Predation on Planted and Wild Bay Scallops (Argopecten Irradians Irradians) by Busyconine Whelks: Studies of Behavior Incorporating Acoustic Telemetry

Quantifying predator-prey interactions and gaining insights into predator behavior are crucial for optimizing restoration strategies; yet, such knowledge is often lacking for marine invertebrates. We examined potential impacts of predation by channeled (Busycotypus canaliculatus) and knobbed whelks (Busycon carica) on natural and planted populations of bay scallops in the Peconic Bays, New York, through laboratory and eld investigations. Mean rates of predation by small channeled whelks were low: 0.06 and 0.005 scallops d -1 for adult and juvenile scallops; respective lab predation rates of small knobbed whelks on juvenile scallops were 24x higher. Channeled whelks usually did not damage shells of scallop prey (86%), but knobbed whelks typically notched the ventral shell margin (73%). In eld plots where scallop densities were manipulated via removals/plantings, whelks consumed ~2% of ~19,100 planted juveniles; crabs and presumably nsh consumed over 40% in all trials overall. Acoustic telemetry revealed that tagged channeled whelks moved shorter distances and spent more time in plots planted with scallops versus those without scallops. Unexpectedly, whelks spent more time in low vs. high density plots, but consumed far more scallops in the latter. In trials without scallops, whelk movement rates were 5x higher, presumably due to increased exploratory behavior. Overall, whelks were most active during crepuscular hours and during periods of increasing wind speeds. Our results, combined with population abundance data, suggest that whelks (especially B. carica) are drawn to high density scallop plantings and may be important causes of bay scallop mortality in the context of restoration efforts.


Introduction
Predation plays a central role in controlling the structure of aquatic and terrestrial communities (Paine 1966;Connell 1970;Janzen 1970) and is generally considered to be the primary cause of mortality of juvenile marine invertebrates (Jensen and Jensen 1985;Eggleston and Armstrong 1995;Hunt & Scheibling 1997;Gosselin & Qian 1997;Newell et al. 2000). Understanding spatial and temporal variability of predator-prey dynamics and how predator behavior changes with prey availability/attributes and environmental factors is vital to better understanding of community dynamics (Martin et al. 2015; Bastille-Rousseauet al. 2016). Resource availability across an animal's landscape, especially at ner resolutions, is one of the primary factors that in uences animal behavior. In particular, heterogeneous landscapes with spatially disparate resources can result in shifts in predator migration modes (Jonzén, et al. 2011) and behavior can subsequently shape community structure and species coexistence (Hilborn 1975;Holt 1984). Predator movements and foraging behavior/ability (Grigaltchik et al. 2012; Hammerschlag et al. 2006) can also be mediated by diel, seasonal or episodic environmental factors, including temperature (Sanford 2002 (Robinson et al. 2011). In general, these processes are less well known for marine taxa, especially in the eld.
In the context of shell sh restoration, understanding dynamics of predator-prey size relationships (Hughes and Seed 1981, Arnold 1984, Boulding 1984) and behavior of predators (e.g. if they are drawn toward high density plantings: Boulding and Hay 1984, Barbeau et al. 1996) is critical to the success of restoration efforts. Field growout of juvenile shell sh is the most common approach followed in commercial aquaculture and restoration efforts (Castagna 2001, Goldberg et al. 2000. Therefore, when animals are planted without protective enclosures or exclosures, appropriate sizes must be seeded to increase the probability of survival, e.g. with Mercenaria mercenaria (Castagna 1984), Ruditapes philippinarum (Cigarría and Fernandéz 2000), Mya arenaria (Beal et al. 1995) and Patinopecten yessoensis (Uki 2006).
We have worked to restore northern bay scallops, Argopecten irradians irradians (Lamarck 1819), in the Peconic Bays of eastern Long Island, NY, USA, over a period of 30+ years (Tettelbach and Wenczel 1993;Tettelbach et al. 2013Tettelbach et al. , 2015 after populations were decimated by brown tide (Aureococcus anophagefferens) algal blooms in the mid-1980's (Cosper et al. 1987). Our strategy has been to plant millions of juvenile, hatchery-reared scallops that ultimately serve as broodstock. In recent years, we have focused on deploying scallops in nets, but we also conduct extensive unprotected (free) plantings of scallops directly to the bay bottom (Tettelbach and Smith 2009). The latter approach is riskier, but much less expensive. The target size (35-40 mm) for free planting is one which affords a partial refuge from predation by the majority of crab species/sizes with which northern bay scallops co-occur (Tettelbach 1986). However, sea stars (Tettelbach and Wenczel 1993), oyster drills (Ordzie and Garofalo 1980) and n sh (Myers et al. 2007) have been documented to cause extensive mortality of juvenile and adult bay scallops in some areas.
Channeled (Busycotypus canaliculatus) and knobbed whelks (Busycon carica) also may be important predators of Peconic bay scallops, as suggested by tethering experiments (Carroll et al. 2010;Mladinich 2017) and our direct eld observations. These two commercially harvested gastropods are large, longlived species (Udelson 2012; Peemoeller and Stevens 2013; Fisher and Rudders 2017; Angell 2018) that are regarded as important predators of clams and oysters (Magalhaes 1948;Peterson 1982, Walker 1988Kraeuter 2001), but much of the basic ecology of these species is not well understood.
In this study, we examined the potential impact of predation by channeled and knobbed whelks on Peconic bay scallops, with an eye to informing restoration strategies, by employing manipulative experiments and by drawing on predator abundance data (Tettelbach et al. 2015). Feeding rates were estimated from laboratory and eld studies; predator-prey size relationships were also examined via opportunistic eld observations. We used acoustic telemetry to investigate how channeled whelk behavior and movement were affected by environmental factors (e.g. tide direction, time of day), at different scallop densities, to provide novel insight into the underlying mechanisms that drive predatory behavior. We hypothesized that tagged whelks would: (1) be drawn to scallops planted at densities well above ambient levels, (2) spend more time in patches of high vs low scallop densities, and (3) exhibit more encamped (less exploratory) behavior at higher scallop densities. We also examined whether (4) whelks would be most active at dusk, as observed previously with channeled whelks (Magalhaes 1948 (Tettelbach & Wenczel 1993). Low and high experimental densities, respectively, represented a relatively high natural population density and the approximate minimum free-planting density that we currently target (Tettelbach et al. 2013(Tettelbach et al. , 2015. Predation rates determined in lab experiments were considered maximal since no alternative prey were available and the probability of scallops avoiding predation was low. Laboratory experiments were conducted in plastic sh totes (66 cm L x 47.6 cm W x ~27 cm D) held within berglass raceways at the Cornell Cooperative Extension lab in Southold, New York, USA; temperature of the air and owing seawater (from Cedar Creek) were both at ambient levels. Tanks were independently supplied with water at a ow rate of 5.8 +/-0.73 l sec -1 . Totes were tted with string inside the perimeter of all sides to prevent whelk escapement. Prior to starting a given predation trial, totes were cleaned with fresh water, rinsed, and then lled with beach sand (sieved to 6-8 mm, then dried) to a depth of 18 cm. This depth of sand was found to be necessary for successful predation on bay scallops by channeled whelks in the laboratory (B. Udelson, unpub. data). After ow rates were standardized, individual whelks were added to each tote and allowed to acclimate for ~24 h; usually individuals were completely buried in the sand within 10 min. Whelks, which had been potted by a commercial sherman in Gardiners Bay and/or collected by divers in the eastern Peconic Bays, were starved for 2 weeks (Rilov et al. 2002) in a owing seawater tank prior to use in experiments -for which they were used just once. Scallops were obtained from nets in Orient Harbor (Tettelbach & Smith 2009) or collected by divers from nearby natural populations just before the start of each experimental trial. Scallops were spread relatively evenly over the surface of the sediment at 24 per tote (=75/m 2 ) and 3 per tote (= 10/m 2 ) for the high and low density treatments, respectively. Whelks were allowed to feed on scallops for 6-7 d. For a given experimental trial, up to 12 tanks were run simultaneously for a given scallop size: 5 replicates and 1 control (scallops with no whelk) for each of the two density treatments. Six and two trials, respectively, were run for channeled and knobbed whelks (Table S1).
At the time scallops were introduced to the totes, dissolved oxygen (DO), salinity (S) and temperature (T) were measured with a YSI Pro 2030 multi-probe meter and/or a Hach meter (HQ 40d). A submersible Tidbit ® automatic temperature recorder was also placed in one of the tanks (except in 2012 experiments) to measure water temperature every 30 min. Totes were inspected every 1-2 d to monitor scallop mortality; water quality measurements were also made at this time. T, S, and DO through all lab experiments ranged from 10.9 -26.8 ºC, 26.4 -30.6, and 4.59 -6.37 mg l -1 , respectively.
When dead scallops were rst seen, their SH, orientation and position in totes were noted; shells that contained most/all of the tissues and/or had a strong odor were considered to have died from causes other than predation. At the end of a given experimental trial, SH of predated scallops (mostly/completely devoid of tissue and without a strong odor) were measured to the nearest mm, and damage (if any) to each shell was characterized (shells chipped, cracked or notched -see below). After experiments had ended, gender of whelks was determined on the basis of whether a penis was present or absent (Gendron 1992  At the completion of each eld experiment, we derived an estimate of the numbers of scallops eaten by whelks and other predators by examining damage to cluckers (recently dead scallops without tissue but with shell valves still articulated) that were collected by divers from inside each of the four 10 m x 10 m sectors and from beyond the perimeter of the grid (out to ~3 m to the west and east, and ~5 m to the north and south). Predation was attributed to different groups on the basis of characteristic traces of predation (Tettelbach 1986, Peterson et al. 1989 Barbeau et al. (1994), channeled whelks (this study).
Assignment of predation to different groups is complicated by the fact that a given species may employ various tactics relative to the size of the prey and thus leave different traces (Elner 1978, ap Rheinallt and Hughes 1985, Tettelbach 1986). Despite these limitations, analysis of predatory traces permitted insights into the relative contribution of different predators to losses of planted scallops.

Whelk Movement/Behavior in the Field in Response to Scallop Plantings
Acoustic telemetry was used to examine the movement of channeled whelk in eld predation trials. Concurrent to lab experiments, a total of ve eld trials were run at the site off Cedar Beach, between 7 October -2 November 2013: two in which all scallops were removed from the grid (controls) immediately before tagged whelks were deployed ( rst and last trials) and three in which hatchery-reared scallops were planted at low (10 ind m -2 ) or high (75 ind m -2 ) densities in each of two 10 m x 10 m sectors (Fig.   S1, Table 1). Prior to the rst whelk deployment on 7 October, mean natural scallop densities were quanti ed in the grid (juveniles = 1.76 ± 0.31 ind m -2 ; adults = 0.17 ± 0.08 ind m -2 ). As the predominant direction of tidal ow was N-S, and because we wanted to factor out other potential differences in bottom type/depth/availability of alternate prey among the grid sectors, we changed the position of the low and high-density scallop treatments in successive trials by moving scallops between sectors (by divers) and adding additional scallops when necessary ( grain size analyses were conducted on samples taken at the start of eld experiments (Appendix S1).
Monitoring of whelk position and time spent in respective grid sectors was done using Vemco® 69Khz (V9-1L) acoustic tags and ve time-synchronized VR2W receivers placed in a pentagonal array (Fig. S1, Appendix S1). For each experimental trial, 10 whelks were individually tted with tags that transmitted unique identi cation codes every 120 s; spatial position of tagged animals within/beyond the receiver array was calculated via hyperbolic positioning (Smith 2013). In this way, we were able to determine: (1) rates of movement; (2) how much time whelks spent in low and high-density planting sectors; and (3) diurnal differences in movement. Expected transmission range for Vemco tags was estimated at 200-300 m through calibration trials, so that positions of whelks that moved well beyond the 20 x 20 m experimental grid (= natural scallop density area) could be determined.
Whelks and scallops used in eld experiments were comparable to the smaller respective size groups used in the lab; tagged whelks ranged in size from 104-140 mm SL, with most between 130-137 mm SL (Tables S1 & S3), while mean SH of planted scallops was 28.1 mm (SE = 0.2; n = 149) on 15 October and 31.1 mm (SE = 0.2, n = 100) on 30 October. Whelks were starved for 2 weeks prior to release; < 4 days prior to eld deployments, individuals were each tted with unique acoustic and 'burial' tags (Tettelbach et al. 1990). The latter allowed us to locate whelks if/when they were buried in the sediment (which was the case for virtually all tagged whelks during the daytime). Acoustic tags were secured to the dorsum of each whelk by rst using superglue to attach a Velcro strip to the shell, then inserting the acoustic transmitter into a Velcro sleeve which was attached to the rst Velcro piece (Brousseau et al. 2004). The proximal end of 'burial' tags was glued to the dorsum of whelk shells while a cork was glued to the distal end. Retention of both types of tags was tested in the lab prior to eld deployments; none were lost there or during any of the eld experiments.
Just prior to deploying scallops and tagged whelks into the eld plot, wild scallops and whelks were removed by divers during parallel transects across each of the four 10 m x 10 m sectors; counts and measurements were then done on the boat (Table S2) Harbor (Tettelbach unpub data). Sizes of wild whelks (Table S2) were somewhat larger than our tagged animals. Wild scallops also were larger (Table S2) than planted ones and had fewer growth checks, so it was easy to differentiate the two groups.
For the rst of the eld predation experiments, a total of 17,000 scallops, which had been obtained earlier that day from nets in Orient Harbor, were distributed from the boat into each of the four sectors at targeted densities. Divers then manually moved scallops that had drifted outside the grid into the nearest sector. Next, counts of scallops were done within 6-8 haphazardly placed 1 m 2 quadrats in each of the sectors to document actual planted scallop densities. For subsequent experiments, in which low-and high-density treatments were rotated among sectors, a total of 4681 scallops from beyond the perimeter were relocated to adjacent sectors (Table 1) and, for the experiment begun on 28 October, an additional 2100 hatchery-reared scallops were planted into Sector 2. Thus, an overall total of 19,100 scallops was planted during eld experiments.
Within 1.75 h of when scallop densities had been achieved for respective grid sectors in each of the experimental trials, 10 tagged whelks were manually placed in a circle around the center of the grid, with the anterior end of each facing away from the central acoustic receiver. Originally, we had planned to run experiments for 6 d, but these were shortened to 2-3 d after it was determined that whelks released in the rst control trial had moved beyond the range of the experimental array in less than 5 h (and had to be manually located with a hydrophone hung from the boat). At the end of all other eld trials, divers systematically swam 1 m wide transects in each of the 4 sectors to collect tagged whelks as well as scallop cluckers; searching was done beyond sector perimeters when necessary. Since all 10 tagged whelks were successfully recovered following each trial, reuse of all transmitters on different whelks was possible for subsequent trials. After the completion of all ve telemetry experiments, data were downloaded from the acoustic receivers and sent to Vemco for position calculations (Smith 2013).
Although we have data for longer time periods, we used only the rst 24 h for analyses of spatial position as we had the highest degree of con dence in these position estimates.

Opportunistic Observations of Predator-Prey Size Relationships
Whenever we encountered bay scallops being preyed upon by whelks in the eld, either in our planted area off Cedar Beach, Southold or during dives in other areas in the Peconic Bays, whelk SL and scallop SH were measured to the nearest mm and observations were made on mechanics of predation.

Statistical Analyses
Rates of predation by whelks (channeled and knobbed) on scallops in laboratory experiments were rst examined with respect to water temperature, via linear regression. Where data were not statistically different, they were pooled and compared via 2-way ANOVA to examine differences in predation rates versus scallop density and size. For eld predation trials, numbers of cluckers within sectors planted at high and low scallop densities were compared via χ 2 tests.

Hidden Markov Model setup
To understand the in uence of environmental factors and prey availability on whelk behavioral patterns across space and time, we employed discrete-time Hidden Markov models (HMM) to analyze acoustic telemetry data separately for each of the ve trials. HMM is a class of time series models that is likelihood-based and is considered a special case of State Space Models (Patterson et al. 2009). HMMs consist of two components to describe animal behavior: observable states and a non-observable state (also referred to as "hidden" states), but makes inference on the unobservable state from either relocation data or movement metrics (i.e. turning angle and step length) from the Markov process ( To assign an individual's activity level for each trial, we used the empirical cumulative distribution function on total distance traveled; individuals that exceeded the median value were considered to have high activity/dispersal and vice versa. The Akaike information criterion (AIC) was used to determine the best tting model for whelk movement in each trial (Burnham and Anderson 2002). Additional details on HMM setup and tting procedures can be found in the Appendix.
We tested the null hypotheses of no differences between control (no scallops) and experimental (scallops present) trials for: (1) time spent within vs. outside the experimental plot, (2) total distance travelled (encamped vs exploratory) behavior and (4) day and night movement distances with Wilcoxon rank-sum tests. To determine if the encampment of whelk differed among scallop densities (natural, low planted, high planted: hypothesis (3)), we used a Kruskal-Wallis test (Hollander and Wolfe 1973). A Post-hoc multiple comparisons Conover test was used to determine if there were pairwise differences in whelk residency at different scallop densities (Conover and Iman 1979). A Holm correction was used to control for familywise type 1 error with an assumed familywise error rate of = .05. The Conover-test was conducted in the conover.test R package (Dinno 2017). All statistical and modelling analyses were conducted in R (R core team 2020).

Laboratory Experiments
Mean rates of bay scallop predation by small channeled whelks in the 6 lab experiments were low: 0.06 and 0.005 scallops eaten whelk -1 day -1 for large and small scallops, respectively (Table S1). During the 27 August -3 September 2013 trial, the rate of predation by jumbo whelks on large scallops was higher than that of smaller whelks (0.119 vs 0.071 scallops eaten whelk -1 day -1 , respectively: Table S1), but a two-tailed t-test comparing these rates showed no statistical difference (t = 0.605, p = 0.562). For small knobbed whelks, the overall mean predation rate on small scallops was 0.12 scallops eaten whelk -1 day -1 : 24x higher than that by small channeled whelks ( =0.0055 scallops whelk -1 day -1 ). The highest individual consumption rates were 5 scallops eaten over a 7 d period (0.71 scallops d -1 ), for a 131 mm SL channeled whelk feeding on large scallops (late July -early August 2012) and a 136 mm SL knobbed whelk feeding on small scallops (late October 2014).
Neither scallop size nor density was shown to affect the rate of predation by channeled whelks in the laboratory: two-way Anova (scallop size: F = 2.54, p = 0.117; scallop density: F = 1.27, p = 0.265; scallop size x scallop density: F = 0.67, p = 0.418). Nevertheless, the total number of large scallops eaten by channeled whelks in all trials (9) was greater than the number of small scallops (1) (Table S1). Although these differences in predation rates may re ect higher water temperatures at which experiments were run for large scallops, the much higher rate of byssal attachment by smaller scallops to the walls of totes, in both control and experimental treatments, may have precluded whelks from preying on these individualsthus effectively reducing the numbers available to be preyed upon. Overall rates of predation were generally higher when water temperatures were higher, except during the 22-26 August 2012 trial when water temperature was ~26.8 ºC. Linear regressions of channeled whelk predation rate (# scallops eaten per whelk during a given trial) versus minimum and median water temperature for a given trial, for all of the trials except the one run from 22-26 August 2012, were both statistically signi cant: (linear regression,R 2 = 0.319, p = 0.037 and R 2 = 0.326, p = 0.033, respectively).
When the latter trial was included and the linear regression run as median water temperature (temperature was only recorded at the end of the 22-26 August 2012 experiment), it was not signi cant: R 2 = 0.210, p = 0.131. Since there were only two trials for knobbed whelks, a linear regression was not done; however, the data strongly suggest that predation rates by this species were also greater at higher temperatures: 0.208 vs 0.042 scallops eaten per whelk per day at temperature ranges of 14.  (Table S1). Knobbed whelks most commonly (8/11 = 73%) notched the ventral margins of predated scallop shells (Table S1), where a thin (< 2 mm) chip, parallel to the hinge line and often only from just one of the valves, was evident (Fig. S2). Of the scallops preyed upon by channeled and knobbed whelks, respectively, hinges were disarticulated in 3/14 (21%) and 5/11 individuals (45%).

Field Experiments
An overall total of 1067 hatchery-reared cluckers were recovered over the course of the three eld predation experiments (ending 18, 24 and 30 October 2013: Table S4). These included 879 from inside the four sectors (including 8 planted scallops seen being eaten by knobbed whelks) and 188 from just beyond the grid perimeter (the latter were only quanti ed after the last experiment). The total of 1,067 cluckers, out of 19,100 planted scallops, represents a minimum predation rate of 5.6%. The total number of live scallops recovered on 30 October, following the last eld predation trial, was 10,404; thus, the maximum rate of losses due to predation was inferred to be 45.5%. In contrast, only two wild cluckers were found while clearing the grid of scallops before starting the rst predation experiment on 16 October 2013.
Higher numbers of cluckers were recovered inside sectors planted with high vs low densities of scallops in each of the three eld predation trials (χ 2 = 26.78, 72.25, 12.19; p < 0.0005; 1 df). Similarly, on 30 October, pooled counts of cluckers from inside and adjacent to high density sectors were higher than those for low density sectors (χ 2 = 14.96; p < 0.0005; 1 df).

Opportunistic Observations of Predator-Prey Size Relationships
A total of 20 whelks preying on scallops were observed directly between 2011-2015: four by channeled whelks (one 0+ yr scallop and three 1+ yr individuals) and 16 by knobbed whelks (eight 0+ yr and eight 1+ yr scallops) (Fig. 1, Table S6). A linear regression of predator-prey size was statistically signi cant for knobbed whelks (whelk SL = 126.822 + (1.015 * scallop SH); R 2 = 0.463, p = 0.004) but not for channeled whelks: (whelk SL (mm) = 249.063 -(1.437 * scallop SH; R 2 = 0.828, p = 0.09). For 7 predation events which we examined closely, knobbed whelks completely engulfed the shells of 4 scallops (two juvenile, two adult) as did 2 channeled whelks (1 juvenile, 1 adult). In another instance, a channeled whelk inserted its outer shell lip between the ventral margins of an adult scallop shell, while the hinge of the shell was held rmly in place by the foot (and perhaps the operculum).

Whelk Movement and Behavioral Response to Scallop Field Plantings
Visual observations by divers revealed that tagged and untagged whelks exhibited similar movement (searching) behaviors, where most oriented their proboscis into the direction of the prevailing current and moved with a sweeping, side to side motion. Tagged whelks exhibited this behavior within 5 min of deployment in all eld trials. In the rst eld predation trial (16 October 2013), large numbers of wild untagged whelks were seen inside the grid within 0.5 h after scallops were planted from the boat -even after we had just removed all visible animals from the area. At this time, nine whelks (1 channeled, 8 knobbed) were seen in the process of preying on scallops; several scallop cluckers which had just been eaten by whelks (as evidenced by the heavy mucus coating of the shell) were also noted.
Acoustic telemetry eld trials yielded very high resolution tracking results for individual tagged whelkswhich allowed us to continuously track all animals for 48 h. Thus, we were able to determine that tagged whelks displayed different movement and occupancy patterns in control trials (no scallops) compared to those with planted scallops (Fig. 1). When no scallops were present, whelks moved out of the experimental grid quickly, often within 4-5 h after their initial release. Thus, the total amount of time that whelks spent inside the grid was signi cantly lower in control trials versus those with planted scallops (Wilcoxon rank-sum , W=134, p<0.001: Fig. 2). Path analysis showed that, on average, the total distance traveled by tagged whelks (sum of the segment trajectories for individuals) was considerably higher in control trials (447 m) compared to those when scallops were present (90.7 m): Wilcoxon rank-sum, W = 556, p< 0.001 (Fig. 3). Average displacement (distance travelled by whelks between the rst and last points of individual trajectories), over the rst 48 hr, were 43.3 ± 8.0 and 20.1 ± 3.2 m, respectively, for whelks in control and planted trials. Similarly, average rates of whelk movement were higher in control trials (10.55 ±1.52 m h -1 = 0.29 ±.036 cm sec -1 ) versus those with planted scallops (3.37 ± 0.23 m h -1 = 0.09 ± 0.006 cm sec -1 ) (Wilcoxon rank-sum; W=52, p<.001). These results corresponded to those for behavioral state, where whelks in control trials spent more time exhibiting exploratory behavior (10.8%-84.8%; average = 33.3%) compared to whelks in predation trials (0.80%-29.4%; average = 12.1%) (Fig. S3).
In general, whelks remained in an encamped behavioral state for most of a given day, thus behavioral state probabilities only varied in a moderate way with time of day; this was true in all eld trials except in trials 3 and 4 (see Fig. 4 C-D). Whelks were seen to be most active during early evening/twilight hours (15:00-20:00 h) and least active from 00:00-10:00 h, in all trials (Fig. 4). Not unexpectedly, marked diel differences in total distances traveled were exhibited by tagged whelks in both control (Wilcoxon ranksum, W= 83, p < 0.001) and predation (Wilcoxon rank-sum, W= 190, p < 0.001) trials (Fig. 5). Surprisingly, however, whelks traveled greater distances in daytime versus nighttime hours.
The average amount of time whelks spent within each scallop density plot varied considerably among predation trials (Fig. 6). In trials 2 and 4, whelks exhibited no differences in time spent among all scallop densities (Fig. 6 A,C); however, in trial 3, whelks spent the majority of their time in sectors with low densities of planted scallop compared to those with high planted or natural densities (i.e. outside the grid) (Fig. 6B). For all 3 experimental trials, the encamped behavior was quite common in both the low and high planted scallop densities. However, in trial 3, there was some evidence of whelks spending more time in the lower density scallop grids and also a higher probability of displaying exploratory behaviors (Fig. 7).
Considerable differences of supported covariates that in uenced whelk behavior was evident between control and experimental trials (Table 3). In all trial HMM models, the covariates time of day, some tidal components (tide direction, tidal water height or both) and a spatial component (either grid or scallop density plot) were highly supported with the exception of the rst experimental trial (Table 3). Of note, the top 2-3 models containing these covariates within each trial had high cumulative AIC weight (>0.98 and ΔAIC >9) ( Table 3). Covariates that were strongly supported in the control trials (1 and 5) but not in the experimental trials were activity state, wind direction, and wind speed. In most predation experimental trials (except trial 2), strong support was present for whelks exhibiting diel movement behavior (most active around 14:00-20:00 h), while diel behavior was not supported in the controls. Spatial variability in scallop densities and time of day in scallop densities appeared to have the strongest support in trial 2 (Table 3) and were the only covariates included in the top two models (collective AIC weight = 0.85).

Predation of Bay Scallops by Channeled and Knobbed Whelks
Busycon are known to prey upon bivalves with tightly closing shells (e.g. clams, oysters) while thinnershelled Busycotyopus prefer to feed on bivalves with a larger shell gape, as well as carrion (Edwards and Harasewych 1988), but our observations con rm that channeled and knobbed whelks both prey upon live juvenile and adult bay scallops. The suggested preference of channeled whelks for larger scallops in lab experiments may be an artifact that re ects active swimming of juveniles at 25-30 mm (Tettelbach 1986), when peak levels of octopine dehydrogenase, the enzyme responsible for fueling bay scallop swimming, are seen (Garcia-Esquivel & Bricelj 1993) but this trend should be investigated further. Nevertheless, in spite of their swimming abilities, many juvenile scallops succumbed to predation <30 min after they were released into eld plots.
The mechanics by which Busycotyopus and Busycon prey on scallops is still not clear. Most often, we observed whelks engulf the entire scallop shell with their foot, but on one occasion a channeled whelk inserted its shell lip between the valves of its prey. The latter is a common method employed by Busycon carica to open Mercenaria shells, but has rarely been observed with Busycotypus canaliculatus (Magalhaes 191). Prescott (1990) observed that knobbed whelks ate adult bay scallops (Argopecten irradians concentricus) in the laboratory, but did not observe any type of shell damage. In our lab experiments, most shells of scallops eaten by knobbed whelks were characteristically notched; this was never observed for Busycotypus. Although not observed directly, this type of damage may result from the 'hammering' method -by which pieces of Mercenaria shell margins are broken off prior to insertion of the proboscis (Magalhaes 1948).
Reduced rates of predation at lower water temperatures in our experiments parallel observations by baymen, who typically stop shing for channeled whelks when they cease feeding in late November (P. Wenczel, pers. comm.). Relatively high rates of predation by whelks in the late August -early September 2013 trial were surprising, as this is the time of year when Busycotypus do not readily come to conch pots in the Peconic Bays (P. Wenczel, pers. comm), likely because they are mating/laying eggs instead of feeding (Edmundson 2016). Reduced catches of whelks in late August may also re ect higher water temperatures, as corroborated by the lack of predation in our 22-26 August 2012 trial.
Of 19,100 scallops planted in the eld, 60% (11,471) were accounted for by the end of our experiments; 5.6% (1,067 of the total planted) were cluckers -which represents the minimum rate of predation. The loss of the other 40% of planted scallops may have been due to dispersal or predation. Relatively high rates of dispersal were illustrated by the transport of large numbers of cluckers outside the planted sectors (especially to the South) and by the rates of immigration of wild scallops into the grid; however, extensive searching beyond the grid perimeter, even out to a distance of ~15-20 m to the South (where the number of planted scallops and cluckers was very low), suggests that we recovered the majority of cluckers. Thus, much or perhaps all of the missing 40% of planted scallops (7,629) may have been lost to predation -whereby shells were crushed to smaller bits (i.e. to the point where they were not cluckers and could not be recognized as recently predated) or shells were removed from the area. Scup, Stenotomus chrysops, are abundant throughout the Peconic Bays and were observed within the planting area; since they swallow scallops whole (Weinstock 2010, Mladinich 2017) they (or other shes) may be responsible for some of these scallop losses. If the missing 40% of planted scallops is added to the con rmed rate of predation (recovered cluckers = 5.6%), maximum cumulative predation amounts to 45.6% over the course of three eld experiments: roughly 3-5% predation d -1 . This aligns fairly well with empirical predation rates determined by Tettelbach (1986) for similar sizes of bay scallops planted in Connecticut over 1 week periods in the fall.
Since ~67% of recovered cluckers had shells that were cracked, chipped, pried or had hole punches, signatures most closely aligned with crustacean predation, we conclude that crabs were probably the most important cause of scallop mortality (Tettelbach 1986;Peterson et al. 1989;Prescott 1990). Cracked shells (36% of cluckers examined) are most likely the result of predation by large crabs -such as blue crabs, Callinectes sapidus, and large male spider crabs, Libinia emarginata; these are both common in the Peconic Bays and can consume scallops at high rates (Tettelbach 1986;Carroll et al. 2010).
Signatures of predation attributed to whelks in the eld and observed rates of predation in the lab were both relatively low -suggesting that the overall importance of whelk predation on planted scallops is of moderate importance. Whelk predation was inferred when cluckers recovered from eld experiments exhibited notches (n = 101) or no shell damage (n = 245): 9.5% and 23% of cluckers, respectively. The only other known predator of adult and large juvenile Peconic bay scallops that leaves no trace of shell damage is the common sea star, Asterias forbesi. However, this species has not been observed in the central and eastern Peconic Bays over the last 15+ years (Tettelbach et al. 2015). As whelks sometimes also left other traces of predation in lab experiments (9% chipped, 9% cracked), we inferred that another 2.6% of cluckers (n = 28) recovered from the eld resulted from whelk predation. Added together, the cluckers that can be attributed to whelk predation represent 4.3% of total presumed scallop losses (374/8709) or 2% of all planted scallops (374/19,100). This may somewhat underestimate overall whelk predation, as 32% of scallops eaten by both species in lab experiments had disarticulated valves and thus would not have been counted amongst cluckers in eld surveys. If the rate of predation on scallops planted in the eld is calculated on the basis of the numbers of acoustic tagged (n = 30) and observed wild whelks (total = 157), this works out to a predation rate of 0.13 scallops eaten whelk -1 day -1 (= 374 scallops eaten/157 whelks/18 days). This is comparable to observed predation rates by knobbed whelks in our laboratory experiments.
Busycon carica appears to represent a greater threat than Busycotypus canaliculatus to planted and natural bay scallop populations in the Peconic Bays because of its much higher abundance (~9-10x

Whelk Movement and Behavior in Response to Scallop Plantings
Intensive predation of scallops by channeled and knobbed whelks right after the rst planting suggests that emergence of buried whelks and foraging activity were both stimulated; mucus trails con rmed that whelks also immigrated into the area. The orientation of most whelks into the direction of the prevailing current, along with a sweeping, side to side motion, were the same behaviors exhibited by Busycon carica in ume experiments (Ferner and Weissburg 2005). This strategy is likely advantageous in that scallops may not detect the odor plume of an approaching whelk until they are almost in physical contact, reducing the window of opportunity for scallops to escape.
While the lack of sudden attraction of other large predators (crabs, n sh) to the seeded scallops is similar to what we observed in previous plantings (Tettelbach et al. 2011), others have observed a marked attraction of crabs (Boulding and Hay 1984, Barbeau et al. 1996) or sea stars (Tettelbach and Wenczel 1993) to high density scallop plantings. These differences may certainly re ect predator/prey densities or environmental factors (e.g. water temperature), but a better understanding of potential differences in predator response is important within the context of restoration efforts -where decisions regarding planting density may be central to their success (Tettelbach and Wenczel 1993, Tettelbach et al. 2013. The greater overall amount of time spent by tagged whelks in the grid after it was planted with scallops versus controls (no scallops) was expected, as were the shorter distances traveled and lower movement rates by whelks in these trials (The Nature Conservancy, 2018). These patterns likely re ected more directed searching for prey/lower encounter rates in the absence of scallops (The Nature Conservancy, 2018), but surprisingly there was a lack of concomitant differences in exploratory behavior probability exhibited by whelks in predation trials. These metrics may re ect the ndings of Ferner and Weissburg (2005), who determined that Busycon carica were able to successfully locate prey odor plumes at distances of >1.5 m in ume experiments; searching behaviors (e.g. side to side scanning) were reduced at higher ow velocities and in the presence of obstructions, so that whelks reached the prey odor source more quickly.
While tagged whelks spent more time encamped inside the grid when planted scallops were present, compared to control trials with no scallops, whelk typically exhibited a higher probability of an encamped behavioral state in sectors planted at lower (6.7 -17.5 m -2 ) rather than higher (51.5 -72.0 m -2 ) scallop densities -which is contrary to most animal movement studies. Encamped movement patterns are commonly characterized in landscapes where prey/resource abundance is high; thus, animal step lengths are short, with sharp turning angles, as animals perform fewer large-scale movements (Zollner and Lima 1999; Morales et al. 2004). Even at lower planting densities, which were ~4x those of the ambient wild scallop population, predator satiation and thus reduced foraging activity might have been expected on the basis of low daily rates of prey consumption in lab experiments (this study). The post-foraging lag time for appetite to return was determined to be 25-39 h for another temperate whelk species (Buccinum undatum) (Evans et al. 1996). While we did not examine scallop predation by whelks from a functional response standpoint, the unexpectedly higher amount of time spent by tagged individuals in grid sectors planted at lower scallop densities may re ect behavioral processes related to the modi ed Type III functional response described for sea stars, Asterias vulgaris, feeding on mobile sea scallops, Placopecten magellanicus (Wong et al 2006). These authors found that handling time and proportion of time spent searching for prey did not vary with prey density but suggested that the decreased foraging e ciency of sea stars observed at high prey densities may have resulted from con icting stimuli from multiple nearby sea scallops (Wong et al. 2006). Interference competition from other predators (Gotelli 2008) within our high density sectors is another possible explanation for greater observed encampment at high versus low bay scallop densities. The potential presence of higher numbers of blue crabs (known predators of whelk and scallops) and spider crabs at higher scallop densities may have resulted in whelk burial/avoidance (Harding 2003;Cordero and Seitz 2014), contributing to more encamped behaviors for longer periods.
Mean overall movement rates of channeled whelk in eld predation trials (average = 45.8 m d -1 ) and in control trials (223.5 m d -1 ) were much higher than those reported by Edmundson (2016) in Lake Tashmoo, a small embayment in Massachusetts, where she observed movement rates of 12 m d -1 from late October -early November for channeled whelks also tracked with Vemco acoustic tags. In other, longer term studies which employed traditional (non-acoustic) tags, daily movement rates were also lower than those for our short-term studies: 12 m d -1 for channeled whelks in Narragansett Bay, Rhode Island (Sisson 1972), and 18 and 0.7 -7 m d -1 , respectively, for knobbed whelks at Beaufort, North Carolina (Magalhaes 1948) and Wassaw Sound, Georgia (Shalack et al. 2007). The latter studies may have underestimated whelk movement rates because they were based on linear distances (start to end positions); however, because they encompassed periods of winter inactivity, annual rates of movement would expectedly be lower than those observed during warmer times of the year. In the study by Edmundson (2016), channeled whelks only moved an average of ~1 m d -1 over a 1 yr period. Nevertheless, total distances traveled by channeled whelks in other longer term (~10 mo) studies in larger bodies of water were considerable: up to 1.6 and 4.2 km, respectively, in Great South Bay, New York (Lynn 2018) and Narragansett, RI (Sisson 1972). These observations and suggestions of seasonality of channeled whelk movement, particularly in the spring and fall, that have come from many years of eld observations by baymen (F. Sloup, P. Wenczel, pers. comm) deserve further study.
The above observations, and those from the present study, provide important insights into the timing and range of movement of mobile gastropods -which in turn may have management implications. For instance, Glazer et al. (2003) determined that the aggregated home range of queen conch (Strombus gigas) was twice as large as a designated no-take reef in the Florida Keys, resulting in incomplete protection. An acoustic telemetry study of giant triton snails (Charonia tritonis) revealed their average daily movement rate (234.2 m d -1 ) was 23x the maximum daily movement rate of their prey, the crown-ofthorns star sh (Acanthaster planci)suggesting tritons could successfully control population outbreaks of the latter species in sections of the Great Barrier Reef (Schlaff et al. 2020). Additional data on the movement rates of channeled and knobbed whelks for longer durations than our trials and across seasons would provide a more comprehensive picture of spatio-temporal variability in whelk-scallop interactions, movement and behavior (Sperry et al. 2008) and thus might help inform the timing of scallop plantings to improve survival and hence success of restoration programs.
Mean rates of movement by whelks in our control trials (223.5 m d -1 ) were considerably higher than in predation trials. This may have re ected greater searching in the absence of scallop prey, as discussed above. However, in the rst control trial, greater dispersion and directed movement of tagged whelks to deeper offshore waters (to the northeast), perhaps to avoid increased wave energy and exposure, may well have been precipitated by a gale that blew in right at the time of planting. Thus, wind direction and wind speed were well-supported predictors of whelk movement in the best models for control trials, but they were not in experimental trials.
Effects of atmospheric phenomena on animal behavior have been described for a variety of taxa but are much more well-known for vertebrates than invertebrates (Massie et al. 2019;Strickland et al. 2020). For example, rock black sh (Girella elevata) in shallow subtidal habitats responded sharply to increased wind speed by moving to deeper depths -likely to avoid greater wave height (Stocks et al. 2015). Blacktip sharks were capable of anticipating incoming hurricanes along the Florida Gulf Coast with as little as a 5mb drop in barometric pressure, without large changes in wind speed, and temporarily migrated to deeper waters to avoid storm exposure (Heupel et al. 2003). Other sh, such as summer ounder, responded to declines in average atmospheric pressure of 4 mbar/week by increasing emigration from estuaries to deeper waters on the continental shelf off New Jersey (Sackett et al. 2007). Amongst insects, rapid changes in barometric pressure (30 mbar h -1 ) resulted in reduced ight initiation frequency in polyphagous wasps (Trichogramma spp.) (Fournier et al. 2005). Pellegrino et al. (2013) found that curcurbit beetles (Diabrotica speciosa) showed reduced locomotive activity when exposed to decreasing barometric pressure at rates as low as 0.4 mbar h -1 .
Atmospheric pressure was not a strong predictor of whelk behavioral switching in any trial, which was surprising considering that whelks in the control trials (1, 5) experienced average ranges of 20.5 mb: 2x higher than those during predation trials (2,3,4). However, it is important to note that average distance traveled was nearly 4x higher in control trials when atmospheric pressure was declining, indicating that whelk locomotive activity may be partially responsive to changes in barometric pressure. Although we do not know the speci cs of how whelks sense atmospheric pressure, it is known that both marine invertebrates and vertebrates without swim bladders detect small changes (5-10 mbar) in hydrostatic pressure via vestibular hair cells (Fraser and MacDonald 1994;Fraser et al. 2003). Our novel results strongly suggest that gastropods respond to weather events; this certainly deserves further study.
The importance of time of day in explaining channeled whelk movement patterns, as supported in HMMs for both control and treatment trials, with highest observed activity in early evening/twilight hours, corroborates the ndings Magalhaes (1948). While we cannot pinpoint the mechanism(s) behind the crepuscular activity pattern within the con nes of our dataset, predator avoidance (Lima and Dill 1990) is a plausible explanation. Blue crabs (see above) are most likely to exhibit agonistic and defensive behaviors during this time (Clark et al. 1999). Diurnal patterns in dissolved oxygen (DO) levels may also potentially in uence whelk activity patterns. Greater locomotion of another large gastropod, queen conch (Lobatus gigas), is suggested to coincide with higher DO concentrations in late afternoon/evening (Dujon et al. 2019).
Pots used to commercially sh for whelks in New York are typically spaced at distances of >50 m (F. Sloup, P. Wenczel, pers. comm); however, distances from which whelks travel to baited pots are not precisely known. Our work suggests that both channeled and knobbed whelks may be drawn to high density scallop plantings. Given this, and the fact that both whelk species can consume juvenile as well as adult scallops, these behaviors should be factored into decisions concerning site selection and other potential strategies (e.g. predator removal) employed in bay scallop restoration.
Examining the behavioral responses of predators to external surroundings and prey density is crucial for identifying both management and ecological implications (Schmitz and Barton 2014). We have provided novel insight into predator-prey interactions among three commercially important marine invertebrate species in both the eld and lab. Despite the relatively low scallop predation rate observed for both channeled and knobbed whelks in the lab, eld experiments revealed that whelks were probably responsible for 4.5% of scallop mortality and that 45% of all planted scallops were lost after 14 days in the eld -plausibly the result of predation. Therefore, additional eld studies are needed to robustly quantify the impact of channeled and, especially, knobbed whelks on wild bay scallop populations and assess their impact on planted stocks in the context of ongoing scallop restoration efforts.

Declarations
Funding: This project was funded through the Suffolk County 277 fund through the Peconic Estuary Partnership.
Con icts of interest/Competing interests: The authors have no con icts of interests.
Availability of data and material: Data is held by the authors and is available upon request from the corresponding author and will also be available on the Peconic Estuary Partnership's website (www.peconicestuary.org).
Code availability: The R-code generated during the current study is available from the corresponding author on reasonable request.
Authors' contributions: MS and ST designed the experiments, carried out the research, analyzed the data, and wrote and revised the original manuscript. JB analyzed the telemetry data and prepared and revised the original manuscript. JE prepared the telemetry data and revised the manuscript. JH, CH, SWT contributed to experimental design, carried out the research, and revised the manuscript. All authors read and approved the nal manuscript.
Ethics approval: This research was carried out in accordance with all applicable institutional guidelines at the time that the study was conducted. Ethical review and approval was not required for the animal study       Signi cance values (*) represent p<0.05 from Conover post hoc pairwise comparison tests adjusted for multiple comparisons with the Holm method (Tables S1 and S2). "ns" denotes non-signi cant differences. The natural scallop treatment density denotes ambient densities outside the experimental grid boundaries. Scallop density (#/m2) dependent stationary state transition probabilities. The "N" scallop density denotes the average ambient scallop densities in the Peconic Bay outside of the experimental grids. Figures A,B,C represent experimental trials 2,3, and 4. Error bars denote 95% con dence intervals.