Sculpin Predation on Lake Trout Eggs in Interstices: Skull Compression As a Novel Foraging Mechanism

Copeia 2014, No. 4, 000–000

Sculpin Predation on Lake Trout Eggs in Interstices: Skull Compression as a Novel Foraging Mechanism

J. Ellen Marsden1 and Harrison Tobi2

Lake Trout (Salvelinus namaycush) spawn in fall and hatch in spring; to protect their eggs over the winter they spawn on rocky reefs, where the eggs settle deeply into interstices. Uptake of water swells the eggs, further protecting them by lodging in crevices. Freshwater sculpin (Cottidae), the primary predator of salmonid eggs, are small, benthic fishes with malleable bodies and large heads. To acquire the lipid-rich resource contained in eggs, sculpin must penetrate deeply into interstices, and have a method to extract lodged eggs. We placed Slimy Sculpin (Cottus cognatus) into a tunnel containing a sequence of funnels with progressively smaller openings to determine the smallest hole they could enter. Forty-three of 138 Slimy Sculpin (31%) moved through openings up to 19.7% smaller than the maximum width of their head, indicating that they compressed their skull to move through the opening. We examined egg acquisition behavior by placing Lake Trout eggs into holes drilled in a Plexiglass plate. Holes varied in diameter from 5.6 to 8.7 mm, and were either shallow (5 mm) or deep (9 mm); after water hardening, eggs were lodged in the smallest holes and loose in the larger holes. Sculpin consumed eggs in the large, shallow holes first, then used suction to extract eggs from small, shallow holes. To extract eggs from small, deep holes, they used a sequence of suction attempts to draw the eggs upward. Sculpin are highly adapted to forage on Lake Trout eggs, including the novel capacity to compress their skulls to access eggs.

UCCESSFUL acquisition of prey by predators involves builders or cavity spawners), burying them (redd-builders), a sequence of steps, including prey detection, recog- or hiding them. Lake Trout hide their eggs using two S nition, approach, capture, handling, and ingestion. strategies: (1) spawn in late fall, so that although the egg For acquiring prey that are hidden in crevices, the processes develops very slowly, predator metabolic rates have also of detection and capture are particularly challenging; slowed down and their nutritional and energy needs are low predators may require a non-visual means for detecting (e.g., Fitzsimons et al., 2006); (2) deposit eggs on rocky reefs the prey, and a specialized method for extracting prey. Some with open interstices, so that the eggs, which are negatively fishes are particularly well equipped for crevice feeding buoyant, will essentially bury themselves. In a separate because of their capacity to use suction. Fishes have a range study, we found that Lake Trout eggs can penetrate of feeding modalities, including ram, suction, and biting, interstices in cobble substrates (mean diameter 12 cm) to but the majority of teleosts use suction feeding (Norton, at least 1 m. Water hardening adds protection by lodging 1991; Gerking, 1994; Westneat, 2005). Suction feeding some eggs into crevices. For predators to obtain eggs involves a complex set of movements of bones in the skull, ‘concealed’ and entrained into interstitial spaces, they must maxillary apparatus, mandible, operculum, and hyoid overcome the challenge of moving into proximity to the apparatus that expand the buccal cavity and draw a current eggs through a matrix of rocks. of water, with the prey, into the predator’s mouth. This Few studies have examined strategies for acquiring method is highly adaptable, and is used by pelagic predators immobile prey that are deeply hidden in interstitial spaces. that chase mobile prey (fish or plankton), by detritivores to Many fish will pick at prey in crevices, dislodging small pull sediments into the mouth, and by benthic foragers to rocks or shells to access prey underneath them (Shibuno extract attached or hidden prey (Gerking, 1984; Ferry- et al., 1994; Jensen, 2005), or burrow into soft sediments or Graham et al., 2002). Suction feeding is the primary feeding sand to obtain prey detected by vibrations or electromag- mode used by benthic predators such as sculpins (Cottidae) netic cues (Kalmijn, 1971; Janssen, 1990), but few non- for capturing sessile species (Norton, 1991, 1995). Suction or anguilliform fishes penetrate small, rocky interstices with biting are the only strategies possible to acquire prey within their entire body. Acquisition of fish eggs in interstitial interstitial spaces, where movement of the predator is highly spaces presents a particular challenge for predators: the eggs limited. are motionless, and therefore not detectable by visual cues Predation on eggs is a relatively simple problem for a fish or the lateral line (at least until the embryo begins to move predator. Eggs are immobile, usually present in high within the egg). There is no reaction distance for the prey, abundance within a short period after spawning, of fixed and no probability of escape by moving, but for large eggs or configuration (spherical), of approximately fixed size (for small predators, gape may be a limiting factor in acquisition. one species of fish), easy to process, and offer a high reward The interaction between Lake Trout (Salvelinus namaycush) in terms of lipid energy. The challenges for the predator are and their major egg predator, sculpins (Cottus spp.) is to be in the right place at the right time (i.e., at a spawning interesting in the context of predator–prey dynamics. Lake site during or after spawning takes place), and have a gape Trout spawn in fall and eggs incubate over winter, so the sufficiently large to ingesttheegg.Thereproductive eggs are vulnerable to predation, and defenseless, for almost behavior of fishes must therefore include some strategy for six months. Their large eggs provide a lipid-rich, highly minimizing predator access to their eggs—by scattering digestible, passive prey throughout the forage-limited winter them (pelagic and broadcast spawners), guarding them (nest months. To protect their eggs, Lake Trout spawn on cobble

1 Rubenstein Ecosystem Science Laboratory, Rubenstein School of Environment and Natural Resources, University of Vermont, Burlington, Vermont 05401; E-mail: [email protected]. Send reprint requests to this address. 2 Rubenstein School of Environment and Natural Resources, University of Vermont, Burlington, Vermont 05401; E-mail: [email protected]. Submitted: 1 February 2014. Accepted: 17 July 2014. Associate Editor: J. F. Schaefer. F 2014 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-14-016 Published online:

Copeia cope-14-04-06.3d 9/10/14 20:07:45 1 Cust # CE-14-016R1 2 Copeia 2014, No. 4 reefs with deep interstitial spaces; the eggs are negatively which an individual can squeeze, and to describe egg buoyant, and settle rapidly into interstitial spaces. There, acquisition behavior by sculpins. they are protected from water turbulence and from predation by all but the smallest species (Fitzsimons et al., 2007). METHODS AND MATERIALS Sculpins can penetrate interstitial spaces due to their small body size and flexibility (Martin and Olver, 1980; Claramunt Slimy Sculpin were collected from Browns River, VT, using a et al., 2005; Fitzsimons et al., 2006). Sculpins theoretically backpack electroshocker. Sculpin were housed in a 150 L have a window of body sizes that is optimal for foraging on aquarium with constant aeration and filtration; water Lake Trout eggs; an individual must have a gape large temperature was maintained at 8.2uC with a chiller. Eggs enough to engulf an egg, but a head small enough to access were obtained from Lake Trout collected in Lake Champlain eggs in interstices. For example, Biga et al. (1998) found during late fall in trap nets; eggs were expressed from ripe fewer sculpins, and fewer eggs in sculpin stomachs, in females, kept dry to prevent water hardening, and stored smaller substrates. Freshwater sculpins have large, flattened prior to use at 5uC. All trials were conducted within seven heads and tapering bodies, so their largest dimension is head days of egg collection. Fish were collected under a Vermont width. Department of Fish and Wildlife collection permit; labora- When eggs are extruded from a female Lake Trout they are tory work was conducted under UVM IACUC protocol 12-014. soft and fairly malleable; they immediately begin to adsorb To determine the smallest space into which a Slimy water until the chorion limits further uptake, at which point Sculpin can maneuver, a cylindrical ‘tunnel trap’ was the egg is turgid and is termed ‘water hardened.’ Eggs are constructed with a series of eight compartments, each fully water hardened in 20–120 min, depending on ambient 15 cm long, separated by funnels of decreasing diameter water hardness; if this process occurs after the egg has fallen (25.4 mm, 22.2 mm, 19.1 mm, 15.9 mm, 12.7 mm, 9.5 mm, into a crevice between hard surfaces, the eggs become firmly 6.4 mm, and 3.2 mm. A 150 L aquarium was partitioned, lodged. To acquire these eggs, sculpin must be able to detect with the tunnel mounted in the partition, allowing entrance an egg, work its body through the maze of connected to the tunnel on the end with the largest funnel. The tunnel interstitial spaces to approach the egg, and then extract it was then covered with rocks to provide a semi-darkened from the crevice in which it is lodged. Vision and the lateral environment and visually isolate the sculpins from outside line are of no use in detecting a motionless, non-breathing disturbance. Slimy Sculpin were placed on the side of the prey, but smell may be useful; sculpin appear to use aquarium with access to the tunnel opening. After initial chemical cues to locate salmon eggs in shoreline habitats one-day trials with and without bait, we found that sculpin (Dittman et al., 1998; Foote and Brown, 1998). A highly explored the funnel ‘maze’ without the stimulus of bait; flexible and malleable body morphology facilitates access to similar to their behavior in the holding tank, they tended to eggs through penetration of interstices. Acquiring the egg is cluster in groups of five or more individuals, usually in close the final challenge; eggs are spherical and smooth, making physical proximity to each other and/or in crevices. For the them difficult to grasp and pull—they must be engulfed by trials, Slimy Sculpin were left for three days in the aquarium. getting the mandible and maxillary past the widest part of A maximum of 34 Slimy Sculpin were given access to the the circumference. If the egg is lodged, suction may be the tunnel at one time; we tested a total of 138 Slimy Sculpin in only method available to a fish in order to extract the egg. the tunnel trap, with an average total length of 66.3 mm 6 Chotkowski and Marsden (1999) determined in laboratory 11.9 SD (range 36.8–90 mm TL) and average head width of experiments that 42 mm standard length (53 mm total 11.6 mm 6 2.3 SD (range 6.3–17.1 mm). After the three-day length) was the minimum size of Mottled Sculpin (Cottus period, Slimy Sculpin were removed from each section of the bairdi) that has a gape sufficiently large to engulf an egg; tunnel and the compartment in which each individual was however, Fitzsimons et al. (2002) found eggs in sculpin as found was recorded. All Slimy Sculpin were alive and small as 43 mm total length in the field, but did not specify showed no visible signs of stress (e.g., lethargy, low response whether the species was Mottled Sculpin or Slimy Sculpin to handling, skin infections) when retrieved from the (C. cognatus). Slightly smaller sculpin will vigorously ‘attack’ funnel. Slimy Sculpin were lightly anaesthetized with clove and engulf an egg, but because they lack the force to crush oil in order to measure total length and maximum the egg, the egg is eventually spit out, and the process of horizontal and vertical width of the head. Head width was acquisition is repeated several times (Marsden, pers. obs.). measured by gently closing a caliper over the widest part of The goal of this study was to understand the interaction the head until it was in contact with the closed operculae between the Lake Trout reproductive strategy of ‘hiding’ (Fig. 1); we did not attempt to squeeze the head. To evaluate their eggs, and the prey capture abilities of their major accuracy of our morphometric measurements, we measured predator, sculpins. The study was stimulated in part by total length and maximum head width of 12 anaesthetized observation of Mottled Sculpins captured in Lake Trout Slimy Sculpin five times, with each Slimy Sculpin measured emergent fry traps (unpubl. obs.). The capture bottle on once in sequence to minimize potential for repetitive emergent fry traps contains a funnel with an opening measure bias. Regression was used to determine how closely 12.5 mm in diameter; the funnels are sometimes equipped head width was related to total length. with a wire or plastic chord across the center of the opening Sculpin foraging behavior to acquire eggs was observed to exclude predators (Marsden et al., 1988). We have found using eggs in artificial ‘crevices.’ Sixteen holes were drilled sculpin up to 74 mm total length (TL) in these traps, with in a grid pattern into a 15 3 15 cm square plate of 1.3 cm head diameters up to 13.5 mm, clearly larger than the trap thick Plexiglas. The holes were 5.6 mm, 6.4 mm, 8 mm, and opening. Apparently, the sculpins must be distorting their 8.7 mm in diameter, and either 5 mm or 9 mm deep; each heads in order to squeeze into the narrow opening. We used diameter:depth combination was used twice. A single ‘dry’ laboratory behavioral trials to determine the relationship egg was added to each hole, and allowed to water harden. between sculpin head size and the smallest opening into Although Lake Trout eggs are nominally 4.6 to 5.7 mm in

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Fig. 1. Slimy Sculpin, showing head width measurement.

diameter (Piper et al., 1982), we discovered that eggs would arrays consumed an average of 8.9 of the 12 eggs available in not fit in the smallest holes. After hardening, eggs were fully the first hour (range 5 4–12). Sculpin explored each plate lodged into the 6.4 mm holes, but were loose within the prior to and during foraging; they did not tend to consume larger holes. A single plate containing eggs was placed in the the egg nearest to the last egg consumed (i.e., there was no bottom of a 19 L aquarium, and four Slimy Sculpin were bias toward adjacent eggs). Eggs from the shallow holes of all added. Each Slimy Sculpin had previously been starved for diameters were consumed first; there was sufficient space 48 hr. Missing eggs were recorded at intervals of 5 min; between the egg and the sides of the large holes so that initial observations indicated that Slimy Sculpin fed vigor- Slimy Sculpin were able to grasp the eggs, whereas they ously for 1 hr, then took eggs infrequently thereafter, so appeared to use suction to remove eggs from the smallest observations were discontinued after 1 hr. Each sculpin was (6.4 mm) holes. Once all eggs from the shallow holes were measured (total length and maximum head width) as before, consumed, Slimy Sculpin began to remove eggs from the after each trial; a total of eight trials was completed using a deep 6.4 mm holes, then from the larger holes at random total of eight Slimy Sculpin, with each Slimy Sculpin used (Fig. 3). To acquire the deep eggs, Slimy Sculpins used a four times. During each trial, Slimy Sculpin foraging series of two to four suction attempts; in the smallest behavior was observed to determine how eggs were diameter holes, the egg was pulled upward by each suction, acquired. then lodged at the new depth, so that the egg eventually reached the surface of the plate and was consumed. Eggs from the larger diameter holes needed to be raised by RESULTS suction, followed by a ‘grab’ as the egg came within reach Forty-three (31%) Slimy Sculpin moved through funnels and before it fell back into the hole; multiple attempts were smaller than the maximum width of their head, indicating usually needed before the egg was seized. that they compressed their skull to move through the opening (Fig. 2). The maximum difference between the hole DISCUSSION diameter and head diameter was 19.7%. Maximum error (i.e., difference between smallest and largest measurements) The present study shows that Slimy Sculpin have the of repetitive measures of Slimy Sculpin was 1.0 mm (average remarkable ability to facilitate their movement into inter- 0.5 mm) for total length and 1.9 mm (average 0.7 mm, or stices by compressing their heads up to 19.7%, allowing for 5.7% of head width) for maximum head width. Total length entrance into openings smaller than the maximum width of was closely correlated with head width (R2 5 0.89). their head. Benthic cottid species mostly have highly In foraging trials, the eight Slimy Sculpin averaged flexible bodies which allow maneuverability in tight spaces, 79.8 mm TL (range 71–90 mm). Sculpin foraging on plate

Fig. 3. Acquisition of Lake Trout eggs by Slimy Sculpin from artificial crevices (holes of varying diameter, in mm) over time. Light bars Fig. 2. Number of sculpin that entered funnels with openings smaller indicate shallow (4 mm) holes; dark bars indicate deep (10 mm) holes. than their maximum head width, shown as percent difference between Data are totals of eight foraging trials with eight sculpin ranging from 71 funnel opening diameter and head width. to 90 mm TL (average 79.8 mm).

Copeia cope-14-04-06.3d 9/10/14 20:07:46 3 Cust # CE-14-016R1 4 Copeia 2014, No. 4 but their large heads would, without compression, limit repeated suction attempts allow Slimy Sculpin to draw eggs access to prey located in deep interstices. We have observed out. Slimy Sculpin penetrate cobbles stacked to 1 m deep, ‘following’ Lake Trout eggs. Fish skull functional morphol- ACKNOWLEDGMENTS ogy and feeding kinetics have been thoroughly studied (e.g., reviews by Ferry-Graham et al., 2002; Westneat, 2005). We thank B. Ladago for assisting with collection of Slimy However, to our knowledge the ability to contort the skull Sculpin and Lake Trout eggs, and with laboratory trials. morphology to allow skull compression has not previously been observed. Skull compression is clearly facilitated by the LITERATURE CITED same complexity of fish skull morphology and mobility of Biga, H., J. Janssen, and J. E. Marsden. 1998. Effect of bones that also allows suction feeding, in which multiple substrate size on lake trout egg predation by mottled bones are moved to expand portions of the head (Westneat, sculpin. Journal of Great Lakes Research 24:464–473. 2005). The ability of sculpin to obtain eggs in crevices is Chotkowski, M. A., and J. E. Marsden. 1999. Round goby highly advantageous, as it gives them access to interstitial and mottled sculpin predation on lake trout eggs: field invertebrate prey and to a spatially concentrated, energy- predictions from laboratory experiments. Journal of Great rich egg supply throughout the winter months when other Lakes Research 25:26–35. food resources are scarce. Claramunt, R. M., J. L. Jonas, J. D. Fitzsimons, and J. E. Slimy Sculpin in our trials appeared to minimize the effort Marsden. 2005. Influences of spawning habitat charac- to acquire eggs. All food items were of roughly equal teristics and interstitial predators on lake trout egg energetic value. The easiest eggs to acquire, those that were deposition and mortality. Transactions of the American loosely contained in large, shallow holes, were taken first, Fisheries Society 134:1048–1057. followed by eggs lodged in small, shallow holes (Fig. 3). Eggs Dittman, A. H., G. S. Brown, and C. J. Foote. 1998. The role in deep holes were more challenging for sculpins to acquire of chemoreception in salmon-egg predation by coastrange in our experimental trials. The holes were all too small to (Cottus aleuticus) and slimy (C. cognatus) sculpins in Iliamna allow the sculpin to insert their heads to grasp the eggs. Lake, Alaska. Canadian Journal of Zoology 76:405–413. Acquisition of lodged eggs was facilitated by suction feeding; Ferry-Graham, L. A., P. C. Wainwright, M. W. Westneat, Slimy Sculpin were able to draw eggs out of deep ‘crevices’ and D. R. Bellwood. 2002. Mechanisms of benthic prey using repeated suction attempts. Eggs in large, deep holes capture in wrasses (Labridae). Marine Biology 141:819–830. could drop back into the hole, so the eggs in small, deep Fitzsimons, J. D., J. L. Jonas, R. M. Claramunt, B. holes that could be drawn upward in stages appeared to be Williston, J. E. Marsden, B. J. Ellrott, and D. C. easier to acquire, and were mostly taken before eggs in large, Honeyfield. 2007. Influence of egg predation and phys- deep holes. Minimizing handling time is a component of ical disturbance on lake trout Salvelinus namaycush egg optimal foraging, in which predators optimize the trade-off mortality and implications for life-history theory. Journal between energy spent acquiring prey and energy obtained of Fish Biology 71:1–16. from prey (Werner, 1974; Werner and Hall, 1974). Because Fitzsimons, J. D., D. L. Perkins, and C. C. Krueger. 2002. suction feeding entails expansion of the buccal cavity, Sculpins and crayfish in lake trout spawning areas in Lake presumably Slimy Sculpin can only access eggs in interstices Ontario: estimates of abundance and egg predation on lake in which the Slimy Sculpin has space for head expansion, trout eggs. Journal of Great Lakes Research 28:421–436. unlike in our foraging arenas. Fitzsimons, J. D., B. Williston, G. Williston, G. Bravener, The question of how Slimy Sculpin detect eggs that are J. L. Jonas, R. M. Claramunt, J. E. Marsden, and B. J. hidden in crevices remains unanswered. Egg deposition by Ellrott. 2006. Laboratory estimates of salmonine egg Lake Trout occurs over a fairly short time period (weeks; predation by round gobies (Neogobius melanostomus), Martin and Olver, 1980), and is focused in relatively small sculpins (Cottus cognatus and C. bairdi), and crayfish areas (spawning reefs may be as small as a few hundred (Orconectes propinquus). 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