmeter (Marsh-McBirney Inc., Gaithersburg, MD, USA; accuracy =±3 cm s−1). If an urchin was dislodged or moved from the initialposition the trial was restarted. Dislodgement was common withS. droebachiensis above 46 cm s−1. Video for each individual was splitinto a series of images representing the urchin's orientation at eachwater velocity. The contrast of each image was manipulated in order

Table 1Morphometric measurements (mean ± SD) of the three species of sea urchin studied. SpecieTukey HSD test (α = 0.05).

n Test diameter (cm) Tukey HSD S

S. droebachiensis 15 6.37 ± 1.37 A 0S. purpuratus 8 6.43 ± 1.28 A 1S. franciscanus 13 8.65 ± 2.94 B 4

to differentiate the background from theorganism, creating a silhouette.Spine angle was measured using spines from first quadrant (top right)of each urchin. Positive angles indicate that spines were above horizon-tal while negative values indicate a position below, as defined byStewart and Britton-Simmons (2011).

2.2. Particle capture

For all particle capture feeding experiments a larger, 4000 literpaddle-driven flume was used (Nowell et al., 1989). The subtidal kelpCostaria costata, known to be consumed by all three species of urchinstudied (Vadas, 1977; Britton-Simmons et al., 2009), were collectedfrom the dock at Friday Harbor Laboratories. Blades were cut into 1 ×1 × 0.1 cm (“small”) and 3 × 3 × 0.1 cm (“large”) pieces to representtypical algal drift fragments that urchins catch in the field (Britton-Simmons, unpublished data). A total of 400 g (wet weight) of kelp par-ticles of a single sizewere added to theflume and circulated for 1 h untilevenly distributed along the raceway.

Urchins were acclimated and filmed in the same way as previouslydescribed. Particle capture was tested at seven flow velocities from 0to 44 cm s−1 (0, 6, 15, 24, 34, 40, and 44 cm s−1), with each watervelocity constituting a single trial conducted in order from slow tofast. For each trial an urchin spent 2 min at one water velocity afterwhich the flume was turned off and the urchin was removed. Thetotal amount of drift particles the urchin capturedwas blotted, weighed,counted, and returned to the flume to ensure that the same number ofparticles was available for the next trial. At faster flow velocities urchinswere protected with a screen until the desired water velocity wasreached, after which the screen was removed and the trial began.

The amount of algal drift captured by each urchin in a trial wasreported as both the number of particles captured (#) and dry algalmass captured (Wdry, grams). Dry algal mass was calculated using aconversion factor described by the linear regression of dry to wet algalmass (Wwet, grams) (r2 = 0.98, p b 0.001):

Wdry ¼ 0:1006 Wwet þ 0:002: ð1Þ

The number of particles captured by each urchin (n, #), over thelength each trial (t, seconds), was then used with urchin test surfacearea (A, defined earlier) to calculate the number of particles capturedper unit area of capture surface per unit time (# m−2 s−1):

capture rate ¼ nA t

: ð2Þ

Similarly, the particleflux past each urchinwithin a trial (#m−2 s−1)was calculated using the concentration of particles within the volume ofthe experimental chamber (C, # m−3), assuming a uniform distribution,and multiplying by water velocity (v, m s−1):

particle flux ¼ Cv: ð3Þ

Particle capture rate and particle flux were then used to calculateparticle capture efficiency (%):

capture efficiency ¼ capture rateparticle flux

: ð4Þ

s with a common letter were not significantly different when compared using a post hoc

pine length (cm) Tukey HSD Spine–body ratio Tukey HSD

.86 ± 0.22 A 0.14 ± 0.05 A

.53 ± 0.17 B 0.24 ± 0.04 B

.36 ± 1.27 C 0.60 ± 0.35 C

104 M.N. George, E. Carrington / Journal of Experimental Marine Biology and Ecology 461 (2014) 102–106

2.3. Statistical analysis

Analysis of variance (ANOVA, α= 0.05) was used to test for the ef-fect of species on test diameter, spine length, and spine-body ratio(MATLAB and Statistics Toolbox Release 2013b, The MathWorks, Inc.,Natick, MA, USA). When the effect of species was significant, a post-hoc Tukey's honest significant difference test (HSD) was employed toevaluate the differences among species. Analysis of covariance(ANCOVA, α = 0.05) was used to investigate the effect of mean spineangle on total mass captured and capture efficiency, using species as acategorical grouping variable and water velocity as a covariate. Spineangle was increased by 90° and log transformed in order to meet theassumptions of normality (Kolmogorov–Smirnov test), homogeneityof variance (Bartlett's test for homoscedasticity), and linearity.

3. Results

Test diameter (F2,32= 4.81, p= 0.015), spine length (F2,32= 70.26,p b 0.001), and spine-body ratio (F2,32 = 15.96, p b 0.001) all showed asignificant species effect. Multiple comparisons of species means re-vealed that the test diameter of S. droebachiensis and S. purpuratus wasnot significantly different, while both species were significantly smallerthan S. franciscanus. All three species were significantly different whencompared pairwise using spine length and spine–body ratio (Table 1).

3.1. Spine angle

Each of the three species included in this study reduced their spineangle to some degree as water velocity increased (Fig. 1).S. franciscanus was the first to lower its spines, with the majority ofindividuals adopting a spines “down” posture at water velocities of20 cm s−1 and greater. S. purpuratus kept spines “up” slightly longer,only reducing its spine angle below zero above 30 cm s−1.S. droebachiensis only minimally reduced spine angle throughout therange of water velocities tested. Analysis of covariance investigatingthe effect of species and water velocity on spine angle affirmed a

Fig. 1. Spine angle as a function of water velocity for S. droebachiensis (n = 15),S. purpuratus (n = 7), and S. franciscanus (n = 6). Symbols represent the mean spineangle for individuals observed with respect to the horizontal plane, with 95% confidenceintervals.

significant interaction between species and water velocity (F2,223 =52, p b 0.001).

3.2. Particle capture

As with spine angle, the interaction between species and watervelocity was also significant for both particle sizes (small: F2,165 = 47,p b 0.001; large: F2,171= 28, p b 0.001) (Fig. 2). The number of particlescaptured by S. franciscanus generally increased with water velocity forsmall (Fig. 2a) and large (Fig. 2b) particles despite adopting a “spinesdown”posture (Fig. 2c) abovewater velocities of 15 cm s−1. Thenumberof particles that S. purpuratus captured also increasedwithwater velocityfor both particle sizes (Fig. 2a,b) below water velocities of ~30 cm s−1,after which the number of particles captured drops off, as does spineangle (Fig. 2c). S. droebachiensis captured relatively few particlescompared to the other species at the water velocities and particle sizesused in this study (Fig. 2).

Capture efficiency varied with urchin species and water velocity forboth particle sizes studied (small: F2,164 = 7, p b 0.001; large: F2,177 =27, p b 0.001) (Fig. 3). For this metric, which removes the effect ofurchin size, S. purpuratus outperformed S. franciscanus while spineswere up for both particle sizes at ~25 cm s−1. As with total mass cap-tured (Fig. 2), S. purpuratus' performance declined after spinesreoriented at flow velocities greater than 34 cm s−1 (Fig. 3a, b).S. franciscanus had relatively stable capture efficiencies across thewater velocities studied for small particles, outperforming the othertwo species at velocities above 40 cm s−1 (Fig. 3a). S. franciscanus alsohad relatively high capture efficiencies above 35 cms−1when capturinglarge particles (Fig. 3b). As is to be expected from total mass captured,S. droebachiensis' capture efficiency was low regardless of particle sizeor water velocity (Fig. 3).

4. Discussion

We find that an urchin's spine position in flow is not only dependenton water velocity, as has been previously described for S. franciscanus(Stewart and Britton-Simmons, 2011), but also on species (Fig. 1).

Fig. 2. Total dry mass and the total number of particles captured over 2 min at differentflow velocities for S. droebachiensis (n = 6), S. purpuratus (n = 8), and S. franciscanus(n = 11). Trials were run using (a) “small” (1 × 1 × 0.1 cm) and (b) “large”(3 × 3 × 0.1 cm) particles. Symbols represent the mean with 95% confidence intervals.Spine posture is presented as either in an “up” or “down” confirmation in panel c, basedon whether the mean spine angle for that water velocity was different than −40° foreach species.

Fig. 3.Drift particle capture efficiency at different flow velocities for S. droebachiensis (n=6), S. purpuratus (n = 8), S. franciscanus (n = 11). Trials were run using (a) “small”(1 × 1 × 0.1 cm) and (b) “large” (3 × 3 × 0.1 cm) particles. Symbols represent themean with 95% confidence intervals. Spine posture is presented as either in an “up” or“down” confirmation in panel c based on whether the mean spine angle for that watervelocity was different than−40° for each species.

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This result also held true for particle capture (Fig. 2) and captureefficiency (Fig. 3) at both particle sizes tested. Coupled with significantdifferences in morphology (Table 1), these results have implicationsfor our understanding of how behavior, body size, and spinemorpholo-gy influence the feedingmode of these organisms and the flow of nutri-ents through marine ecosystems.

Passive mitigation of drag forces in marine organisms is common. Aclassic example is that of some species of sea anemones which bend inflow, reducing drag on feeding structures in the process (Koehl, 1976).In contrast, we find in three urchin species that shape change is behav-iorally controlled, with spines actively reorienting downward intostreamlined positions. The degree and flow threshold for streamliningalso appear to be species specific (Fig. 1). S. franciscanus, the specieswith the largest drag profile, initiated spine reorientation at thelowest flow, followed by S. purpuratus at intermediate flows, andS. droebachiensis at the highest flows. This trend of smaller urchinsmaintaining a “spines up” posture in high water velocities is consistentwith differences in spine morphology among the three species, a factorwhich we represent as the relative length of the spines to test diameter(spine–body ratio) in Table 1. The fact that S. franciscanus has a highratio while S. droebachiensis has a low ratio suggests the relative rewardof streamlining. Smaller-spined urchins either lack the behavior orchoose not to reorient, perhaps because the impact on their drag profileis relatively low.

Changes in an urchin's drag profile also alter the hydrodynamiclandscape surrounding them (Nishizaki and Ackerman, 2007). It ischanges in this landscape that govern howdrift will approach and inter-act with the organism. In the field, all three species studied have beenobserved capturing pieces of kelp from the water column as it floatsoverhead or rolls along the bottom (Duggins, 1981; Harrold and Reed,1985). With spines in an “up” confirmation, particles pass through thespine rows or become lodged on spines. Dorsal tube feet, although lon-ger than the spines of both S. droebachiensis and S. purpuratus, aremuchless efficient at capturing drift particles (Contreras and Castilla, 1987).However, once lodged on the spines, kelp is anchored to the bodyusing the tube feet and subsequently guided toward the mouth andconsumed underneath the organism.

With increased flow, more particles pass an urchin per unit time.Therefore, we expect that urchins maximize foraging effort by main-taining a spine “up” posture as long as drag forces remain manageable.In this regard, adopting a spine “down” posturewould sacrifice foragingefficiency through the reduction of capture surface area. The otherpossibility is that having spines “down” at fast water velocities actuallyincreases particle capture due to the reduction in thickness of theboundary layer surrounding the organism, allowing more particles toreach the tube feet and become attached.

To evaluate these alternate views of how water velocity affectsurchin feeding, we can compare particle mass capture (Fig. 2) andcapture efficiency among species (Fig. 3). What stands out immediatelyis the lack of any significant mass captured by S. droebachiensis acrosswater velocities for both particle sizes. Measurements of captureefficiency lead us to conclude that drift capture is not a viable feedingstrategy for S. droebachiensis. This result is consistent with other studieswhich describe foraging behavior in which they move often (Lauzon-Guay et al., 2006), can be found sitting beneath larger urchins (Tegnerand Dayton, 1977; Duggins, 1981), form aggregations to capture driftparticles (Vadas et al., 1986), and are omnivorous (Briscoe and Sebens,1988). Short spines, in this instance, may help to facilitate behaviorsother than drift capture that require the species to be more maneuver-able than its larger counterparts, such as opportunistic feeding on kelpcaptured by other species.

Our results demonstrate that S. purpuratus captures kelp in flow(Figs. 2, 3), a behavior which has been explored in the context of cover-ing behavior (Douglas, 1976), nutrient flow across habitats (Kenner,1992), and intraspecific competition (Duggins, 1981). However, wefound a dependence of particle capture on spine position. Shown inpanel c of Figs. 2 and 3 as a schematic representation of whether ornot spines were “up” or “down” at each water velocity, S. purpuratus'capture rate increased approximately linearly for both particle sizeswith spines “up” and subsequently both total mass captured andcapture efficiency declined when spines reoriented “down” at andabove ~35 cm s−1. These results are consistent with observations thatS. purpuratus is more abundant in intertidal habitats where they livein rock crevices and are battered by waves (Tegner, 2001). In this con-text, it is easy to see how behavioral modification of drag would be ofparamount importance for S. purpuratus to prevent dislodgement(Denny and Gaylord, 1996), while also retaining a viable mechanismof feeding on drift brought to them by wave action.

We observed that S. franciscanus reorients its spines readily at watervelocities below 20 cm s−1, a result which is consistent with previousstudies (Stewart and Britton-Simmons, 2011). While this velocitythreshold is apparent in a flow tank, it may not readily translate tosubtidal habitats, where an urchin body is often not fully exposed(Harrold and Reed, 1985) and flow regimes are unsteady. Nonetheless,with spines oriented “down” S. franciscanus was still able to capture asignificant number or particles above 30 cm s−1 (Fig. 2), even whencorrecting for its size (Fig. 3). This suggests that in high current areas,S. franciscanus ismore efficient at capturing drift particles than its small-er counterparts, possibly due to theway particles interact with its spinemorphology (Table 1). Interestingly, S. franciscanus was also moreefficient at capturing large particles than smaller ones (Fig. 3), againpointing to a possible link between spine morphology and an urchin'sability to capture drift of different sizes. While further investigationwould firm up the relationship between particle size, capture efficiency,and spine morphology, it is worth noting that the density and size offloating particulate are known to fluctuate seasonally (Britton-Simmons et al., 2009) and S. franciscanus is capable of capturing intactblades of kelp that are much larger than the pieces used in this study.

4.1. Conclusions

Differences in the size and shape of urchins in flow dramatically af-fects the forces they experience as well as their foraging efficiency. In

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this studywe show that (1) streamlining behavior varies amongurchinswith different morphologies and (2) spine orientation interacts withparticle capture as water velocity increases. Therefore, we proposethat streamlining is a behavioral mechanism that allows urchins tomit-igate hydrodynamic forces, at the expense of particle capture efficiency.This process of shape change with flow provides a mechanistic frame-work to explore several aspects of urchin feeding, such as the role of ur-chins on subtidal shelves where organisms are subsidized by algal drift,how specific species interact within guilds of herbivores, and whycertain spine morphologies are seen in some habitats but not others.

Acknowledgments

Funding for this work was provided by the Stephen and RuthWainwright fellowship to M.N. George and NSF award #EF104113 toE. Carrington. A special thank you goes to Kevin Britton-Simmons forsharing data and personal observations, and advising on experimentaldesign. We also would like to thank Hilary Hayford, Laura Newcomb,Jaquan Horton, Kyle Demes, John Gosline and Ken Sebens for theirinsight. Data collected in this study are archived under project #2250at http://www.bco-dmo.org. [SS]

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