Abstract

The Northern Pacific Starfish, Asterias amurensis (Lütken, 1871), is an active consumer of valuable bivalve mollusks, well adapted to a wide range of temperatures observed in the sea. Thanks to its ecological flexibility, this species significantly expanded its geographical range with ballast water and, due to colonization of artificial substrata by larvae, raised panic among marine aquaculture farmers. Within 2-3 months after settling on a substrate, its juveniles begin actively feeding on valuable bivalve mollusks: Patinopecten yessoensis, Mytilus trossulus, and Chlamys nipponensis. As it cannot eat adult P. yessoensis, the predator has adapted to its prey by coincidence of dynamics in their abundance. These dynamics have a quasi-two-year pattern, with the odd-numbered years within the interval 1977-1986 being fruitful in these two species. In 1986, a new 22-year solar cycle began, and since then the even-numbered years during the 23-year period were fruitful in these two species. However, after another 22-year solar cycle started since 2008, the odd-numbered years became fruitful again. A. amurensis uses alternative sources of food, and, due to the non-fastidious dietary habits, its nutritional demands vary depending on abundance of bivalves. As a result, the dynamics of bivalves population becomes smoothed. Abundance of A. amurensis larvae is adversely affected by industrial cultivation of M. trossulus; the red king crab Paralithodes camtschaticus, as in the case of introduction into the waters of Australia, Tasmania and New Zealand, can also reduce the abundance of A. amurensis spawners.

1. Introduction

The Northern Pacific starfish, Asterias amurensis (Lütken, 1871), is a native inhabitant of coastal waters of Russia, Japan, Korea, and northern China, which was introduced with ballast waters into the southern part of the Australia coast (particularly Tasmania), as well as into Alaska and the Aleutian Islands, into Europe and the American state of Maine ¹. In Australia, native scallop species respond weakly to the starfish ², which increases its negative impact on the local fauna. Due to the predatory activity of this animal, it is deservedly called “the sea pirate” ³. In its native region, the species inhabits depths of 0.5-103 m ⁴; in Australia, it can occur at a depth of more than 220 m ¹. On artificial substrates in semi-enclosed bays, its larvae can be found at depths of up to 14.5 m ⁵; in more open and deeper bays, up to 26.5 m ⁶. In the northwestern Sea of Japan (Russia), this starfish overwinters under negative temperatures of -1.6 to -1.9°C ⁷, and in shallow-water bays in summer it lives at temperatures of 28-30°C ⁸. According to our observations, it can survive ice-freezing, while its prey, Yesso scallop Patinopecten (=Mizuhopecten) yessoensis, dies under these conditions. Being more viable than P. yessoensis, the starfish A. amurensis showed good survivability in a solution of calcium hydroxide at a concentration of 3 to 6 g/L during 30 min. After being released to the natural environment, juvenile A. amurensis survived, while up to 75% of juvenile P. yessoensis were lost at a calcium hydroxide concentration of 3 g/L, and all scallops died at a concentration of 6 g/L ⁵. In the native range, the species spawns twice a year ⁹, with spring spawning being more favorable for its reproduction ⁵. Spawning in A. amurensis occurs later than that in P. yessoensis ¹⁰, and the duration of the pelagic period, about 6 weeks, is longer than in scallop ^{5, 11, 12}. At the moment when A. amurensis larvae are settling on a substrate, the latter is already occupied by bivalves whose metabolites can attract larval predators. Therefore, when selecting a substrate for settling, A. amurensis larvae use chemotaxis ¹³ and are found in those spat collectors, where the abundance of juvenile P. yessoensis is 1.23 times as high, the abundance of juvenile Chlamys nipponensis is 1.99 times as high, and that of the mussel Mytilus trossulus is 2.9 times as high ⁵. If the density of bivalves is connatural, its larvae settle in the collectors that are already occupied by starfish, even if they settled a few months before. Quite frequently two starfish of different sizes can be seen in one collector or cage with the absence of other starfish at the top and the bottom ⁵. The use of chemotaxis in searching for food was also noted for adult starfish individuals ^{14, 15}. As a result of the favorable feeding conditions that arise under scallop plantations, 10-year-old A. amurensis individuals with a diameter of 55 cm can be found on the bottom ⁵.

In the case larvae of A. amurensis settle in scallop collectors, its juveniles have a catastrophic effect on P. yessoensis cultured ¹⁶. A similar impact of starfish on cultured bivalves of the family Pectinidae was described earlier ^{17, 18}. Due to the similarity in dynamics of abundance of A. amurensis and the scallop P. yessoensis ¹⁹, as well as the increase in the predatory activity of A. amurensis in a fruitful year ⁵, surges of P. yessoensis population become smoothed. For this reason, aquaculture farmers are interested in developing methods to control A. amurensis ⁵. Farmers in Japan spend millions of dollars to mitigate its negative impact on cultivated bivalves ²⁰. The damages, caused to aquaculture farms by attacks of this predator, can be reduced when having a good knowledge of features of its ecology. However, the previously published works ^{21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32} are dedicated to other starfish species, or they need to be updated with the latest information on the ecology of its habitat in the native range. The goal of the presented work is to summarize materials of the long-term study, obtained from artificial substrates in Russia.

2. Material and Methods

To achieve this goal, the long-term studies of the spatial distribution of marine invertebrates on artificial immersed substrates were conducted off the coast of Primorsky Krai of Russia. The optimum time for installing artificial substrates-scallop collectors of the Japanese design-was determined for one of the first fouling organisms, the Yesso scallop P. yessoensis. Observations on its reproduction began with the study of the dynamics of gonadal index. In 1977-1990, every ten days, starting from the middle of May to late June, 25-30 individuals of P. yessoensis were collected in Minonosok Cove, Possyet Bay (42°36´ N, 130°51´ E) (Figure 1, st.1) using SCUBA diving equipment. Sex, total weight, weight of soft tissues, muscle, and gonads of each individual were measured to an accuracy of ±0.02 g. Similar works were conducted in Kit Cove (Figure 1, st. 15) (43°31´ N, 134°11´ E) from early June to early July in 1985-1987. The gonadal index in P. yessoensis was determined according to the method of ³³. The spawning time in bivalves was determined by a rapid decrease in the gonadal index in females by 9-12%. A week after spawning, plankton samples were taken with an Apstein net from the horizon 0-10 m at stations 1-3 in Minonosok Cove, every two to three days in 1977-1990, in 1995, and 1996; in Kit Cove, in 1985-1988; in Vladimir Bay (43°54´ N, 135°30´ E) (Figure 1, st. 16) in 1989; and in Amur Bay (43°09´ N, 131°47´ E) (Figure 1, st. 12) in 1999. The mesh size of the mill screen was 100 μm. Plankton samples were fixed with 4% formaldehyde. Larvae were counted and measured in Bogorov’s chamber under a MBS-9 microscope; the number of larvae was calculated per 1 m³. Simultaneously with plankton sampling, water temperature was measured at three horizons (0, 5, and 10 m). After scallop larvae reached 250 µm in shell height (settling stage), garlands of scallop collectors of Japanese design were installed in the western part of Possyet Bay (42°33´ N, 131°0´ E) in 1977-1982, 1985, 1988, and 1989; in Kit Cove in 1985-1988; in Vladimir Bay, in 1988-1989; and in Amur Bay, in 1999-2000. The general horizon of positioning of the collectors covered depths of 0-26 m. In 1980, self-designed collector - cages ³⁴ with an area of 6 m² were suspended with 0.5-meter intervals in a sea farm with an area of 0.25 ha, located in Kalevala Cove, Possyet Bay (42°30´ N, 13 0°51´ E) (Figure 1, st. 10). garlands of Japanese-design collectors consisting of 10 bulbous bags were suspended in the horizon 7-9.5 m at tri - stations in Minonosok Cove, Possyet Bay, from 1977 to 2015. During this period, the substrates were hauled up to the surface after 2-4 months of immersion of the collectors in the sea each year; in 1977-1984, twice a year. All bivalves and starfish were picked from the substrates, and living and dead individuals were counted. Shell height of bivalves and diameter of starfish were measured with a vernier caliper accurate to ±0.1 mm. The arithmetic mean and the error of the mean of the obtained values were calculated. In the autumn seasons of 1980 and 1981, we conducted observations over three-year-old P. yessoensis in lantern-shaped cages of Japanese design, seeded there at one year of age in June 1978 and 1979, respectively. Survival rate, shell height, and weight of soft tissues of scallops were compared between cages with and without starfish. To determine the impact of starfish on bivalve molluscs, the results obtained from collectors and cages without starfish were used. Marine bivalves provide the material evidence of mortality from starfish ³⁵.

The range of food preference in A. amurensis was determined according to: ³⁶; the range of diet, based on preference index α: ^{37, 38}.

where i = type of prey; n_io = number of prey organisms of the i^th type available; r_i = number of prey organisms of the i^th type consumed. The maximum estimated life span of A. amurensis was found based on Walford’s method using the following formula ³⁹:

where L is the theoretically maximum size, mm; L_max is the maximum size among the measured ones in the considered body of water, mm; t_max is the longest life span, years; K is the growth constant, determined as tangent of the slope of the straight line running through the experimental points.

To study the degree of influence of climatic factors on the dynamics of abundance and spatial distribution of A. amurensis, the daily values of water temperature and salinity, sea level, precipitation, and wind speed and direction in 1977-2014 were used. These data were collected by the Hydrometeorological Station (HMS) at the village of Possyet (42º39' N, 130º48' E) and granted to the author by Rostov I.D. from the Pacific Oceanological Institute (POI), Far Eastern Branch, Russian Academy of Sciences (FEB RAS). Spawning and the pelagic period of the considered invertebrates in Possyet Bay occur in June; therefore, to study the degree of influence of climatic factors during the period most important for their reproduction, the data of HMS for June were used. The values of solar activity, expressed in the Wolf numbers, were taken from the official website of the National Oceanic and Atmospheric Administration, USA: ftp://ftp.ngdc.noaa.gov. The error of the mean sea surface temperature in June of each year was calculated; the duration of the ice period in shallow-water bays was estimated by summarizing the days from the freeze-up to complete removal of ice from the bay.

In the autumn of 1977, an experiment was set up to determine the possibility of destroying juvenile A. amurensis with a concentrated solution of calcium hydroxide. A total of 4 juveniles of A. amurensis and 4 juveniles of P. yessoensis were placed for 30 minutes into a tank with a capacity of 3 L filled with a calcium hydroxide solution at a concentration of 3 and 6 g/L. The controls groups were A. amurensis and P. yessoensis, placed into tanks with clean sea water. At the same time, observations on the behavior of this predator and its prey in a large tank in the presence of 250 g calcium hydroxide, placed locally, were conducted for 2 days. The collected materials were processed statistically using the STATISTICA 6.0 software for PC (StatSoft Inc., Tulsa, Oklahoma, USA). The values of the regression analysis were tested at the level α = 0.05.

3. Results and Discussion

As a result of 38-year observations on artificial substrates, periodic changes in the abundance of settled A. amurensis larvae (Figure 2) were found. The most significant factors influencing on reproduction of the A. amurensis in Possyet Bay there was temperature of water and wind direction in June (Figure 3). Juveniles of this species cannot cope with one-year-old individuals of P. yessoensis, and, therefore, the dynamics of their abundance coincide ¹⁹. A similarity in the abundance dynamics between the predator and the prey was also found in Avacha Bay, Russia ⁴⁰. Until 1986, in odd-numbered years the abundance of juvenile starfish in scallop collectors was higher than that in even-numbered years; since 1986 (the new 22-year solar cycle), its abundance was usually higher in even-numbered years during 23 years (Figure 2). There are many works on the periodicity of variations in abundance of various animals ^{41, 42, 43}. The authors of the latter two publications associate the abundance fluctuations with quasi-two-year and longer, 11- and 22-year, cycles of solar activity. The variations in abundance of generations are apparently a response to the annual variability of climatic factors such as wind force, and solar radiation ⁴⁴. The coincidence of the abundance of juvenile predator and prey indicates a similarity of the factors regulating the dynamics of this parameter. In 1977-1979, the abundance of juvenile A. amurensis in the collectors reached approximately 1-2% of the abundance of juvenile P. yessoensis ⁵. In 1977, in Minonosok Cove, Possyet Bay, a high abundance of juvenile A. amurensis was recorded from the scallop collectors (with a mean value of about 10 ind./m²), which resulted in 95% mortality of juvenile P. yessoensis ⁵. To reduce the future abundance of A. amurensis larvae, a large-scale catch of individuals (with a total number of 2,000) from the bottom was organized, and, at the same time, one-year-old and adult P. yessoensis from the cages were seeded to the bottom. After that, the ratio of the abundance of juvenile A. amurensis and P. yessoensis spat changed and became better. In 1983, the density of juvenile starfish was already 22 times as low, and the density of juvenile P. yessoensis was 2 times as high as those in 1977, when the breeding conditions were similar. As catches of A. amurensis and seeding of P. yessoensis onto the bottom have been continued to date, the current ratio of abundance of juvenile A. amurensis to that of P. yessoensis spat is already 0.24%, according to the observations in 1997-2008.

During 23 years (1986-2008), higher abundance of the predator and the prey was recorded in even-numbered years. However, after a decade of industrial cultivation of the bay mussel Mytilus trossulus over 16% of the area of Minonosok Cove, Possyet Bay (1979-1989), when its daily filtration activity reached 86.4% of the water volume of the cove ⁴⁵, the relationship between the dynamics of P. yessoensis and A. amurensis was somewhat disturbed (Figure 2). As is known, larval mussels cause a grazing load on a phytoplankton community of coastal waters ^{46, 47}. The bay mussel, M. trossulus, spawns earlier than A. amurensis ¹⁰; therefore, by the time when A. amurensis larvae appear, a shortage of food can arise in the sea ⁴⁸. The presence of adult mussels on collectors, due to their filtration activity, can also have a negative effect on abundance of A. amurensis larvae, as ingestion of large-sized larvae from plankton by mussels was known long ago ^{49, 50}. After the termination of industrial cultivation of M. trossulus in Minonosok Cove, the abundance of juvenile A. amurensis in scallop collectors began increasing (Figure 2). During the period 1977-1990, the periodicity of fluctuations in the abundance of juvenile A. amurensis in the western part of Possyet Bay was similar (Figure 4), and in 1981-1986 it coincided with that in other areas of Peter the Great Bay ⁵¹.

In open waters of Possyet Bay, due to the abundant settlement of A. amurensis larvae, an increased mortality of juvenile P. yessoensis was observed in 1978-1979 (Figure 5). One individual of A. amurensis with a diameter of 20-30 mm destroyed 18.3 ± 12.7 scallops by October 3-24 (within 2-2.5 months on a substrate), i.e. it consumed 0.3 scallops per day ¹⁶. However, according to the data from literature, one A. amurensis consumes 0.8 individuals of P. yessoensis spat per day ²². This difference can probably be explained by the fact that we observed younger individuals of A. amurensis that had just switched to animal food. Recently metamorphosed carnivorous starfish of 0.5 mm in diameter use organic particles suspended in the water ³⁰. To increase the body weight by 2.1 g, it took for A. amurensis to eat 3 g of bivalves’ meat within a month (digestibility 70%) ⁵. This is much less than recorded from older starfish in tanks ²⁴. In our experiment in tanks, from October 3 to October 4, 1977, only the biggest starfish individuals, 58 mm in diameter, were hunting scallops, and they attacked in a group of 2-3 individuals. A young A. amurensis with a diameter of 17 mm and a weight of 0.5 g, placed into a tank, spends some time in the surface layer of water ²⁴, which has a concentration of microalgae and organic matter several times as high as that at the bottom ^{52, 53}. Starfish feeding on algae, as well as on suspended and dissolved food were reported earlier ^{54, 55, 30}. Single A. amurensis begin feeding on P. yessoensis not immediately, but some time later, when bivalves reach 20 mm in shell height. In a collector without starfish, even smaller dead scallops occur than in collectors with starfish. They begin preying on mussels a little earlier (Figure 6).

The favorite prey of A. amurensis is P. yessoensis and M. trossulus (Figure 7). In collectors-cages the substratum for settlement of larvae is presented by the polyethylene cones are produce on the press automatic machine with platforms ³⁴, A. amurensis mainly eat P. yessoensis, M. trossulus, and Ch. nipponensis (Figure 8). The preference for some bivalves, manifested by A. amurensis, was previously found by ⁵⁶. The Swift’s scallop Swiftopecten swifti, settling mainly into the internal part of the cones in collector - cages, survives even if other bivalves die. Here it is inaccessible to A. amurensis; however, the starfish Lisastrosoma anthosticta, especially if several individuals are present in the same collector, can reach and eat s. swifti thanks to the softness of their skeleton. In Japanese bag collectors, A. amurensis has no barriers, and S. swifti is also destroyed. A high survival rate in cage collectors is observed only for the mussels Crenomytilus grayanus, Modiolus kurilensis, and Arca boucardi. Their high survival rate is probably explained by the fact that they inhabit the inner part of collector - cages, and also that A. amurensis are not adapted to them.

In collectors with and without starfish, dead 5-6-millimeter P. yessoensis have a similar diet index, which suggests their death without the participation of starfish. The increased occurrence of dead 6-7-millimeter P. yessoensis can already be considered as an evident ingestion for this size group among starfish. They begin preying on M. trossulus earlier, when the latter reach a shell height of 4-5 mm (Figure 9A). On a substrate with two A. amurensis, mainly Ch. nipponensis with a shell height of 0-5 mm are consumed, while on a substrate with three starfish, M. trossulus of the same size is the most preferred prey. A little later, after bivalves reach 5-10 mm in size, starfish’s dietary preferences shift towards P. yessoensis, and this species becomes the most popular food item among two starfish after reaching the size of 10-15 mm (Figure 9B). In another collector with one starfish, the most preferable among the smallest bivalves (2-4 mm) was M. trossulus and, to a much lesser extent, Ch. nipponensis and P. yessoensis. However, when bivalves reached 4-6 mm, Ch. nipponensis became the most preferable food for A. amurensis. (Figure 9C). At the same time, among the smallest bivalves (2-4 mm), four A. amurensis showed preference for Ch. nipponensis; among larger ones (4-6 mm), M. trossulus (Figure 9C). If the substrate is abundantly populated with A.amurensis (6 ind.), they, as in the previous case, switch to animal food earlier and begin consuming small bivalves (0-5 mm), with P. yessoensis and M. trossulus destroyed in greater numbers; however, after bivalves reach 5-10 mm, Ch. nipponensis becomes most preferable (Figure 8D). In case of 8 individuals of A. amurensis settling in the collector, the most preferable among small bivalves are M. trossulus and Ch. nipponensis; among larger bivalves (5-10 mm), again M. trossulus (Figure 9D).

During three years of being in a scallop cage, A. amurensis, born in a year of middle abundance, has time to destroy 59 ind. of P. yessoensis, 44 ind. of M. trossulus, and 12 ind. of Ch. nipponensis. The total wet weight of animals consumed by A. amurensis is about 870 g, i.e. its annual food consumption is 400 g, which is close to the ration of this starfish in a tank ²⁴. Within these three years, the wet weight of A. amurensis reached 271 g, and, thus, the digestibility of its food constitutes about 31%. Processing of the material for the entire observation period (1978-2008) showed that the overall rate of mortality of P. yessoensis in a collectors is 31.9%; S. swifti, 26.9%; M. trossulus, 10.8%; and Ch. nipponensis, 6.6% (Figure 10 ). Taking into account that the mean rate of mortality of P. yessoensis without A. amurensis does not exceed 1.48%, the net mortality caused by starfish is therefore 30.4%. This confirms the conclusion about P. yessoensis as the most preferred food for A. amurensis.

The study of the entire size group of P. yessoensis individuals lost in the collectors, shows an increase in 7-mm individuals to 4%, and larger ones, 8-12-mm, to 5% (Figure 11). After seeding of P. yessoensis onto a sandy bottom with the biocenosis of Spisula sachalinensis + Zostera marina, the mortality of one-year-old to three-year-old individuals was low and did not reach 2%. However, after reaching the age of four (shell height 132 mm), it increased sharply to 3% (Figure 11).

However, A. amurensis does not always have a negative effect on P. yessoensis. For the predator, the great value has a choice of a prey ⁵⁶, and if A. amurensis larvae settle in cages with one-year-old P. yessoensis, they cannot cope with the latter and destroy bivalves of the same generation as they are (M. trossulus and P. yessoensis). A reduction in food competition results in the situation when the values of production of cultivated bivalves increase. In August 1980, the mortality of three-year-old P. yessoensis in the cages without stars in Minonosok Cove reached 20%, and in the cages with A. amurensis almost all P. yessoensis were alive. These three-year-old P. yessoensis individuals, living in cages with two-year-old A. amurensis, had a higher survival rate, size, and weight of soft tissues than in cages without A. amurensis (Table 1).

Both the absence of A. amurensis and their abundant presence in collectors have an adverse effect on biodiversity of bivalves. The number of A. amurensis optimal for providing the diversity of species is 1 individual. In this case, the number of bivalve species is by 1 greater than in collectors without starfish and by 2 greater than in collectors with two starfish (Figure 12). Predators increase the diversity of species in a community ⁵⁷.

The damage caused by A. amurensis to bivalves varies between years. It is lower in the years of lean of P. yessoensis (Figure 8), which indicates an optimization of consumption of the trophic resources by starfish. The equation describing the relationship between the abundance of juvenile P. yessoensis and the abundance of individuals eaten by one A. amurensis by September 14 of each year is as follows:

where x is the abundance of juvenile P. yessoensis in collector; Y is the abundance of consumed individuals.

In a fruitful year, one A. amurensis on the average destroyed 47.2% of P. yessoensis, 22.5% of M. trossulus, and 30.8% of Ch. nipponensis; in a lean year, the mortality from one starfish decreased to 2.4; 2.3, and 4.7%, respectively (Figure 8). The similar dynamics in abundance of the predator and the prey, as well as the variations in predatory activity depending on abundance of the prey, result in the situation when at about the same time, but in different years, the number of bivalves consumed by starfish has different values. The higher the fruitful of juveniles of the studied bivalves, the more of them die (Figure 8). In nature, this has a certain biological sense that leads to stabilization of a community.

According to observations of Japanese researchers, the maximum feeding intensity in A. amurensis occurs at a water temperature between 10 and 20°C ^{25, 58}, with the optimum temperature of 14°C ⁵⁹. By late October 1977, at a water temperature of about 10°C, we observed the largest number of empty valves of P. yessoensis of different ages and the maximum number of A. amurensis attacks on this bivalve on the bottom of Minonosok Cove. It is probable that a decrease in the water temperature from 15.2 to 10.7°C after the autumn storms caused the bivalves to fall into a torpid state, which was used by predators. Juvenile P. yessoensis, which have not reached 23-27 mm in shell height on the bottom by autumn, are usually destroyed (Figure 11). Variations in feeding behavior are observed in other starfish species also. One of the maxima in starfish occurs in October ⁶⁰, whereas in winter their predatory activity frequently declines ^{61, 62}. The ration and behavior of starfish during feeding may depend on their size, type of prey, behavioral features, time, and season ³⁰. In October 1977, juvenile A. amurensis in the tank attacked juvenile P. yessoensis only in the afternoon ⁵. This is also confirmed by ⁶³. Starfish adapted to darkness move in a random direction ⁶⁴, cited by: ³⁰. At the same time, Asterias rubens occurred in traps at from 20:00 to 12:00 and never was caught from 12:00 to 20:00 ²⁰.

The curves of growth of A. amurensis in scallop collectors are quite similar during several years; however, in a lean year the growth curve is gentler (Figure 13). In autumn, their growth rate is higher and decreases in winter. Decrease in rates of growth in the winter is registered and at Asterias rubens ³¹. The equation of group growth of A. amurensis within the first 3 years is as follows:

where x is the period from the beginning of spawning, days; Y is the body diameter, mm. By late October of the third year of life, the diameter of A. amurensis reached 233 mm. On the bottom, A. amurensis are apparently in less favorable conditions. In the first ten days of June 1981, starfish born in 1979, which had got from the collectors to the bottom, were smaller in size than those in cage collectors of our design. After settling in a more fruitful year, 1983, the wet body weight of starfish with a similar size proved to be higher. It has long been known that fecundity of organisms depends on body weight ⁶⁵. According to our observations, A. amurensis, as well as P. yessoensis, achieve high fecundity by the third year. Therefore, a more abundant and prolific generation proceeds to spawning, more sexual products are released, and the abundance of juvenile P. yessoensis coincides again with that of A. amurensis within a year after birth. The coincidence of breeding conditions and the flexible tactics of feeding behavior in A. amurensis slightly smooth down the fluctuations in the abundance of P. yessoensis.

According to our observations, P. yessoensis is able to live up to 17 years; however, in a major portion of bivalves the life span does not exceed 10 years, and, as we have already noted, four-year-olds show a higher mortality rate (Figure 11). The mass mortality of the starfish A. amurensis also occurs at four years age, after spawning ⁶⁶. The similarity in life span between A. amurensis and P. yessoensis suggests that starfish accompany and actively regulate the abundance of scallop starting from the first year of their life. A. amurensis, which reduces the density of bivalves, as its competitors, in a collector, apparently facilitates availability of food, which often results in increased size of survived P. yessoensis and M. trossulus as compared to a collector without starfish (Figure 6). As the number of predators increases to two, the size of P. yessoensis sometimes also grows there (Figure 14). In 71.4% of cases, sizes of live P. yessoensis in the collectors with A. amurensis and without them differ significantly.

It is probable that the violation of the classic thesis on reduction in prey size as a result of consumption of large individuals by predators ⁶⁷ can be explained by the delayed switching to animal food in A. amurensis, and by the tendency in bivalves to prevent themselves from death with intensified growth of shell ⁶⁸. However, in the case the number of A. amurensis increases to three, the size of P. yessoensis and M. trossulus in the collector reduces (Figure 14). When several individuals of A. amurensis settle in the same collector, they begin destroying younger P. yessoensis (Figure 6). In fruitful years, 1981 and 1994, two or more individuals of A. amurensis settled on the cones of cage collectors with an area of 0.1 m². It is probable that due to the group effect, they destroyed all bivalves as early as in the autumn (the mean size of empty valves of P. yessoensis was 11.1 mm). Other species of dead bivalves were also small in size. However, despite the lack of animal food, all A. amurensis remained alive by late April of the following year. Feeding on alternative food in A. amurensis is observed at an older age also. In the cage collectors, which were installed in Kalevala Cove, Possyet Bay (42°30´ N, 130°51´ E), in 1980 and touched the bottom by September 1982, some A. amurensis individuals became pressed (immobilized) between the cones and the cover. They were alive, their diameter was about 190 mm, and only tips of the rays began decaying. In order to prevent dying from hunger, A. amurensis had to feed on alternative food sources. The lack of animal food in A. amurensis is probably compensated by detritus-eating and seston-eating, which confirms the observations by ⁶⁹. A flexible food strategy is demonstrated by related species, A. rubens ^{70, 71} and Stichaster australis ⁷².

Larval A. amurensis do not move far from spawners. According to our SCUBA-diving examinations, adult A. amurensis do not occur on the bottom of Kit Cove (43°3´ N, 134°11´ E), and during four years of observations we did not find juvenile A. amurensis in collectors. However, north of this area, in Vladimir Bay (43°54´ N, 135°30´ E), at a distance of about 150 km up the cold coastal Current, flowing from the north along the coast of Primorsky Krai, adult and juvenile individuals are found in scallop collectors (Figure 4). Therefore, in case of catching the spawners within the water area assigned to a farmer, settling of starfish larvae on substrates will be limited. In the western Possyet Bay, juvenile A. amurensis occurs more frequently in collectors installed in the open Reid Pallada Cove (42°32´ N, 130°52´ E) (Figure 4). In this area, more P. yessoensis settle in collectors also ⁷³, but the largest number of juvenile A. amurensis was found in the collectors in Ussuri Bay (43°02´ N, 132°09´ E) (Figure 4). In 1991, there we found an unusually high abundance of this starfish and on the bottom at a depth of 20 m. The young-of-the-year of A. amurensis formed a continuous cover on the silty/sandy bottom sediment. This bay is probably favorable for breeding of the species because it does not receive large rivers and is characterized by a higher water salinity compared to that of Possyet Bay ⁷⁴. Negative influence of storm and low salinity on population of starfishes is revealed and at Asterias rubens ³¹. The climatic features of the year have a significant impact not only on the reproductive success in the starfish, but also on the spatial distribution of its juveniles. In the cold year 1977, the maximum abundance of juvenile Northern Pacific starfish was recorded 9 km off the warm-water Expeditsii Cove (42°39´N; 130°44´E); in the warm year 1980, it was already 12 km off (Figure 15). The site of the greatest distance of the maximum abundance of juveniles in the open sea depends on the solar activity, expressed in Wolf numbers, and on the mean value of wind direction in June (Figure 16).

The most intensive settling of A. amurensis larvae into scallop collectors is observed at a horizon of 4.0-6.5 m ¹⁶, and the maximum depth of occurrence in semi-enclosed coves of Possyet Bay reaches 14.5 m ⁵. It is probable that, in addition to chemoreception, A. amurensis larvae use thermopathy when selecting a substrate, because, as we noted in the semi-open Reid Pallada Cove (42°32´ N, 130°52´ E), they occupy the horizon 18 m, and in the more open Kitovy Bay (42°35´ N, 131°3´ E) they occur at a depth of 26.5 m ⁶. The structure of vertical distribution of larvae Asterias rubens depends on temperature at a surface ⁷⁵, and also speeds of a current and its direction ³². The increase of larval aggregation about of water - table at high of population density is result of the behavioural response to competitors ⁷⁶. In the cold and fruitful year, 1979, A. amurensis larvae rather occupied the horizon 3-7 m, but in warmer lean years, they moved deeper (Figure 17). The depth of the maximum abundance of A. amurensis is greatly influenced by the duration of the previous ice period, precipitation, and height of tides in June (Figure 18). This relationship of the vertical distribution of A. amurensis with climatic factors can be used for optimizing the horizon at which collectors are positioned. Taking into account that in a fruitful years the largest number of starfish larvae occupy the horizon 3-7 m, scallop collectors can be positioned not at depths of 10-16 m ⁷⁷ but above, in the horizon 9-15 m. The most variable horizon of vertical distribution of A. amurensis is located at depths of 3 and 9 m (Figure 19).

One of the measures that provide more successful cultivation of bivalve mollusks is to reduce the population of predatory starfish. The techniques to control A. amurensis, known to us, can be divided into chemical, biological, and physical ⁵. The increase in oyster production in the USA since 1965 after a 50-year decline in catches is explained mainly by the efficient measures to protect oysters from predators ⁷⁸. The known chemicals used in aquaculture are calcium hydroxide (slated lime) ^{78, 79}, copper sulphate (blue vitriol) ^{17, 80}, halite (rock salt), organochloride-based biocides (“Polystream”) ⁷⁸, as well as water freshening ⁸¹. In addition, ⁸² recommend using barriers built of sand treated with dipolychlorinated benzene supplemented with insecticides (2-chloro-1-nitropropane, or Sevin) against predators of edible mollusks (gastropods, sea stars, and crabs): these barriers having a width of 1 m kill predators or frighten them away.

In our experiments on A. amurensis control, we used calcium hydroxide. The experiment has shown that A. amurensis respond to the presence of this compound in water faster than P. yessoensis do. They stop moving earlier, and their color turns pale. However, after returning to the clean seawater, almost all individuals revive and normally move within at least 3 h of observation. At the same time, 70-75% of P. yessoensis are lost after being in water with a calcium hydroxide concentration of 3 g/L; at a concentration of 6 g/L, all bivalves die. Based on this experiment, as well as on the simultaneous observations over the behavior of A. amurensis and P. yessoensis near a handful of calcium hydroxide in a tank, it can be concluded that this compound cannot be used for selective destruction of A. amurensis in the presence of P. yessoensis, for example, by placing collectors in a container with a limewater solution. For this, copper sulphate is more suitable. According to Japanese researchers ¹⁷, the effect of copper ions at a concentration of 1.5 parts per million kills juvenile starfish within 50 min without causing harm to scallop. Calcium hydroxide can be used to create obstacles on the bottom, preventing starfish from penetration into scallop cultures.

The significant decrease in abundance of juvenile A. amurensis at depths greater than 7 m can be used to reduce its abundance on artificial substrates. In collectors and cages suspended at a depth of 10-14 m there will be 2-3 times fewer starfish (Figure 20). In other regions, farmers use their own horizons of preferred depths for starfish and scallops. off the Atlantic coast of Canada the number of scallops increases and the number of starfish decreases in collectors immersed deeper than 8 m ⁸³. In the same region, larval scallops settle later than starfish, and thus, when collectors are placed in the sea after settling of starfish larvae, their number in collectors decreases ¹⁸.

No less important are biological methods of protection of bivalves from starfish. Cultured bivalve mollusks spawn earlier than A. amurensis do ⁹, and M. trossulus larvae can exert a trophic load on phytoplankton in semi-enclosed coves ⁴⁷. Therefore, a reduction in food availability in the sea due to its consumption by larval and adult bivalves can lead to a decrease in the survival and growth rates of A. amurensis larvae. Shortage of food can be one of the main factors that caused a ten-year decline in the abundance of A. amurensis after the beginning of cultivation of not only P. yessoensis, but also M. trossulus in Minonosok Cove, Possyet Bay, in 1979 ⁴⁸. The study of the 35-year dynamics of abundance of A. amurensis and M. trossulus has shown that the Pearson’s coefficient of correlation between them is -0.39 (p = 0.022). The industrial cultivation of M. trossulus affected the dynamics of abundance of not only A. amurensis, but also on spawning later the oyster Crassostrea gigas and the valuable echinoderm Apostichopus japonicus ⁸⁴. After the termination of the industrial cultivation of M. trossulus in this cove in 1989, the abundance of juvenile A. amurensis in scallop collectors began recovering (Figure 2). We have already noted that in the open Reid Pallada Cove, more larvae of A. amurensis settled into collectors. The positive effect of waves on abundance of fouling organisms is reported by ⁸⁵. Therefore, the use of semi-enclosed coves for cultivating bivalves can also reduce the negative impact of the dangerous predator.

The study of horizontal distribution of spawners and larvae of A. amurensis showed that the coast of Primorsky Krai has open areas exposed to severe storms, where this species is not found: Melkovodnaya Cove (42°51´ N, 133°36´ E) and Kit Cove. Moreover, adult and juvenile A. amurensis in the north, in Vladimir Bay, are not as aggressive as in Possyet Bay. This can be explained in part by the fact that at the time of observations the starfish in the collectors were still small and just switching to animal food, and no observations over the bottom were conducted in autumn. However, in spring and summer we did not find high predatory activity of adult A. amurensis and empty valves of P. yessoensis that had died in the autumn on the bottom. The reduction of mortality of P. yessoensis from starfish in the northern part of the population range may be explained by the fact that there may be genetic differences between the two remote populations of A. amurensis, caused by different proportions of prey species and resulting in different food preferences at predators ^{86, 87}. These areas with a lack of starfish or a reduced predatory activity of A. amurensis are most preferable for harvesting and on-growing larval P. yessoensis.

As is known, in its native range A. amurensis is consumed by the starfish Solaster paxillatus ⁸⁸ and a valuable commercial crab species, the red king crab Paralithodes camtschaticus ⁸⁹. Introduction of the starfish into the southern hemisphere does not make sense due to the existence of native starfish species there, while P. camtschaticus can be a desired invader in coastal waters of Australia and New Zealand. There the Pacific oyster Crassostrea gigas ⁹⁰ has already successfully adapted, but P. camtschaticus is an even more valuable seafood item. It does not need to be cultivated, as it makes shoreward migrations for spawning, and at this time its meat becomes of high value. Before the economic reforms in Russia, the price of one large live crab reached $120 USD at Japan markets. In the late 20^th century it was successfully transplanted from the Pacific Ocean to the north of Europe, and now its stock has reached a commercial size.

The optimum ranges of such parameters as water temperature and salinity for the normal life activity of red king crab in the Barents Sea, the same as in the native range, are from 2.4 to 7.0°C, with the boundaries of its temperature tolerance ranging from -1.6 to 18°C ⁹¹, and 31-33‰ ⁹², respectively. During spawning, the crab moves to shallow water and spends there 4-6 months ⁹¹. Coastal waters of New Zealand provide the same conditions ⁹³, which allows us to conclude that the local abiotic environmental factors are suitable for acclimatization of P. camtschaticus in the new region. It consumes a wide range of living and dead organisms ^{91, 94, 95}, including algae ^{91, 96}, and, therefore, does not have a negative impact on the benthos of the habitat new to this species ^{94, 97, 98, 99}. Consumption of echinoderms, including the starfish A. amurensis, is required for the crab to build its own exoskeleton after molting ⁸⁹. There are already several predatory invertebrates introduced on the Australia-New Zealand shelf. In addition to A. amurensis, it is inhabited by the European green shore crab Carcinus maenas ¹⁰⁰, on which P. camtschaticus can also prey, as can be confirmed by our observations over the dynamics of abundance of juvenile crabs settling in scallop collectors. Since the middle 1990s, when the P. camtschaticus juveniles ceased to occur in scallop collectors after the overharvesting of spawners in Possyet Bay, a surge of abundance of small-sized crabs-Cancer amphioetus and Pugettia quadridens-was recorded there. By consuming active phytophages such as sea urchins, P. camtschaticus contributes to the recovery of marine algae stocks in the Barents Sea, the new habitat to it ⁹¹. Juveniles of this crab are a prey for valuable fish species, which improves their living conditions ¹⁰¹.

The materials presented allow drawing a conclusion that there is an opportunity to reduce the abundance of the dangerous predator-starfish A. amurensis-on the Australia-New Zealand shelf by introducing the red king crab P. camtschaticus, a valuable omnivorous species.

Our observations in Minonosok Cove, Possyet Bay, showed that the ratio of P. yessoensis to A. amurensis decreased from 1-2% to 0.1-0% from 1977-1979 to 1983-1984 (Figure 2). This is related most likely to the measures for controlling the starfish abundance, taken by aquaculture farmers in this cove since 1977. Almost every year, 1,500-2,000 mature individuals of A. amurensis were caught there, and, simultaneously, year-old and adult P. yessoensis were seeded on the bottom. The positive effect of harvesting mature starfish on reduction in the abundance of starfish larvae can also be used in other areas. The cheapest mechanical techniques of starfish control are the use of underwater plow, suction dredge ⁷⁸, or modern types of dredges.

4. Conclusion

The Northern Pacific Starfish, Asterias amurensis (Lütken, 1871), due to its good adaptability to a wide range of water temperatures, as well as thanks to active marine traffic, has distributed widely around the globe. Its capability of colonizing artificial substrata and active feeding on valuable bivalve mollusks raised panic among marine aquaculture farmers. Our long-term observations in the native range allowed us to reveal some ecological features of this predator, which can help mitigate its negative impact and also control the dynamics of its abundance. It turned out that juvenile A. amurensis cannot cope with their main prey, the scallop P. yessoensis, in case it is one year older than the starfish, and this evolutionarily resulted in a similarity in the dynamics of their abundances. These dynamics have a quasi-two-year pattern, which is replaced by the opposite one with the onset of another 22-year solar cycle. In our case, until 1986, odd-numbered years were fruitful both in the predators and in the prey, whereas from 1986 to 2008 the even-numbered years were fruitful in them. With the onset of another 22-year solar cycle, in 2009, the odd-numbered years became fruitful again. In case of lean year, A. amurensis is able to switch to alternative sources of food without any serious harm to its growth, which allows the offspring of bivalves, being not so numerous, to survive. We have found that this predator is more tolerant than the scallop to ice-freezing and being in solution of calcium hydroxide; therefore, not all chemical reagents can be used for selective destruction of starfish in the presence of mollusks. The dynamics of A. amurensis abundance can be negatively affected by freshening of surface waters, industrial cultivation of the early-spawning bay mussel Mytilus trossulus, as well as harvesting of starfish spawners near aquaculture facilities. However, the mussel M. trossulus can also negatively influence the reproduction of such late-spawning valuable invertebrates as Crassostrea gigas and Apostichopus japonicus. Therefore, in our opinion, the introduction of a valuable crustacean-the red king crab Paralithodes camtschaticus-into the waters of Australia, Tasmania and New Zealand can be the most preferred biological protection against A. amurensis. This crab shows the temperature and salinity preferences which meet the conditions existing in the region new to it. It spends 4 to 5 winter and spring months in shallow waters, where it has a wide feeding spectrum, including A. amurensis and small-sized crabs required to build a new carapace, and thus it will not cause any substantial damage to valuable invertebrates.

Acknowledgements

The author thank the translator Shvetsov e.P. for transfer of the manuscript into English language, and also Grigoriev V. N, Shevchenko Е.N. and Yakovleva M. for the help in carrying out of technical works. The presented material has not been supported by grants.

References