Mar Biol (2015) 162:1047–1059 DOI 10.1007/s00227-015-2648-2

ORIGINAL PAPER

Differences in feeding adaptations in intertidal and subtidal suspension-feeding gastropods: studies on fornicata and Crepipatella peruviana

Casey M. Diederich1,3 · Oscar R. Chaparro2 · Daniela A. Mardones-Toledo2 · Gabriela P. Garrido2 · Jaime A. Montory2 · Jan A. Pechenik1

Received: 25 September 2014 / Accepted: 2 March 2015 / Published online: 15 March 2015 © Springer-Verlag Berlin Heidelberg 2015

Abstract Suspension-feeding organisms living in the inter- individuals of C. peruviana were on average smaller than tidal zone experience reduced feeding times associated with subtidal individuals and may be stressed in the intertidal. periodic aerial exposure. The potential morphological and physiological adaptations to this reduced feeding time were investigated for two closely related gastropods, Crepidula Introduction fornicata and Crepipatella peruviana. Intertidal C. forni- cata had heavier gills than subtidal conspecifics, a difference The physical and ecological factors that control spe- mediated by larger gill surface areas and greater numbers of cies’ distributional ranges have recently received height- gill filaments among intertidal individuals of a given size. ened attention due to anticipated climate change and an In contrast, the gills of intertidal and subtidal C. peruviana increased number of biological invasions (Sexton et al. were morphologically indistinguishable. Despite relatively 2009). Because are usually distributed over large larger food-collecting organs, individuals of C. fornicata areas latitudinally, species range limits are most often stud- from the intertidal zone had clearance rates (CR) that were ied on a broad geographic scale (e.g., Sagarin and Gaines not significantly different from those of subtidal conspecif- 2002; Sorte and Hofmann 2004; Kuo and Sanford 2009). ics. In contrast, the CR of intertidal C. peruviana were sig- Such studies have been important for identifying poten- nificantly lower than those of subtidal conspecifics. The low tial biotic and abiotic limiting factors for a host of differ- CR of intertidal C. peruviana may be partially explained by ent species and their potential adaptations at range edges significantly lower measured particle transport velocities (e.g., Fawcett 1984; Zacherl et al. 2003; Lima et al. 2007; across their gills. In the context of feeding, intertidal indi- reviewed by Bridle and Vines 2007; Sexton et al. 2009). viduals of C. fornicata performed at least as well as subtidal However, large distances separating central populations conspecifics, resulting in a population whose adults were as from those at range edges can make the study of limiting large as those found subtidally. This suggests that C. forni- factors and adaptation difficult since a variety of different cata has had a long interaction with the environmental heter- conditions (e.g., climate, temperature, salinity, wave action, ogeneity associated with intertidal life. In contrast, intertidal available substrate, species composition, species interac- tions, and food sources) vary considerably. Communicated by J. Grassle. The intertidal zone represents an abrupt spatial limit over * Casey M. Diederich very short distances for many marine organisms (Holt and [email protected] Keitt 2005). Though some marine species are only found subtidally (e.g., Tomanek and Somero 1999; Collin 2000; 1 Biology Department, Tufts University, Medford, MA 02155, USA Stillman and Somero 2000), and some are found chiefly in the intertidal zone (e.g., Connell 1972; Perez et al. 2009; 2 Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Casilla 567, Valdivia, Chile Bourdeau 2011), a number of species are abundant in both areas (e.g., Dame 1972; Fletcher 1984; Saier 2002; 3 Present Address: Massachusetts Institute of Technology Sea Grant College Program, 292 Main Street, E38‑300, Schaffmeister et al. 2006; Dong et al. 2011; Diederich and Cambridge, MA 02139, USA Pechenik 2013) and so experience a remarkable range of

1 3 1048 Mar Biol (2015) 162:1047–1059 conditions over very short distances. Species whose popu- Crepipatella peruviana (formerly Crepipatella fecunda, lations extend from the intertidal zone (the upper edge of native to the Chilean coast) live both intertidally and subtid- their range) into the adjacent subtidal zone can be studied ally (Gallardo 1979; Collin 2003; Diederich and Pechenik in the context of range boundaries, but on a much smaller 2013). These gastropods eat by collecting particles from spatial scale. At high tide, intertidal organisms experience the water using their modified gill (ctenidium) and trans- many of the same conditions that subtidal organisms do, porting those particles to a food groove, where they are as the two groups are often only meters apart, and a well- concentrated, directed to the mouth (via the food groove in established gradient of stressors exists as one moves from the neck), and ingested (Chaparro et al. 2002). Because C. the subtidal up through the intertidal zone (Menge 1976; fornicata and C. peruviana do not move as adults and have Newell 1979; Denny 1985; Helmuth 1998). Thus, the limit- only limited mobility as juveniles (and as small males) ing factors associated with aerial exposure in the intertidal (Conklin 1897; Chaparro et al. 2001a), individuals living zone and species’ adaptations to those factors can be stud- at the upper edge of their intertidal range have less time to ied by investigating the characteristics of species whose collect food than their subtidal conspecifics. Unless they members are living both intertidally and subtidally. have a mechanism that compensates for reduced feeding The gradients of stressors most closely associated with inter- time, this could potentially limit their vertical distribution, tidal life are usually linked to environmental heterogeneity from especially if slower growth delays a potential escape in size aerial exposure: when compared to subtidal organisms, inter- from mortality in the intertidal zone (Gosselin and Qian tidal organisms experience periodic exposure to desiccation 1997; Hunt and Scheibling 1997). (e.g., Garrity 1984) and to hypoxia (e.g., Brinkhoff et al. 1983), In this study, we investigated the gill morphology and rapid changes in salinity (especially in tide pools—e.g., Morris feeding physiology of C. fornicata and C. peruviana that and Taylor 1983), and greater and more rapid temperature fluc- were exposed to reduced suspension-feeding time at their tuations (e.g., Diederich and Pechenik 2013). However, sessile vertical range edge. We compared various allometric rela- suspension-feeding invertebrates, such as those investigated in tionships of the gill among intertidal and subtidal indi- the present study, are at an added disadvantage if they live inter- viduals living only meters apart at the same field sites for tidally, as they are unable to feed while exposed to the air. both C. fornicata and C. peruviana. We then used labora- A number of studies have documented differences in tory-based clearance rate (CR) experiments to assess the feeding organs or feeding strategies among some popula- extent to which any differences in gill morphology actu- tions of marine invertebrates living in different conditions ally affected the rate at which these organisms cleared food (e.g., Morton et al. 1957; Payne et al. 1995; Ito et al. 2002; particles from the water. In addition, the speed of particle Chaparro et al. 2004; Dutertre et al. 2007). For example, transport across the gill was quantified for C. peruviana Newell et al. (1971) found that although the periwinkle Lit- using endoscopic analysis. Finally, size frequency distribu- torina littorea only feeds while submerged, periwinkles liv- tions were used to estimate maximum growth potential for ing high in the intertidal zone compensated for shorter feed- both species in the intertidal and subtidal zones. ing times with quicker radular rasping rates when compared to those of periwinkles living in the low intertidal zone. Similarly, Drent et al. (2004) found that gill-to-palp ratios Materials and methods (which determine particle sorting efficiency) of the deposit feeding , Macoma balthica, were flexible and depended Collection and maintenance of upon the grain size of the material that the were feed- ing on. In general, intertidal grazers typically change their For all experiments, specimens of C. fornicata were col- feeding activities depending on the duration of aerial expo- lected from Bissel Cove, Rhode Island, USA (41.549920, sure (Newell et al. 1971; Zeldis and Boyden 1979; Little 71.430584), where they can be found both intertidally − 1989; Little et al. 1991; Santini et al. 2004, but not always, and subtidally in large numbers (Diederich and Pechenik e.g., Underwood 1984), but the situation is not as clear 2013). Collections were made for studies of gill morphol- for suspension-feeders (Morton et al. 1957; Griffiths and ogy on April 20, 2011 and for clearance rates (CR) on May Buffenstein 1981; Widdows and Shick 1985; Bayne et al. 22, 2012. Adults (14–40 mm SL) were collected at low tide 1988; Kreeger et al. 1990; Charles and Newell 1997). At from approximately 0.5 m above ( 0.5 m) the mean low + least some suspension-feeders have the ability to compen- lower water mark (MLLW) (hereafter, “intertidal”) and sate for differences in water turbidity with flexibility in the 1 m below ( 1.0 m) MLLW (hereafter, “subtidal”), and − sizes of their feeding organs (Payne et al. 1995; Honkoop transferred to the laboratory in aerated seawater. Speci- et al. 2003; Drent et al. 2004; Dutertre et al. 2007). mens of C. peruviana (scientific name from the World The closely related calyptraeid gastropods Crepidula Register of Marine Species, date accessed: December 3, fornicata (native to the east coast of North America) and 2014) were collected from Pelluco Beach in Puerto Montt

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( 41.478820, 72.914508), Chile, where they can be individually on their original substrate in glass aquaria with − − readily found both intertidally and subtidally (personal aerated, 0.5 µm filtered seawater. For C. fornicata, ambient observation C. Diederich, O. Chaparro). For both species, temperature was 20 °C (field site water temperature at col- intertidal and subtidal individuals were physically sepa- lection time was 17.9 °C) and salinity was 28; for C. peru- rated by ~50 m. Collections were made for the gill mor- viana, ambient temperature was 12–14 °C (similar to field phology studies and clearance rate experiments on October site water temperature at collection time) and salinity was 17, 2012 and for particle velocity experiments on January 30. In order to avoid acclimation to laboratory conditions, 18, 2013. Adults were collected at low tide from approxi- all experiments were performed within 24 h of collection mately 1 m above MLLW (hereafter, intertidal) and 1 (Rising and Armitage 1969; Widdows and Bayne 1971; + − to 2 m below MLLW (hereafter, subtidal), and transferred Mcmahon and Payne 1980). Individuals were not fed after − to the laboratory in aerated seawater. Both of these species collection and prior to experimentation, and intertidal and are protandrous hermaphrodites and both brood embryos subtidal snails experienced identical conditions except that for several weeks prior to larval release. Brooding status intertidal snails were exposed to air for 3 h (C. fornicata) or was incorporated into the clearance rate experiments (see 6 h (C. peruviana) (these times correspond to typical aer- below). ial exposure times at the edge of the vertical distributions All experiments with C. peruviana were conducted of these species, Diederich and Pechenik 2013, personal using females (shell length >26 mm), which use suspen- observation O. Chaparro) prior to experimentation to simu- sion-feeding exclusively to obtain food; smaller individu- late low-tide conditions. als (males and juveniles) can also use the as a major Each was placed in an individual aquarium; for C. means of food collection (Navarro and Chaparro 2002; fornicata, each aquarium (N 95 total) contained 3 L of = Montiel et al. 2005). Both male and female C. fornicata 0.5 µm filtered seawater at salinity of 30 and at 20 °C, and were included for studies, since this species actively sus- for C. peruviana, each aquarium (N 79 total) contained = pension-feeds even as recently metamorphosed juveniles 10 L of 0.5 µm filtered seawater at salinity of 30 and at (Eyster and Pechenik 1988). 14 °C. Air was continuously bubbled into each aquarium to ensure adequate mixing and to maintain a sufficient sup- Gill morphology ply of dissolved oxygen. Pure cultures of either Dunaliella tertiolecta (for C. fornicata) or Isochrysis galbana (for C. For studies of gill morphology, all specimens (N 40 peruviana) were used as the food sources for the snails, and = intertidal and 40 subtidal C. fornicata; 40 intertidal and these microalgae were added to each aquarium to achieve 1 40 subtidal C. peruviana) were rinsed in deionized water initial concentrations of approximately 30,000 cells mL− and immediately preserved in 10 % formalin (diluted with (Mardones et al. 2013). Because we could not add microal- 0.5 µm filtered seawater) buffered with sodium borate. gae and take samples from each aquarium simultaneously, Gills were dissected and photographed under a stereomi- the addition of microalgae (and sampling) was performed croscope fitted with an ocular micrometer. The number sequentially with ~1 min between aquaria. All times were of gill filaments (minimum length 1 mm) in each gill was recorded so that CR could be computed. After aerial expo- subsequently determined. The gill and remaining tissue sure (intertidal only), individuals were allowed ~10 min in were then dried separately on pre-weighed foil at 60 °C for seawater before phytoplankton suspensions were added. 48 h to determine gill and total dry tissue weight. Using One milliliter water samples was taken from each photographs taken under a stereomicroscope and analyzed aquarium at the start of the experiment, and cell concen- using ImageJ (version 1.43; National Institutes of Health, trations were measured (in triplicate) using a model ZM Bethesda, Maryland, USA) for C. fornicata and Image-Pro (C. fornicata) or Z2 (C. peruviana) electronic particle Plus for C. peruviana, the longest five gill filaments were counter (Beckman Coulter Electronics) (incurrent aperture measured from the base to the most distal section of the fil- diameter of 140 µm). Snails were then allowed to filter the ament bulb to determine the maximum filament length for microalgae from the water for 2–4 h before final concentra- each individual; these filaments were adjacent to each other tions were determined. Because of the staggered sampling and nearly identical in size. Finally, the gill surface area approach, we recorded the time between samples, but this was determined using image analysis software by tracing amount of time was not exactly equivalent for each indi- the area of the intact, excised gill of each specimen. vidual. Pilot studies revealed this amount of time to be appropriate in order to detect a reduction in cell concentra- Clearance rates tion without allowing too many cells to be grazed from the suspension. However, clearance rates are notoriously vari- For the clearance rate (CR) measurements, the experi- able from individual to individual in C. fornicata and even mental snails were cleared of all epibionts and maintained within an individual over time (Newell and Kofoed 1977a).

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In addition to measuring algal concentration in all experi- particles driven by ciliary filament actions (not water flow mental aquaria, an additional two (for C. fornicata) or six in the mantle cavity) were measured, only particles in very (for C. peruviana) control tanks were set up with microal- close contact with the gill were selected. The time elapsed gae but without snails to determine settling or growth rates was determined by stepping through the video frame by 1 of algal cells during the experimental period. The clear- frame (NTSC format: 30 frames s− , Ward et al. 1991), and ance rate of each individual was estimated following the the distance travelled by the particles was determined using approach of Coughlan (1969): the width of the gill filaments as a reference (Ward et al. 1991; Beninger et al. 1992; Mardones et al. 2013). Gill CR = V Log C −Log Ct − a /t  e 0 e    filament widths were determined after the particle velocity where V is the volume of suspension, C0 is the initial con- experiments were finished by dissecting the gill out of each centration, Ct is the final concentration, a is the rate at specimen and measuring the filament width with a dissect- which particle concentration changed in the control sus- ing microscope at 40X. The filaments that were measured pension, and t is the duration of the experiment. At the end for width were in close proximity to the location where the of the CR experiments, all snails were then removed from particle movements were recorded. their substrate to determine their brooding status, and dry tissue weights were determined (see above). Maximum size

Particle transport velocity on the gill Maximum size (shell length, SL) was used to estimate the growth potential of snails in the intertidal and subtidal The speeds at which particles moved along the gill fila- zones. For C. fornicata, intertidal (N 206) and subtidal = ments of intertidal and subtidal C. peruviana were meas- (N 203) adult snails (>15 mm SL) were collected in = ured using endoscopy (OLYMPUS model OTV-S4 endo- the spring of 2011, 2012, and 2013, and the longest shell scope, power source OLYMPUS model CLV-10). This dimension of each organism was measured to the near- method has previously proven successful for determining est 0.1 mm with calipers. For C. peruviana, intertidal particle velocity in this and closely related species (Mar- (N 147) and subtidal (N 91) adult snails (>25 mm = = dones et al. 2013; C. fornicata, Shumway et al. 2014). SL) were collected in spring 2012, and the longest shell Freshly collected (see above) intertidal and subtidal snails dimension of each organism was measured to the nearest were removed from their substrates and allowed to adhere 0.01 mm with calipers. Starting at 15 mm for C. fornicata to transparent plastic plates. A small hole (diameter 3 mm) and 25 mm for C. peruviana, snails were grouped into was first drilled in each plate where the endoscope would 2-mm SL classes. later be inserted and particle velocities were measured after specimens were allowed to adhere securely to the plates for Statistical analyses 24 h. This procedure was performed on more organisms than were actually used in the analysis (10 intertidal, 11 Normality and homogeneity of variances were confirmed subtidal) because some of the snails moved slightly after using D’Agostino and Pearson omnibus normality tests and being placed on the substrate and thus did not allow for F tests to compare variances; all analyses were performed accurate placement of the endoscope. To measure particle in GraphPad Prism version 4.0. velocity, each snail was maintained in its own 1-L aquar- For the studies of gill morphology, the size of each snail ium with seawater at salinity of 30 and at 14 °C. Individuals needed to be accounted for before the gills of intertidal 1 were fed I. galbana at approximately 30,000 cells mL− . and subtidal snails could be compared. An information- The tip of the endoscope was inserted through the hole in theoretical approach was used to model selection based on the plastic substrate and into the pallial cavity of the organ- biological hypotheses and previously used models (Burn- ism until the gill could be visualized. Filming was initiated ham and Anderson 2002; Johnson and Omland 2004) to once snails began filtering, and then, a suspension of non- determine the model that best suited each data set. Lin- toxic bright orange particles (2–10 µm diameter, Chaparro ear (y ax b) and power (y axb) models were com- = + = et al. 2001b, 2002) was added to the water near the incur- pared using a corrected Akaike information criterion score rent feeding stream. These particles are easy to visualize, (AICc) (Akaike 1973) (GraphPad Prism version 4.0). and they move along the gill at the same speed as does I. After the appropriate model was selected, regressions of galbana (Mardones et al. 2013). Videos were visualized each gill variable against the dry weight of the snail for on a Trinitron Sony monitor and recorded to VHS for the intertidal and subtidal subpopulations were compared analysis of particle velocity. To determine particle veloc- using either ANCOVA (when the best model was linear) ity, the displacement of orange particles along the gill was or extra sum-of-squares F test (when the best model was measured between two points. In order to ensure that only nonlinear).

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Clearance rates (CR) were standardized for organismal (A) Crepidula fornicata weight as they have been shown to increase as the snails 20 grow (Navarro and Chaparro 2002). For both species, CR was standardized (CRs) to one gram of dry tissue weight using the allometric exponent of 0.56 (Navarro and Chap- 15 arro 2002) to describe the relationship between CR and tis- sue weight for C. peruviana, which was achieved following 10 Bayne et al. (1987): b CRs = (1/W) CRe 5 Intertidal Gill Dry Weight (mg) Subtidal where W is the dry tissue weight of the individual, b is the allometric exponent 0.56, and CRe is the experimen- 0 tally determined clearance rate. This method of standardi- 0 100 200 300 400 500 600 700 Total Dry Tissue Weight (mg) zation has also been used successfully for C. fornicata (Barillé et al. 2006), and the exponent used is very close (B) Crepipatella peruviana to the universal scaling exponent for weight and oxygen 100 uptake in gastropods (0.58–0.62, Marsden et al. 2011). 90 Comparisons of CR among treatments were made using 80 two-way ANOVA. Using our methodology, clearance rate 70 could be underestimated if too much of the algal suspen- 60 sion was grazed (>35 %, Mardones et al. 2013) during the 50 experimental time, so we repeated the above analysis after 40 excluding data points from organisms that cleared >35 % 30 of the algal suspension and the results did not change. Gill Dry Weight (mg) 20 Intertidal Subtidal The individuals of C. peruviana used for the particle 10 velocity experiments differed little in SL (<12 mm range), 0 and particle velocity was not correlated with snail size 0 300 450 600 750 900 1050 (linear regression of SL vs. particle velocity: intertidal, Total Dry Tissue Weight (mg) r2 0.04, F 0.34, p 0.58; subtidal, r2 0.00069, = (1,8) = = = F 0.0063, p 0.94). Thus, particle velocities were Fig. 1 Influence of habitat on the relationship between gill weight (1,9) = = and total dry tissue weight for a Crepidula fornicata and b Cre- not standardized to the size of each snail. The velocities of pipatella peruviana. Each point represents data from one individual. particles were averaged for each individual, and the data Detailed statistical information can be found in Table 1 for intertidal and subtidal subpopulations were then com- pared using an unpaired, two-tailed t test. Size frequency distributions of intertidal and subtidal of intertidal individuals had more filaments than those of populations within each species were compared using con- subtidal individuals (Fig. 4; F 5.69, p 0.0050). (2,76) = = tingency table analyses (χ2 tests). The gills of the largest intertidal C. fornicata were about 80 % greater in surface area and about 30 % greater in the number of gill filaments than those of the largest subtidal Results members of the same species (Figs. 3, 4). The maximum lengths of the gill filaments, though, did not differ among Individuals of C. fornicata and C. peruviana showed dra- intertidal and subtidal individuals (Fig. 2; F 0.95, (2,76) = matically different patterns of gill morphology across the p 0.39). = intertidal–subtidal boundary. In particular, all measures of Unlike C. fornicata, however, the gills of intertidal gill morphology were more strongly correlated with indi- and subtidal C. peruviana showed no significant dif- vidual size for C. fornicata than for C. peruviana (Figs. 1, ferences in weight (Fig. 1; F 0.82, p 0.37 for (1,76) = = 2, 3, 4; Table 1). slope; F 0.094, p 0.76 for intercept), maximum (1,77) = = Intertidal C. fornicata had gills that were as much as filament length (Fig. 2; F 1.45, p 0.23 for slope, (1,76) = = 50 % heavier than those of subtidal members of the same F 0.0026, p 0.96 for intercept), surface area (1,77) = = species, with the differences being greatest among larger (Fig. 3; F 0.99, p 0.38), or number of filaments (2,76) = = adults (Fig. 1; F 10.53, p 0.001). This differ- (Fig. 4; F 0.51, p 0.61). (1,76) = = (2,76) = = ence was at least partially mediated by differences in sur- Clearance rates for both intertidal and subtidal C. forni- face area (Fig. 3; F 4.75, p 0.032), and the gills cata were highly variable. The range of CR for intertidal (1,76) = = 1 3 1052 Mar Biol (2015) 162:1047–1059

(A) Crepidula fornicata (A) Crepidula fornicata

13 400 ) 12 2 350 11 300 10 250 9 200 8 7 150 Length (mm) Intertidal 6 Subtidal 100 Maximum Filament Intertidal 5 Gill Surface Area (m m 50 Subtidal

0 0 0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700 Total Dry Tissue Weight (mg) Total Dry Tissue Weight (mg)

(B) Crepipatella peruviana (B) Crepipatella peruviana 750

20 ) 2 650 m 18 550 16 450 14 Length (mm) 350 Maximum Filament 12 Intertidal Intertidal

Subtidal Gill Surface Area (m Subtidal 250 0 0 0 300 450 600 750 900 1050 0 300 450 600 750 900 1050 Total Dry Tissue Weight (mg) Total Dry Tissue Weight (mg)

Fig. 2 Influence of habitat on the relationship between the maximum Fig. 3 Influence of habitat on the relationship between gill surface length of gill filaments and total dry tissue weight for a Crepidula area and total dry tissue weight for a Crepidula fornicata and b Cre- fornicata and b Crepipatella peruviana. Each point represents data pipatella peruviana. Each point represents data from one individual. from one individual. Detailed statistical information can be found in Detailed statistical information can be found in Table 1 Table 1

velocities across the gills of intertidal and subtidal C. peru- 1 1 1 snails (0.24–1.84 L h− g− ) was somewhat greater than viana varied widely (intertidal range 42–307 µm s− , 1 1 1 = that for subtidal snails (0.03–1.48 L h− g− ). However, subtidal range 77–660 µm s− ), the average velocity of = average CR did not differ significantly between inter- particles moving across gills of subtidal snails was 294.7 1 tidal and subtidal C. fornicata (Fig. 5; two-way ANOVA, ( 164.8 SD) µm s− , whereas the average velocity across ± 1 F 1.87, p 0.17), and reproductive state (brooding vs. gills of intertidal snails was only 153.3 ( 93.8 SD) µm s− = = ± not brooding) also did not have a significant effect on CR (Fig. 6), ~50 % slower than that for subtidal snails. (Fig. 5; two-way ANOVA, F 1.19, p 0.28; interac- The size structures (SL) of intertidal and subtidal popu- = = tion, F 0.73, p 0.40). Conversely, intertidal C. peru- lations of C. fornicata differed significantly χ( 2 38.11, = = = viana had significantly lower clearance rates than subtidal df 14, p 0.0005), as there were generally more larger = = C. peruviana (Fig. 5; two-way ANOVA, F 14.44, (>27 mm) intertidal individuals. However, members of both = p 0.003). Crepipatella peruviana that were brooding had intertidal and subtidal subpopulations reached nearly identical = higher clearance rates than non-brooders (Fig. 5), though maximum SL (44.6 mm subtidally, 43.3 mm intertidal). Con- the difference in CR was not quite significant (F 3.25, versely, C. peruviana attained a maximum SL of 66.2 mm in = p 0.075; interaction, F 0.029, p 0.86). the subtidal zone, a length that was ~34 % larger than that of = = = In C. peruviana, particles were transported across the intertidal C. peruviana (46.4 mm). The size structures of inter- gills of intertidal organisms significantly more slowly than tidal and subtidal populations of C. peruviana also differed those being transported across the gills of subtidal organ- significantly (χ2 85.13, df 20, p < 0.0001), due princi- = = isms (Fig. 6; t 2.38, p 0.028). Though particle pally to more large (>45 mm) subtidal individuals (Fig. 7). 19 = = 1 3 Mar Biol (2015) 162:1047–1059 1053

(A) Crepidula fornicata Drent et al. 2004; Dutertre et al. 2007, 2009; Yoshino et al. 450 2013). For example, Franz (1993) showed that Geukensia

s 400 demissa from Jamaica Bay, New York, living high in the intertidal zone had relatively larger gills than those 350 living in the low intertidal. 300 In C. fornicata, the larger gills of intertidal organisms 250 were not accompanied by a significant increase in clear- ance rate (CR) in our study; intertidal and subtidal C. forni- 200 cata fed at comparable rates. When data from intertidal and 150 Intertidal subtidal snails were pooled, the average CR was approxi- Subtidal

Number of Gill Filament 1 1 100 mately 0.85 L h− g− for C. fornicata, which agrees with 0 values of CR previously found for this species (Newell and 0 100 200 300 400 500 600 700 Kofoed 1977a, b; Shumway et al. 2003; Barillé et al. 2006; Total Dry Tissue Weight (mg) Harke et al. 2011). Though the gill morphology data sug- gest a mechanism by which C. fornicata may compensate (B) Crepipatella peruviana for reduced feeding time in the intertidal, our CR experi- 500 ments were not able to detect any such compensation. Some suspension-feeders show considerable flexibility in feed- 450 ing behavior (Bayne 2004), and compensatory increases 400 in CR in response to aerial exposure have been found in some cases (Morton et al. 1957; Charles and Newell 1997; 350 Marsden and Weatherhead 1999; Galimany et al. 2013); 300 however, many suspension-feeders do not show increased Intertidal CR or ingestion rates as compensation for aerial exposure 250 Subtidal Number of Gill Filaments in the intertidal zone (Griffiths and Buffenstein 1981; Wid- dows and Shick 1985; Bayne et al. 1988; Kreeger et al. 0 0 300 450 600 750 900 1050 1990). For example, Kreeger et al. (1990) found that Geu- Total Dry Tissue Weight (mg) kensia demissa mussels held under intertidal conditions (50 % exposure time) did not compensate for reduced feed- Fig. 4 Influence of habitat on the relationship between the number ing time with an increased ingestion rate when compared of gill filaments and total dry weight for a Crepidula fornicata and to mussels held in subtidal conditions. Charles and Newell b Crepipatella peruviana. Each point represents data from one indi- vidual. Detailed statistical information can be found in Table 1 (1997) confirmed these results, but did find increased CR in mussels held under conditions simulating a much higher tidal level (75 % exposure). Though we did not detect CR Discussion compensation in intertidal C. fornicata, it is important to note the high variability in CR among individuals in our Though C. fornicata and C. peruviana are closely related experiments, which may have prohibited us from detecting (Collin 2003) and have similar ecological niches, our meaningful compensation in this species; high variability in results demonstrate that members of the intertidal range feeding rate has been found for this species before (New- edge populations of these two species have responded very ell and Kofoed 1977a). Though other filter feeders may differently to the feeding disadvantages imposed by peri- periodically stop feeding while submerged (e.g., Cranford odic aerial exposure. The gills of intertidal individuals of C. et al. 2011), it is unknown what would cause C. fornicata fornicata were considerably heavier than those of subtidal to perform in this way while under water in ideal condi- conspecifics, a difference mediated both by a larger over- tions (e.g., normal salinity, oxygen, and temperature, and all gill surface area and a greater number of gill filaments. no predators). No such differences were found for C. peruviana: members In our study, pooled data for clearance rates of C. peru- of intertidal and subtidal populations of that species were viana also fell within the expected range determined by morphologically indistinguishable for the gill parameters previous studies (Navarro and Chaparro 2002; Mardones that we measured. et al. 2013). However, intertidal C. peruviana had a sig- Morphological differences in the feeding organs of other nificantly lower average CR than subtidal C. peruviana, conspecific suspension-feeders from different environ- contrary to what we found for C. fornicata. Since gill ments have previously been reported, mostly in bivalves morphologies did not differ among intertidal and subtidal (e.g., Franz 1993; Payne et al. 1995; Honkoop et al. 2003; C. peruviana, it was surprising to find such a dramatic

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Table 1 Summary statistics for different aspects of Crepidula fornicata and Crepipatella peruviana gills regressed against total dry tissue weight Figure Species Gill parameter Model equation Intertidal and Location a (95 % CI) b (95 % CI) r2 (p)b (difference in subtidal compari- AICc)a son

1a Crepidula forni- Weight (mg) a bX (0.079) ANCOVA Intertidal 0.74 0.029 0.88 + cata F1,76 10.53, ( 0.48–1.98) (0.025–0.033) (<0.0001) p = 0.001 − = Subtidal 0.0099 0.022 0.91 ( 0.69–0.71) (0.019–0.025) (<0.0001) − 2a Crepidula forni- Maximum a*bX (38.97) F test Intertidal 1.90 0.29 0.86 cata filament length F2,76 0.95, (1.42–2.38) (0.25–0.33) (mm) p = 0.39 = Subtidal 2.06 0.28 0.94 (1.77–2.35) (0.25–0.30) 3a Crepidula forni- Surface area a bX (1.932) ANCOVA Intertidal 25.60 0.43 0.71 2 + cata (mm ) F1,76 4.75, ( 5.40–56.61) (0.34–0.52) (<0.0001) p = 0.032 − = Subtidal 32.88 0.33 0.93 (24.18–41.57) (0.30–0.35) (<0.0001) 4a Crepidula forni- Number of fila- a*bX (22.24) F test Intertidal 40.30 0.33 0.81 cata ments F2,76 5.69, (25.45–55.15) (0.27–0.40) p = 0.005 = Subtidal 47.68 0.29 0.90 (37.89–57.47) (0.25–0.33) 1b Crepipatella Weight (mg) a bX (1.34) ANCOVA Intertidal 10.26 0.079 0.68 + peruviana b, F1,76 0.82, (1.01–19.50) (0.061–0.097) (<0.0001) p 0.37= = Subtidal 18.17 0.065 0.39 a, F1,77 0.094, (3.74–32.60) (0.038–0.092) (<0.0001) p 0.76= = 2b Crepipatella Maximum a bX (0.55) ANCOVA Intertidal 13.29 0.0052 0.21 + peruviana filament length b, F1,76 1.45, (11.60–14.98) (0.0019–0.0084) (<0.0028) (mm) p 0.23= = Subtidal 14.97 0.0019 0.018 a, F1,77 0.0026, (12.52–17.43) ( 0.0027–0.0064) (0.41) p 0.96= − = 3b Crepipatella peru- Surface area a*bX (0.64) F test Intertidal 41.05 0.38 0.31 2 viana (mm ) F2,76 0.99, ( 6.63–88.72) (0.19–0.57) p = 0.38 − = Subtidal 37.51 0.40 0.23 ( 18.50–93.51) (0.17–0.64) − 4b Crepipatella peru- Number of a*bX (1.46) F test Intertidal 64.80 0.29 0.30 viana filaments F2,76 0.51, (8.41–121.20) (0.15–0.43) p = 0.61 = Subtidal 104.7 0.21 0.16 (1.05–208.30) (0.054–0.37) a As compared to the competing model (only power and linear models were compared) b Test for zero slope. Linear models only

difference in CR between those two groups. Moreover, Assuming that decreased particle velocity across the the difference was not in the direction that we had initially gill surface also reflects a reduced capacity of the gill cilia anticipated. Our endoscopic results indicate that intertidal to collect food, the slower CR for intertidal individuals of individuals started to collect phytoplankton immediately C. peruviana could be in part due to a decreased particle upon immersion. Thus, clearance rates of intertidal indi- velocity along the gills of intertidal individuals. Slower viduals were not artificially low because of a reluctance of particle velocity could be the result of reduced ciliary beat these snails to begin feeding after they were submerged. frequency on the gills of intertidal C. peruviana, something We found that brooding individuals of C. peruviana had that could be examined in a future study. Overall, the parti- faster clearance rates than non-brooding individuals, and cle transport velocities found in this study were slower than 1 to nearly the same degree as was found by Mardones those previously found in C. peruviana (~1,400 µm s− , et al. (2013); this trend was observed among intertidal and Chaparro et al. 2002). However, our experiments were subtidal individuals. performed at cooler temperatures than in Chaparro et al.

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(A) Crepidula fornicata (2002), and C. peruviana in our study were first removed 1.2 from their substrates and transferred to plastic plates, both Intertidal of which may have contributed to the slower particle veloc- Subtidal 1.0 ities that we found. 25

) The intertidal zone is a particularly stressful place to live

-1 0.8

g 28 (e.g., Brinkhoff et al. 1983; Morris and Taylor 1983; Gar- 20 21 -1 rity 1984; Petes et al. 2007; Harley et al. 2009; Miller et al. 0.6 2009; Diederich and Pechenik 2013) for sedentary marine

CR (L h 0.4 organisms, and physiological stress has previously been associated with reduced performance (i.e., feeding rate) in 0.2 some marine invertebrates (Abel 1976; Menge 1978; Wid- dows et al. 1981; McCormick et al. 1998). The pattern of 0.0 Brooding Not Brooding CR and particle velocity transport across the gill in addition Reproductive State to the pattern of size distribution (subtidal > intertidal) in C. peruviana suggests that intertidal individuals could be (B)Crepipatella peruviana stressed in relatively poor physiological condition. Indi- 2.0 viduals of C. peruviana may of course have physiological 1.8 adaptations for maximizing energy gain in the intertidal 16 zone that we did not quantify but should be studied further. ) 1.6 -1

g Energetic compensation for aerial exposure time in other 1.4 12 -1 1.2 species has been linked to a number of other processes not explored here, including changes in metabolic rate, gut pas- 1.0 23 sage time, and absorption or assimilation efficiency (Grif- CR (L h 0.8 28 fiths 1981; Kreeger et al. 1990; Charles and Newell 1997; 0.6 Marshall and McQuaid 2011). Additionally, clearance rate 0.4 and condition index may not be tightly coupled for some 0.2 species: suspended virginica with 0.0 BroodingNot Brooding smaller gills and lower CR than bottom oysters were actu- Reproductive State ally found to have higher condition indices (Comeau 2013). If larger gill size in intertidal C. fornicata is driven by adaptive plasticity, what mechanisms might control such a Fig. 5 Clearance rates of intertidal and subtidal a Crepidula forni- cata and b Crepipatella peruviana. Sample size is indicated in each change? Like the compensatory feeding of the Geu- bar; error bars represent SEM. Asterisks denote significant differ- kensia demissa (Charles and Newell 1997, see above), C. for- ences in CR between intertidal and subtidal individuals, two-way nicata may experience a threshold shore level above which ANOVA, p < 0.05

) 700 -1 Intertidal 600 Subtidal m sec

µ 500 ( p = 0.028 400

300

200

100 Particle Velocity

0 1 2345678910 1234567891011 Intertidal Subtidal Individual Habitat

Fig. 6 Rate ( SEM) at which intertidal and subtidal Crepipatella in the left panel, and mean particle velocities of all individuals peruviana moved+ particles across the gill toward the food groove. grouped by habitat are shown in the right panel (result of unpaired t Mean particle velocities along the gills of each individual are shown test is shown above the bars)

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(A) Crepidula fornicata eurythermal (Diederich and Pechenik 2013) and tolerant 16 of long periods of aerial exposure (Hoagland 1984), traits Intertidal necessary for intertidal life, though intertidal individuals in 14 Subtidal some areas may be living close to their thermal maximum ) 12 (Diederich and Pechenik 2013). As it relates to feeding, the 10 intertidal C. fornicata in our study may be better equipped to cope with the disadvantages associated with aerial expo- 8 sure than those of C. peruviana. This may help to explain the 6 ability of intertidal C. fornicata to attain sizes equivalent to Population (% 4 those of subtidal snails, while intertidal C. peruviana did not 2 seem to grow to be as large as subtidal C. peruviana. Our studies highlight the value of investigating organ- 0 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 isms of the same species from intertidal and subtidal zones Size (mm shell length) in the context of range boundaries. At a single field site, some organisms will experience conditions associated with “cen- (B) Crepipatella peruviana tral” (subtidal) populations, while conspecifics only meters 16 away can be characterized as experiencing “range edge” con- Intertidal 14 ditions (intertidal). Additionally, abiotic conditions in inter- Subtidal

) tidal and subtidal areas may be nearly identical when the tide 12 is in, and when the tide is out, the suite of abiotic conditions 10 that change is both easily measurable (time emersed, temper- 8 ature, water lost, etc.) and well characterized (Newell 1979; Denny 1985; Helmuth 1998; Helmuth and Hofmann 2001). 6

Population (% Finally, our results may have implications for the rela- 4 tive success of these species as it relates to their potential 2 for invading new areas. In fact, C. fornicata is an extremely successful invasive species along European coastlines (and 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 other areas, Blanchard 1997), though they are not always Size (mm shell length) found intertidally in the invaded area, while C. peruvi- ana has not been found outside its native range. While the Fig. 7 Size distributions for intertidal and subtidal individuals of repeated importation of C. fornicata into European waters a Crepidula fornicata collected from Bissel Cove in Narragansett (e.g., on shipments, Blanchard 1997) caused their Bay, RI, USA, and b Crepipatella peruviana collected from Puerto initial introduction, the reasons for its remarkable success Montt, Chile. Numbers on the x-axis represent the lower end of each size class (15 15–17 mm). a Frequency distributions of intertidal as an invasive species are less clear (Dupont et al. 2006; (N 206) and= subtidal (N 203) subpopulations are significantly Viard et al. 2006; Blanchard 2009; Bohn et al. 2012). When different= (χ2 38.11, df 14,= p 0.0005), though the snails reach = = = viewed in the context of habitat colonization, the ability of similar maximum sizes. b Frequency distributions of intertidal C. fornicata to perform well in the stressful living condi- (N 147) and subtidal (N 91) subpopulations are significantly dif- ferent= (χ2 85.13, df 20,= p < 0.0001), with subtidal individuals tions that characterize the intertidal zone may be contribut- reaching a =maximum size= 34 % greater than intertidal individuals ing to their relative abilities to invade new areas.

Acknowledgments In addition to the anonymous reviewers, we it is advantageous to have a relatively larger gill. However, thank R. Burns, A. Franklin, and K. Boisvert for helpful comments on the manuscript. We thank Nelson Dow for help in dissecting snails, intertidal individuals of C. fornicata are usually relegated measuring gills, and counting gill filaments. We thank C.J. Segura to the mid- to low intertidal zone (Diederich and Pechenik and V.M. Cubillos for help in collecting of C. peruviana and running 2013), and even short bouts of aerial exposure may trigger a CR experiments, and M.V. Garrido for help with CR and endoscopy shift in resource allocation toward growing relatively larger experiments in Chile. Portions of this research were supported by a Tufts University grants-in-aid of research award to CMD and Fonde- gills. It is interesting that intertidal C. fornicata had larger cyt-Chile Grant 1100335 to ORC. gills but similar CR when compared to subtidal conspecif- ics, while intertidal C. peruviana had reduced CRs relative to those of subtidal individuals despite no difference in gill References sizes. Individuals of C. fornicata may have a longer history of association with the environmental heterogeneity found Abel PD (1976) Effect of some pollutants on the filtration rate of Myt- in the intertidal zone. Indeed, C. fornicata is also relatively ilus. Mar Pollut Bull 7:228–231

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