Predatory Behavior of the Sea Stars Asterias Amurensis and Distolasterias Nipon on the Japanese Scallop, Mizuhopecten Yessoensis

Plankton Benthos Res 14(1): 1–7, 2019 Plankton & Benthos Research © The Japanese Association of Benthology

Predatory behavior of the sea stars Asterias amurensis and Distolasterias nipon on the Japanese scallop, Mizuhopecten yessoensis

1 2 1, Hiroyuki Nishimura , Koji Miyoshi & Susumu Chiba *

1 Department of Ocean and Fisheries Sciences, Tokyo University of Agriculture, 196 Yasaka, Abashiri, Hokkaido 099–2493, Japan 2 Abashiri Fisheries Research Institute, Fisheries Research Department, Hokkaido Research Organization, 1–1 Masuura, Abashiri, Hokkaido 099–3119, Japan Received 9 April 2018; Accepted 20 October 2018 Responsible Editor: Masakazu Aoki doi: 10.3800/pbr.14.1

Abstract: Because sea stars are the primary predators of the Japanese scallop, Mizuhopecten yessoensis, they are being removed from scallop fishing grounds, despite the lack of information on their predatory impacts. We experimentally examined the predatory behavior of the sea stars Asterias amurensis and Distolasterias nipon on the Japanese scallop. In the first experiment, we hypothesized that sea stars respond to distant chemical cues from live scallops. However, the results showed that neither A. amurensis nor D. nipon responded to the chemical cues of live intact animals, though it is commonly known that they respond to the chemical cues of carrion. We also examined the effects of the relative sizes of the sea stars to the scallop on their predator-prey relationship. We altered the body size ratios of the Japanese scallop to A. amurensis in the summer and winter, and to D. nipon in the summer, and observed the scallops’ survival. In all experiments, logistic regression models were applied to changes in survival under different prey-to-predator size ratios, which were calculated by dividing the scallop size by the sea star size. Our results suggested that survival of the Japanese scallop rapidly increases with increasing body size. The ratios at which mortality was 50% provide an important parameter in estimating the predation risk from sea stars in scallop fishing grounds. Our study will contribute to the effective and responsible management of Japanese scallop mariculture.

Key words: Asteriidae, body size, Pectinidae, predator-prey interaction, sowing culture

has been improved over time by technological advance- Introduction ments (Nishihama 1994, Kosaka 2016), much remains un- The largest scallop fisheries in the world (FAO 2018) known about the latter step beyond basic population pa- are those that produce the Japanese scallop, Mizuhopec- rameters such as growth, survival, and age structure in the ten yessoensis (Jay 1857). Their profit yields via export wild (Goshima & Fujiwara 1994, Kurata 1996, Paturusi et have also been the largest among all Japanese fisheries al. 2000, Shinada 2006). since 2012 (Ministry of Agriculture, Forestry, and Fisher- Understanding the process of mortality in the released ies, Japan 2017). As over 50% of Japanese scallops are scallops is the most important challenge in this maricul- produced by mariculture along the Sea of Okhotsk coast ture. Predation is the primary cause of their mortality, of Hokkaido (Chiba 2016), its sustainability and effects on and many local fishermen and researchers, based on their the ecosystem should be considered as an important com- experiences, think that sea stars are the main predators ponent of the Code of Conduct for Responsible Fisheries influencing scallop populations. Large numbers of sea (FAO 1995). Scallop mariculture is divided into two steps: stars have consequently been removed from many scallop the aquaculture of juveniles in suspended cages and the fishing grounds (Kosaka 2016) simply due to speculation release of the juveniles to the wild. While the former step regarding a negative correlation between the densities of the sea stars and scallops. However, no reports have yet quantified the effect of sea star predation in the wild. The * Corresponding author: Susumu Chiba; E-mail, [email protected] removal of sea stars is thus based on uncertain information 2 H. Nishimura et al. about their predation. In scallop mariculture, simple predator-prey relationships at the species level should be care- fully examined to efficiently manage a responsible fishery. To discern the predation effect of sea stars on the survival of the Japanese scallop, it is necessary to know basic information about their predator-prey relationship. Al- though sea stars are certainly predators of the Japanese scallop, their predatory impacts may not always be seri- ous in the wild. It is well known that sea stars respond to the chemical cues of food (Castilla & Crisp 1970, Zafiriou 1972, Sloan & Northway 1982, Valentinčič 1985, Drolet & Himmelman 2004), however, there have been no reports on how sea stars detect live scallops in the wild. In addition, body size is not a negligible factor when quantifying the Fig. 1. Schematic drawing of the Y-maze trough. Two channels predation impact of sea stars on the Japanese scallop. As were separated by a plastic board. Before starting the experiment, the Japanese scallop grows larger than other sea star prey one live scallop or one pair of scallop shells was tethered at the such as clams and mussels, the value of scallops as prey for upstream section of each channel, and one sea star was placed at sea stars may depend on their relative sizes. Indeed, size- the downstream section of the trough. Thick black arrows indicate dependent predation by sea stars is also known in other the direction of water flow. scallop species that grow to large sizes (Barbeau & Scheib- ling 1994, Barbeau et al. 1994, Arsenault & Himmelman detection ability of A. amurensis in the winter (from No- 1996, Magnesen & Redmond 2012). The assumption that vember 21, 2015 to January 14, 2016), whose mean water all sea stars can consume all scallops would oversimplify temperature was 2.5°C (between 0.0 and 6.0°C). We could their actual relationship. not collect D. nipon during the winter, thus excluding it This study experimentally examines the feeding behav- from the winter studies. In this experiment, we hypoth- ior of sea stars and how predation risk by sea stars on the esized that sea stars respond to distant feeding chemical Japanese scallop changes with their relative body size. As cues that are upstream because we empirically knew that Asterias amurensis Lutken, 1871 and Distolasterias nipon sea stars aggregate to the carrion of various animals in a (Döderlein, 1902) have been recognized as major scallop cage trap. This hypothesis was tested in a Y-maze trough predators in the Sea of Okhotsk (Volkov et al. 1982, Silina that was constructed from plastic boards, and seawater 2008), our investigations focused on these two sea star spe- (2 L min−1) was supplied from the corners of two chan- cies. nels (Fig. 1). One live scallop (between 94 and 126 mm in SH) and one pair of only scallop shells were tethered at the upstream sections of each channel (Fig. 1). The shells were Materials and Methods washed and dried for the new trial to remove the chemi- Between two and four weeks before starting each ex- cal cues of the internal organs. One sea star (between 113 periment in this study, we collected Japanese scallops and and 226 mm in AL) was acclimatized for 24 h in a mesh A. amurensis and D. nipon individuals from the coast of cage and placed at the downstream section of the trough the Sea of Okhotsk near Abashiri, Hokkaido, Japan by (Fig. 1). Observations started after the cage was removed. employing a bottom trawl and a cage trap, respectively. We recorded the behavior of the sea stars for 24 h using a We measured the shell height (SH) of the scallops and the digital video camera (Everio GZ-VX895, JVC Kenwood length between the mouth and the tip of one arm near the Corp. Kanagawa, Japan) set above the trough. After each sieve plate (arm length, AL) of the sea stars. The scallops trial, the scallop and shells were replaced with new ones, and sea stars were separately reared in aquariums (700 L) the channels of placement were switched, and a new sea for which ambient seawater (approximately 10 L min−1) star was placed at the downstream section for the new trial. was pumped up from Lake Notoro, one of the lagoons on This observation was repeated 13 times for A. amurensis the coast of the Sea of Okhotsk, at the Okhotsk Marine Re- and 12 times for D. nipon in the summer, and 23 times for search Center of Tokyo University of Agriculture. While A. amurensis in the winter. Our definition of channel selec- food was not supplied to the sea stars for two to four weeks tion by the sea star was when it passed through two thirds before the start of each experiment, the scallops could al- of the channel length and, via the video images, we ex- ways feed on plankton in the pumped water. amined which channel the sea stars selected first after the To estimate how sea stars searched for live scallops cage was removed. If the sea stars were motivated to feed in the wild, we examined the food detection ability of A. and traced the chemical cue of the live scallop, they would amurensis and D. nipon in the summer (from June 11 to have moved directly to the channel where the live scallop July 29, 2015), whose mean water temperature was 17.4°C was tethered. We defined that sea stars showed predatory (between 13.2 and 20.4°C). We also examined the food behavior when they covered the scallop, even if they could Predatory behavior of sea stars on scallops 3 not successfully consume it and the scallop was still alive. All statistical analyses were conducted with freeware R To confirm a sea star’s response to the chemical cue of the 3.4.3 (R-Development-Core-Team 2017). live upstream scallop, we used Fisher’s exact test in a 2×2 contingency table to compare the frequency with which Results sea stars selected a channel (a live scallop or only shells) at their first migration against the types of behavior (preda- The Y-maze experiments showed that both A. amuren- tory or non-predatory). If they had tracked the chemical sis and D. nipon did not exhibit any significant selection cue of a live scallop, they would have more frequently se- behavior towards the live scallops placed upstream of the lected the channel where the live scallop was tethered and sea stars. In the summer, A. amurensis moved to one of possibly have shown predatory behavior. the two channels in 12 trials (92%) and D. nipon moved To examine the effect of relative body size on the pred- to one of the channels in 10 trials (91%). Predatory be- ator-prey relationship, we collected differently-sized Japa- havior was observed in 10 trials with A. amurensis (77%) nese scallops and the two sea star species. This experi- and in 9 trials with D. nipon (90%). In these trials, there ment was first conducted in the winter (from December 11, was no significant difference between the types of behav- 2016 to March 14, 2017) with a mean water temperature of ior (predatory or non-predatory) concerning the frequency −0.2°C (between −0.6 and 1.1°C), and then in the sum- with which the sea stars selected a channel (a live scallop mer (from July 1 to August 5, 2017) with a mean water or only shells) in A. amurensis (p=0.52, Table 1A) and in temperature of 20.2°C (between 17.4 and 23.0°C). The size D. nipon (p=1.00, Table 1B). In the winter, sea star move- of the scallops we used ranged between 47 and 124 mm in ment was observed in 11 of 23 trials (48%) and predatory SH, and the size of A. amurensis ranged between 40 and behavior was observed in five of 11 sea stars that moved 160 mm. The size of D. nipon (used for the summer experi- to one of the channels (45%). In the winter trials, there ments) ranged between 51 and 215 mm. We then experi- was no significant difference between the two types of be- mentally examined the effect of relative size between the havior concerning the frequency with which the sea stars sea star and the scallop on their predator-prey relationship. selected a channel (p=0.44, Table 1C). One sea star was put into a round basket (464 mm in diam- In the experiments that examined the effect of relative eter at the base, 310 mm in height, approximately 5×5 mm body size on scallop predation, both A. amurensis and D. in mesh size) that was sunk in a large seawater aquarium nipon exhibited two types of predatory behavior. In one (1200 L). As the ability of scallops to escape increases with type, the sea star completely covers the scallop from above their body size, we placed five size-matched scallops in and slightly lifts the center of its body while consuming the round basket to allow the sea star to easily access any the scallop by inserting its stomach into the shell (Fig. of the five scallops without chasing a specific one. These 2A). In the other type, the sea star holds the scallop from trials were repeated by changing the size combination of one sea star and five size-matched scallops in the baskets. Table 1. Frequencies of the channel directions that the sea stars We made 36 combinations for A. amurensis during the selected when predatory behavior was observed or not observed winter experiments, and 37 and 44 combinations for A. using Asterias amurensis in the summer (A), Distolasterias nipon amurensis and D. nipon, respectively, during the summer in the summer (B), and A. amurensis in the winter (C). Scallop and experiments. Each trial period was a maximum of 10 days Shell denote the channels where a live scallop or pair of shells was in the winter and four days in the summer. Survival of the tethered, respectively. Predation and No predation denote trials in scallops was observed each day, and the trial was termi- which predation behavior was observed or not observed, respec- nated when one or more of the five scallops died. As an tively. experimental control, we simultaneously observed the sur- A. Scallop Shell Total vival of differently-sized scallops in round baskets where sea stars were not included. As all scallops survived in Predation 4 6 10 11 replications of the control in the winter and only one No predation 0 2 2 of 140 individuals died in 28 replications of the control in Total 4 8 12 summer, we concluded that the deaths of scallops in the trials were caused by sea star predation. We calculated B. Scallop Shell Total ratios by dividing the size (SH) of the scallop by the size Predation 5 4 9 (AL) of the sea star in each size combination. We used the No predation 0 1 1 size of the largest scallop when two or more scallops were Total 5 5 10 preyed on in one trial, and we used the size of the smallest scallop when all five scallops survived, although their C. Scallop Shell Total size differences were small. To estimate the probability of Predation 4 1 5 scallop survival against the size ratio, we applied a logistic No predation 4 2 6 regression model to the binary data, i.e., survival or death, Total 8 3 11 collected from each experiment in the winter and summer. 4 H. Nishimura et al.

Fig. 2. Two types of predatory behaviors of the sea stars observed in our experiments. The photos were taken in the trials that used Disto- lasterias nipon. (A) Sea star is completely covering a scallop with its body. (B) Sea star is holding a scallop from the side.

Table 2. Results of the logistic models from each experiment. (A) Asterias amurensis in the summer, (B) A. amurensis in the winter, and (C) Distolasterias nipon in the summer. PP size ratio denotes the size ratio of prey to predator. Factor Estimate S.E. Z-value P-value A. Intercept −14.12 6.11 −2.31 0.021 PP size ratio 19.88 8.33 2.43 0.017 Residual deviance=9.8 df=34 B. Intercept −3.752 1.75 −2.04 0.041 PP size ratio 6.28 2.63 2.39 0.017 Residual deviance=26.4 df=34 C. Intercept −10.70 3.81 −2.81 0.005 PP size ratio 14.46 5.77 2.51 0.012 Residual deviance=15.2 df=42 Fig. 3. The probability of survival of the Japanese scallop when the relative sizes of the scallops and sea stars were changed. The prey-to-predator size ratio was calculated by dividing the size of (Fig. 3B, Table 2B). When the scallops were exposed to the scallop by that of the sea star. The results of experiments using D. nipon in the summer, M50 was 0.74 (Fig. 3C, Table 2C). Asterias amurensis in the summer and winter are shown in panels A Figure 4 shows the relationship between the size of the and B, respectively. The results of the experiments using Distolas- Japanese scallops and the prey-to-predator size ratio. The terias nipon in the summer is shown in panel C. Filled dots indicate horizontal axis begins with the smallest size (30 mm) of the results of each trial. Lines and gray areas indicate the estimated scallops that are released into the ﬁshing grounds of the logistic model in each experiment and its 95% conﬁdence interval, Sea of Okhotsk. The sizes of the sea stars are displayed in respectively. Open dots denote survival at which the scallops’ mor- 50 mm intervals (50, 100, 150, and 200 mm) that approach tality was 50% in each experiment. the maximum size used in our samples (226 mm). The area

above the constant lines of M50 in Fig. 4 suggests that the the side of the scallop’s shell and then consumes it (Fig. predation risk by sea stars rapidly decreases with increas- 2B). The latter behavior was generally observed when the ing scallop size. For example, the predation risk from sea arm of the sea star was shorter than the SH of the scallop. stars that are smaller than 100 mm is very low for scallops The logistic models in all three experiments showed that that are larger than 70 mm. the survival of the scallop increased with increases in the prey-to-predator size ratio (Fig. 3, Table 2). In A. amuren- Discussion sis, the ratios at which mortality was 50% (M50) was 0.71 in the summer (Fig. 3A, Table 2A) and 0.57 in the winter This study provides basic information about the preda- Predatory behavior of sea stars on scallops 5

ity is low when their prey is a live intact animal. The experiment investigating the effect of relative body size on scallop predation showed how the predator-prey relationship between the sea stars and scallops changes with their relative body sizes. As the sea stars in our experiments could easily access the scallops if they wanted to, the changes in the scallops’ survival rate because of the different relative size ratios was not caused by an increase in the ability of relatively large scallops to escape. A sea star would generally consume the scallop from the side when they could not cover it from above, suggesting that arm length was the determining factor in the predator-prey

relationship. There was little difference in M50 between sea Fig. 4. The relationship between the size of the Japanese scallop star species in the summer experiments, supporting the and the prey-to-predator size ratio. Dotted sloping lines indicate idea that arm length is a factor contributing to the success the changes in the ratio calculated from four fixed arm lengths (50, of their predation. Our study also showed that sea star pre- 100, 150, and 200 mm) of the sea stars when the shell height of the dation risk changes seasonally. The scallops tended to have scallop changes. Solid lines indicate the relative size ratio at which higher survival rates in the winter (Fig. 3A) than in the the scallops’ mortality was 50% (M50) in the experiments using summer (Fig. 3B), although the prey-to-predator size ratio Asterias amurensis in the summer (upper line) and winter (lower was lower than M50, indicating that the motivation or abil- line). Dashed line indicates M50 estimated from the experiment using Distolasterias nipon in the summer. ity of A. amurensis to seek prey decreased in the winter. The predator-prey relationship between the sea stars and the Japanese scallop at the species level is a case where the tory behavior of sea stars on the Japanese scallop. In the predatory impact in a food web has been oversimplified food-search experiment, we hypothesized that sea stars re- (Nakazawa 2017). spond to the chemical cues emanating from live scallops; The present study provides an important parameter in however, it was rejected under our experimental condi- estimating the predation risk from sea stars in scallop fish- tions. The results of Y-maze experiments suggest that sea ing grounds. In a typical Japanese scallop maricultural stars cannot correctly track live scallops using chemical year, fishermen release 1-year-old scallop juveniles to one cues flowing from a few meters away in the wild. This re- of four designated areas at the bottom of the sea after cul- sult was unexpected because tracking the chemical cues of turing the scallop spats in a suspended cage (Nishihama food is common in other sea star species (Castilla & Crisp 1994, Kosaka 2016). All surviving scallops are harvested 1970, Zafiriou 1972, Sloan & Northway 1982, Valentinčič three years later from the released area, and new juveniles 1985, Drolet & Himmelman 2004), and we also trapped the are released to the vacant area again after the harvest. In sea stars using fish meat in a cage. This unexpected result this cyclic culture, the scallops are composed of individ- may be related to the types of molecules coming from the uals from a single year class with little size differences food. According to a review by Kamio & Derby (2017), within each area. The minimization of the risk of predation scavenging foragers often search for food using dissolved by considering the sizes of both the scallops and sea stars amino acids (DFAA), which are released at high concen- has been suggested in other species of scallops and sea trations from recently injured organisms or fresh carrion stars (Barbeau et al. 1996, Magnesen & Redmond 2012). but are released at low concentrations from live intact or- We can recognize the density of all sea stars as a poten- ganisms. If sea stars indeed respond to specific molecules tial predator in each area from the relationships shown in such as DFAA, it would be reasonable that the sea stars Fig. 4. The monitoring of scallop size in each area of each did not respond to the live scallops with upstream orienta- fishing ground has already been conducted in the Sea of tion in our experiment. In fact, amino acids (Zafiriou 1972, Okhotsk, and the measurement of sea star size would also Valentinčič 1985) or fresh carrion (Castilla & Crisp 1970, be possible if scallop monitoring were conducted through Drolet & Himmelman 2004) were used in past studies that photographic images (Goshima & Fujiwara 1994) because demonstrated sea stars’ responses to chemical cues, al- sea stars would also appear in the images. In the wild, M50 though it is unclear whether those molecules were DFAA. may actually be lower than the one presented here because Thus, our observations of sea stars feeding in the cage the scallops can escape from the sea stars. However, the traps as scavengers suggest that sea stars would not track values may not be very different because the densities of the distant chemical cues of live Japanese scallops in the scallops in the fishing grounds are not low, i.e., between wild, but would instead forage the Japanese scallops once 15 and several individuals per m2 (Goshima & Fujiwara they got close enough to touch the scallops. The results of 1994, Paturusi et al. 2002, Miyoshi unpublished data). In this experiment suggest that foraging by A. amurensis and addition, Miyoshi et al. (2018) demonstrated that A. amu- D. nipon is opportunistic and that their food detection abil- rensis can move more quickly (45.9 m h−1 maximum) than 6 H. Nishimura et al. we previously imagined, implying that sea stars would eas- (Placopecten magellanicus (Gmelin)). J Exp Mar Biol Ecol ily be able to encounter a scallop in the fishing grounds. 180: 103–136. Barbeau MA, Scheibling RE, Hatcher BG et al. 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