Offshore dispersion of ephyrae and medusae of Aurelia aurita s.l. (Cnidaria: Scyphozoa) from port enclosures: Physical and biological factors

Journal of Marine Systems 152 (2015) 75–82

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Offshore dispersion of ephyrae and medusae of Aurelia aurita s.l. (Cnidaria: Scyphozoa) from port enclosures: Physical and biological factors Ryosuke Makabe a,b,⁎, Hidetaka Takeoka c, Shin-ichi Uye d a

National Institute of Polar Research, 10-3 Midori-cho, Tachikawa, Tokyo 190-8518, Japan Department of Polar Science, The Graduate University for Advanced Studies (SOKENDAI), 10-3 Midori-cho, Tachikawa, Tokyo 190-8518, Japan c Center for Marine Environmental Studies, Ehime University, Matsuyama 790-8577, Japan d Graduate School of Biosphere Science, Hiroshima University, 4-4 Kagamiyama 1 Chome, Higashi-Hiroshima 739-8528, Japan b

a r t i c l e

i n f o

Article history: Received 10 February 2015 Received in revised form 21 August 2015 Accepted 24 August 2015 Available online 29 August 2015 Keywords: Jellyfish bloom Artificial structures Polyps Physical model Predation Chrysaora

a b s t r a c t Recurrent outbreaks of the common jellyfish Aurelia aurita s.l. have been increasingly significant, particularly in human perturbed coastal waters, where numerous artificial constructions increase suitable habitat for polyp populations. We examined the spatiotemporal dispersion process in 6 ports of ephyrae of A. aurita after release from strobilating polyps, to offshore waters of northern Harima Nada (eutrophic eastern Inland Sea of Japan) from January to May 2010. Almost exclusive occurrence of the ephyra stage in the ports demonstrated that their seeding polyps reside in the port enclosures, and liberated ephyrae are rapidly exported offshore by tidal water exchange. Post-ephyra stages occurred primarily outside the ports, and their age increased gradually offshore, ca. up to 9 km off the ports, and the pattern of age increase could be simulated by a simple diffusion model. However, there was an abrupt decline in A. aurita density beyond ca. 3 km off the shore, where jellyfish-eating Chrysaora pacifica medusae were prevalent. We conclude that physical forces are primarily responsible for offshore dispersion of A. aurita, and a biological factor, i.e. predation by C. pacifica, jointly affects the distribution pattern of A. aurita. © 2015 Elsevier B.V. All rights reserved.

1. Introduction In recent decades, more attention has been paid to large and/or unusual population outbreaks, or blooms, of jellyfish around the world's oceans (Brotz et al., 2012; Condon et al., 2012; Hamner and Dawson, 2009), because they often exert negative impacts on various human enterprises (fisheries, aquaculture, tourism, power plant operation, etc.) and marine ecosystem services involved in fish production (Pitt and Lucas, 2014; Richardson et al., 2009; Uye, 2011). Among scyphozoans causing problematic blooms, the common jellyfish Aurelia aurita s.l. has been most intensively studied, because of cosmopolitan distribution in temperate coastal regions and more recurrent and extensive outbreaks in association with increased human impact on marine coastal environment (Di Camillo et al., 2010; Dong et al., 2010; Purcell, 2012; Purcell et al., 2007; Uye and Ueta, 2004). However, our current knowledge is still inadequate to understand how the population dynamics of A. aurita lead to medusa outbreaks. Hence, full identification of causes for the outbreaks is necessary for forecasting outbreaks prior to the

⁎ Corresponding author at: National Institute of Polar Research, 10-3 Midori-cho, Tachikawa, Tokyo 190-8518, Japan. E-mail address: [email protected] (R. Makabe).

http://dx.doi.org/10.1016/j.jmarsys.2015.08.002 0924-7963/© 2015 Elsevier B.V. All rights reserved.

season of medusa blooms, and for developing countermeasures to alleviate their damage. The size of an A. aurita medusa population can be determined basically by two factors, viz. the abundance of ephyrae produced, and their mortality to recruit into medusa stage. The former factor, in turn, integrates settlement of planulae on suitable substrates, asexual reproduction of polyps by budding, proportion of strobilating polyps and number of disks produced by strobilae (Lucas, 2001; Lucas et al., 2012; Miyake et al., 2002). Previous studies have suggested that temperature elevation, increase of food supply by eutrophication, elimination of competitors and predators by hypoxia, and increase of attachment sites on marine structures favor reproduction of polyps to build a larger population (e.g. Duarte et al., 2013; Han and Uye, 2010; Ishii et al., 2008). Such environmental conditions often prevail in ports and marinas constructed along the coast, particularly in densely populated urban areas, and these port areas often harbor huge numbers of sessile polyps (e.g. Duarte et al., 2013; Makabe et al., 2014; Malej et al., 2012). Having been released from strobilating polyps, ephyrae are subjected to starvation as well as predation, jeopardizing their survival and recruitment into the medusa stage (Fu et al., 2014; Ishii et al., 2004). At the same time, they are also subjected to physical forces, such as tidal residual current and wind turbulence, thereby advected from their place of release to remote locations as they grow to medusa stage, forming

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aggregations (Barz et al., 2006; Graham et al., 2001). However, no detailed studies have been conducted on this type of biogeographical advection process of ephyrae and medusae of A. aurita on a relatively small geographical scale, (i.e., less than 10 km) in eutrophic urban coastal waters. The Harima Nada (“nada” means “a small open sea” in Japanese), in the eastern part of the Inland Sea of Japan, is one of the regions where problematic blooms of A. aurita medusae frequently occur, hampering local fisheries and coastal power station operations (Uye and Ueta, 2004). Along the ca. 70-km northern coast of Harima Nada, more than half of which is protected with concrete walls, tetra-pods and riprap (Environmental Agency, 1996), there are the industrialized and densely populated cities such as Himeji, Akashi and Kakogawa (total population: ca. 1.4 million). There are about 50 concrete-walled ports and marinas of various sizes, where many artificial structures such as piers, buoys and breakwaters have been installed. Previous studies have demonstrated that A. aurita polyp colonies attach to these artificial substrates in 9 ports, or all ports investigated (Watanabe, 2011), implying that the majority of ports and marinas along the northern Harima Nada can constitute seeding places for local A. aurita medusa populations. In this study, we periodically sampled ephyrae and medusae of A. aurita in 6 ports and the adjacent northern Harima Nada, and examined their offshore, or southward, dispersion process. Although the M2 tidal current, which generates semi-diurnal reciprocating current in the east-west direction, is dominant in the northern Harima Nada (Hydrographic and Oceanographic Department, Japan Coast Guard, http://www1.kaiho.mlit.go.jp/KANKYO/TIDE/curr_pred/; Yanagi, 1990; Takeoka, 2002), the advection of plankton in the north-south direction is mostly determined by tidal diffusion (Murakami et al., 1985). Hence, we constructed a simple diffusion model to simulate the

spatiotemporal distribution of A. aurita, and assessed which factors are responsible for the actual dispersion process. 2. Materials and methods 2.1. Occurrence of A. aurita in 6 port enclosures The occurrence of A. aurita in the plankton was investigated in 6 ports, i.e. Harima, Mega, Himeji, Murotsu, Sakoshi and Hinase (Fig. 1), biweekly from January to May 2010. A minimum of three oblique tows (distance per haul: 30–50 m) of a Norpac net (45 cm diameter, 180 cm long, 315 μm mesh, flow meter) from 1 m above the bottom to the surface, and vertical profiles of water temperature and salinity with a Compact CTD (ASTD687, JFE Advantech Co., Ltd.) were carried out from piers. In addition, twice-weekly surveys were performed from January to April 2010 in Mega. Zooplankton samples were immediately preserved with neutralized formalin (final conc. 5%). Counting of A. aurita ephyrae and post-ephyra stages (i.e. metephyrae and medusae) and measurement of their body diameters (BD: distance between opposite sensory organs) were carried out under a dissecting microscope. All microscopic analyses were completed within two weeks after preservation. 2.2. Occurrence of A. aurita in offshore waters Four port-to-offshore transects were established in the central part of northern Harima Nada, between Mega and Sakoshi (Fig. 1), to investigate the geographical distribution of A. aurita. Oblique tows (distance per haul: ca. 100 m) of a conical net (60 cm diameter, 1 mm mesh opening, with a flow meter) were carried out from a

Fig. 1. Locations of Harima, Mega, Himeji, Murotsu, Sakoshi and Hinase ports (open squares) and 5 stations (closed circles, D1 is the innermost and D5 is the outermost) along 4 inshore– offshore transects (D1–5 stations are only shown for the transect from Sakoshi) in northern Harima Nada, east Inland Sea of Japan, to investigate the spatiotemporal distribution of planktonic Aurelia aurita.

R. Makabe et al. / Journal of Marine Systems 152 (2015) 75–82

chartered fishing boat at 5 stations (D1: the inshore-most station, D5: the offshore-most station) along each transect (approximate distance from the inshore-most to the offshore-most stations: ca. 9 km) on 28 March, 11 April and 30 May, 2010. A larger net (130 cm diameter, 5 mm mesh opening, with a flow meter, ca. 100 m towing distance) was used to catch medusae, except inside port enclosures (D1 stations), where the larger net was too cumbersome to operate. Vertical profiles of water temperature and salinity were determined at each station using the Compact CTD or a Memory Chlorotech (ACL 220-PDK, JFE Advantech Co., Ltd.). Plankton samples were preserved with neutralized formalin (final conc. 5%), and in the laboratory the numbers of A. aurita and coexisting scyphozoan Chrysaora pacifica were counted and their BD were measured. The density of jellyfish ≤ 2 cm-BD was determined from the 60 cm-diameter net samples and those N 2 cm-BD from the 130 cm-diameter net samples, because of higher densities in respective net samples. The distribution patterns of A. aurita and C. pacifica were compared. First, heterogeneity (variance/mean) in abundance of each species at 20 stations along the 4 transects was calculated on each sampling occasion. Second, their relative abundances, which were determined by dividing their abundance at respective stations by the mean for each sampling occasion, were determined by a test for no correlation after excluding stations where neither of them occurred. 2.3. Application of a physical model In order to assess whether physical processes regulate the transport of A. aurita in the northern Harima Nada, the following simple physical model was tested. First, it was assumed that the northern coast of Harima Nada is straight and sufficiently long, and the source of ephyrae is uniformly distributed along it. Second, physical transport processes were assumed to be uniform parallel to the coast. Then, vertically integrated density of A. aurita, C (x, t), would follow the one-dimensional diffusion equation: 2

∂C ∂ C ¼D 2 ∂t ∂x

ð1Þ

77

and the average age of A. aurita, τa, is calculated as, Z τa ðx; t Þ ¼

t 0

τψðx; t; τ Þdτ

ð5Þ

(see Bolin and Rodhe, 1973 and Takeoka, 1984, for detail). To calculate C (x, t) and τa (x, t), and to compare the results with those observed, values of M and D are necessary. For M, we used an arbitrary value in order to compare the relative distribution patterns in the density to the average age composition. For D, we used two horizontal diffusion coefficients, i.e. 1 × 105 and 5 × 105 (cm2 s−1), from the results of drift-card experiments in northern Harima Nada (Nakata and Hirano, 1990). We calculated C (x, t) and τa (x, t) at t = 60, 90 and 120 days, assuming that the liberation of ephyrae from strobilating polyps started on 1 January 2010. The age of A. aurita was estimated from the increment of BD by assuming that the BD of newly-released ephyrae was 2.0 mm (see Results) and daily BD growth rate was 0.07 day−1 (Båmstedt et al., 2001). 3. Results 3.1. Occurrence of A. aurita in 6 port enclosures The water-column mean temperature at each port varied similarly; it was lowest (8.1–8.5 °C) in January and February, and gradually increased to 16.6–18.8 °C toward 31 May (Fig. 2A). The water-column mean salinity ranged from 30.6 to 32.3, except on 12 April, when it was lower, particularly in Himeji (24.9), because of rain (Fig. 2B). Release of A. aurita ephyrae had started prior to our sampling and had ceased by the end of our survey. Their abundance varied temporally, showing one to three peaks in the several ports, although timing of the peaks differed among ports (Fig. 3). Mean (±SD) ephyrae density ranged over the survey period, from 0.5 ± 0.5 ind. m−3 in Harima to 2.4 ± 2.5 ind. m−3 in Murotsu. During the observation, A. aurita caught in these ports usually comprised nearly 100% of ephyrae in Mega, Murotsu, Sakoshi and Hinase, with overall mean BD of 2.0 ± 0.3, 2.4 ± 0.6, 1.9 ± 0.2 and 2.3 ± 0.6 mm, respectively. The occurrence of metephyrae (BD range: 5–10 mm) and medusae (BD: N 10 mm) was

where x is horizontal distance from the shore (i.e. x = 0), t is time and D is an apparent diffusion coefficient that includes effects of turbulent diffusion and current shear. If a given number of ephyrae (M, per unit coastal length) were to be instantaneously released at x = 0, the solution under the condition where C = 0 at x → ∞ would be,   M x2 C ðx; t Þ ¼ pffiffiffiffiffiffiffiffi exp − 4Dt πDt

ð2Þ

(e.g. Csanady, 1980). In the case where ephyrae per unit coastal length and unit time, M, are continuously released after t = 0, the solution C (x, t) is obtained by the superposition of the solution of instantaneous release during t* = 0 to t as, Z C ðx; t Þ ¼

t 0

C ðx; t−t  Þdt 

ð3Þ

where t* is the time of release. In Eq. (3), C (x, t − t*) shows the distribution of A. aurita aged t − t* (age, τ = t − t*); therefore, the age distribution function, ψ (x, t, τ), is calculated as,

ψðx; t; τ Þ ¼

C ðx; τÞ C ðx; t Þ

ð4Þ

Fig. 2. Temporal variations of vertically integrated average temperature (A) and salinity (B) in 6 ports in northern Harima Nada.

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Fig. 3. Temporal variations of abundance (filled circles) and composition of ephyrae (open squares) of Aurelia aurita in 6 ports located in northern Harima Nada. Vertical bars: standard deviations.

occasional, but more prominent in Harima and Himeji in late March and April. 3.2. Occurrence of A. aurita in Mega During the twice-weekly survey in Mega, the surface water temperature ranged from 7.7 to 14.6 °C, but with repeated short-term oscillations (Fig. 4A). The surface salinity ranged from 28.5 to 32.1, except on 13 April when it was 15.4 (Fig. 4A). Except for a single metephyra in the plankton sample taken on 26 March, A. aurita caught in Mega consisted entirely of ephyrae, which were present at 1.6 ind. m − 3 already on the first sampling date (6 January), and varied without regularity until the end of the survey (30 April). There were 4 marked peaks on 22 January, 26 February, 16 March and 20 April (Fig. 4B). Overall mean BD of ephyrae was 1.8 ± 0.2 mm (Fig. 4C).

Fig. 4. Temporal variations of temperature (filled circles) and salinity (open squares) at 0.5 m depth (A), and of abundance (B) and body diameter (filled circles) and composition of ephyrae (open squares) (C) of Aurelia aurita in Mega. Vertical bars: standard deviations.

medusae usually dominated and their mean BD increased from 11.2 ± 4.1 mm on 28 March to 44.5 ± 17.2 mm on 25 April (Fig. 5C). The heterogeneity (variance/mean) of abundance at 20 stations was 1.73, 0.70 and 0.37 on 28 March, 11 April and 25 April, respectively, showing that the spatial distribution of A. aurita became gradually more homogeneous with time. C. pacifica, which had grown much larger than A. aurita by 28 March, did not occur at D1 stations but were present at D2–D5 stations throughout the survey period. Their overall mean densities ranged from 0.011 ± 0.015 ind. m−3 on 28 March to 0.005 ± 0.006 ind. m−3 on 25 April, and were 1–2 orders of magnitude lower than those of A. aurita (Figs. 5D, 6). Heterogeneity of their occurrence at 20 stations was 0.02, 0.01 and 0.01 on 28 March, 11 April and 25 April, respectively, denoting much more homogenous distribution as compared to A. aurita. There was a significantly negative correlation (test for no correlation, n = 52, p b 0.01) between relative abundances of A. aurita and C. pacifica. 3.4. Dispersion-modeled distribution of A. aurita versus actual distribution

3.3. Distribution of A. aurita and Chrysaora pacifica in offshore Harima Nada Along the 4 transects, there was a slight decrease in temperature and increase in salinity from inshore to offshore stations (Fig. 5A, B). The overall mean temperature for transect stations increased from 10.1 ± 0.2 °C on 28 March to 12.0 ± 0.4 °C on 25 April. The mean salinity decreased from 32.2 ± 0.2 on 28 March to 31.5 ± 0.2 on 25 April. Although A. aurita spread over the entire survey area, their main distribution was confined to the most inshore D1 and D2 stations, ≤ ca. 2 km from shore, where the mean density was highest (0.53 ± 0.96 ind. m− 3) on 28 March and then dropped later (Figs. 5C, 6). At D1 stations, ephyrae and metephyrae dominated, and their mean BD was usually smaller than those at D2–D5 stations, ranging from 5.4 mm on 25 April to 7.0 ± 2.2 mm on 28 March., For D2–D5 stations,

First, we reconstructed the geographical distribution of vertically integrated density and average age of A. aurita along the inshore-offshore transect (Fig. 7A, B). Second, we projected the results predicted from the dispersion model using two diffusion coefficients, i.e. 1 × 105 and 5 × 105 cm2 s− 1 (Fig. 7C–F). The modeled distribution of relative density differed widely from the observed pattern (Fig. 7A, C, E). Actual A. aurita density abruptly declined around 3 km from the shore (i.e. between D2 and D3 stations), with the largest inshore-offshore contrast of 1 inshore to 1/74 offshore (on March 28), while the density predicted by the model gradually decreased offshore, with greatest inshore-offshore difference of only ca. 1 inshore to 1/3 offshore (at t = 90 days). For the distribution in average age, the physical model predicted a gradual increase seaward and with time (Fig. 7D, F), which was identical to the observed pattern (Fig. 7B).

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Fig. 5. Spatial variations of vertically integrated average temperature (A), salinity (B), abundance (columns) and body diameter (circles, squares and triangles) of Aurelia aurita (C) and Chrysaora pacifica (D) along the inshore–offshore transect in northern Harima Nada on 28 March, 11 April and 25 April, 2010. Vertical bars: standard deviation.

4. Discussion As had already been demonstrated in temperate coastal waters in the northern hemisphere (e.g. Lucas, 2001; Makabe et al., 2014; Miyake et al., 1997; Yasuda, 1988), A. aurita in the northern Harima Nada strobilated and liberated ephyrae into the water during the coldest seasons of the year. Twice-weekly samplings in Mega detailed the temporal variation in the abundance of ephyrae, which showed at least 4 prominent peaks, each coinciding with sea surface temperature increases of ca. 3 °C due to sunny, warm weather (Fig. 4). Laboratory experiments have demonstrated shorter strobilation duration at higher temperatures (Ishii and Katsukoshi, 2010; Liu et al., 2009; Makabe et al., 2014), suggesting that the observed thermal upsurges might induce liberation of ephyrae to form peaks. In all 6 ports, A. aurita populations were almost exclusively comprised of ephyrae, consistent with previous studies in Tokyo Bay (Toyokawa et al., 2000), Mikawa Bay (Toyokawa et al., 2011) and Hiroshima Bay (Makabe et al., 2014), where the samplings were confined to port enclosures. Thus, these 6 ports constitute seeding sources of A. aurita by harboring polyp populations in the enclosures. This finding is consistent with previous findings of polyp colonies in ports along the northern coast of Harima Nada (Watanabe, 2011), which in turn strongly supports our view that port enclosures along the northern coast of Harima Nada constitute a polyp shelter. On the other hand, post-ephyra stages were also prominent at all stations outside the ports, indicating that most newly-released ephyrae are rapidly transported from port enclosures to adjoining open waters. According

to calculations by Takeoka (1989), the average water exchange rate generated by M2 tide for Mega (area: 2.1 × 104 m2, mean depth: 2.5 m), the smallest of the 6 ports, is 0.09 d−1 (or ca. 10 days residence time). For Himeji (area: 160.5 × 104 m2, mean depth: 8.2 m), the largest port sampled, the exchange rate is 0.005 d−1 (or ca. 200 days residence time). Thus, the water exchange generated by M2 tide may be the major vehicle that transports A. aurita ephyrae to outside any port enclosure (Fig. 8). Once A. aurita are transported to the open northern Harima Nada, they are also subjected to horizontal tidal mixing, and may be dispersed further offshore. The physical dispersion model predicted both gradual decrease in their density and gradual increase in their age seaward (Fig. 7 C, D). However, the model did not correctly simulate the observed pattern of their density, which showed a remarkable gap between D2 and D3 stations (Fig. 7A). This discontinuity was not attributable to any notable change in physio-chemical environmental factors (Fig. 5). This, however, could be explained by significant predation of A. aurita at offshore stations by C. pacifica. In contrast to inshore origin of A. aurita, the main habitat of C. pacifica tends to be in the offshore Japanese coastal waters (Kinoshita et al., 2006; Yasuda, 2003). In the northern Harima Nada, ephyrae of C. pacifica were not found in the plankton samples collected in the port enclosures, whereas some 1200 A. aurita ephyrae were caught. Hence, we speculate that the habitat of C. pacifica polyps may be on hard benthic substrates, such as stones and bivalve shells in offshore areas, as was found in Sagami Bay, central Japan (Toyokawa et al., 2011). As C. pacifica polyps strobilate and release ephyrae slightly earlier

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Fig. 6. Occurrence of Aurelia aurita (right panels) and Chrysaora pacifica (left panels) in northern Harima Nada on 28 March, 11 April and 25 April, 2010.

in the cold season than A. aurita (Kakinuma, 1967; Kinoshita et al., 2006; Thein et al., 2013), C. pacifica had grown much larger than A. aurita by March, when our sampling started. Extremely strong endurance under prolonged starvation (Fu et al., 2014; Hamner and Jenssen, 1974) implies that predation loss may be a significant cause for the mortality of an A. aurita population during the course of development from the ephyra to medusa. Although interspecific predation among jellyfish is widely known (e.g. Hansson, 1997; Hosia and Titelman, 2010; Strand and Hamner, 1988; Tilves et al., 2013), information on the prey-predator relationship between A. aurita and C. pacifica is limited. However, A. aurita medusae are commonly given as food to C. pacifica in many Japanese commercial aquaria (e.g. K. Okuizumi of Kamo Aquarium, Tsuruoka, personal comm.). Sato et al. (1996) observed in the laboratory that one C. pacifica individual of BD = 9.0 cm was capable of consuming daily two A. aurita (BDs = 8.5 and 9.0 cm), even when the body mass of the prey was nearly double the predator's. We determined the predation and clearance rate of a C. pacifica medusa (BD: ca. 6 cm) on A. aurita ephyrae (initial concentration: 100 ephyrae l−1) using a 10-l volume kreisel at 16 °C. In this case, the predation rate and clearance rate was 108 ephyrae medusa−1 h−1 and 1.85 l medusa−1 h−1, respectively (Takao and Uye, unpublished). Thus, C. pacifica could act as major predators of offshore-spreading A. aurita, and possibly distort their model-predicted distribution (Fig. 8). Such a predation impact may occur in most Japanese coastal waters, where seaward A. aurita and shoreward C. pacifica are sympatric (Morandini and Marques, 2010). Similar intraguild interactions may

also take place between A. aurita and two predatory Cyanea species (i.e. C. capillata and C. lamarckii) in the Skagerrak and Kattegatt Seas, where the A. aurita originate from inshore areas such as fiords and the Cyanea species are primarily transported from the North Sea (Båmstedt et al., 1994; Gröndahl, 1988; Hosia et al., 2014). Another similar interaction occurs between A. aurita and opportunistic-feeding Pelagia noctiluca in the northern Adriatic, where ephyrae of the former originate in port enclosures, and the latter spend their holoplanktonic life in offshore waters (Kogovšek et al., 2010; Malej et al, 2012). Sympatric occurrence of Aurelia spp. and Chrysaora sp. in the northern Gulf of Mexico (Graham, 2001; Robinson and Graham, 2013) may also imply similar prey-predator interactions between them, but none of the studies to date have been conclusive. According to our previous report (Uye and Ueta, 2004) and observations by local fishers (e.g. H. Kobayashi, Boze Fisheries Cooperative, personal comm.), A. aurita used to bloom extensively over the entire northern Harima Nada in the 1980s and 1990s, when C. pacifica were observed in low numbers. However, C. pacifica began to bloom prominently after the turn of this century (Uye and Ueta, 2004; H. Kobayashi, Boze Fisheries Cooperative, personal comm.). The recent blooms of C. pacifica have impacted the various net fisheries extensively, such that fishermen of Boze Fisheries Cooperative, Himeji (see Fig. 1, Boze Island), have performed extensive jellyfish slicing and removal operations, employing ca. 90 fishing vessels per day. Such removal vessels have operated for a total of 27 working days each year since 2010, clearing thousands of tons of jellyfish, the majority of which were C. pacifica (N. Uenishi, Boze

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Fig. 7. Spatial variations of vertically integrated abundance (left panels) and age (right panels) of Aurelia aurita along the inshore–offshore transect in northern Harima Nada. Observed patterns (A, B) and predicted patterns from physical models with dispersion coefficients of 105 cm2 s−1 (C, D) and 5 × 105 cm2 s−1 (E, F).

Fisheries Cooperative, personal comm.). This species has continued to bloom every year (including the current year 2015). As a similar increasing trend of C. pacifica population arises in other parts of the Inland Sea of Japan (Ueda, 2007; Uye and Ueta, 2004), it is important to investigate the predatory consequence of recently proliferated C. pacifica on A. aurita population and blooms. It is also necessary to study ecological roles of

C. pacifica, which may play important roles as a predator for various fish and zooplankton species, as reported for Chrysaora spp. in other waters (Flynn and Gibbons, 2007; Purcell, 1992; Zavolokin et al., 2008). 5. Conclusions We have demonstrated that both physical and biological factors are important to determining the spatiotemporal distribution of A. aurita across ca. 9-km transects in northern Harima Nada. Inshore port enclosures were where ephyrae were released, and developed medusae were only found in offshore waters. Physical factors were primarily responsible for exporting ephyrae from inside the port enclosures to outside, and then transporting them, in the course of development to the medusa stage, further offshore. However, the actual distribution of A. aurita inshore and offshore differed from the physically-simulated patterns, because C. pacifica medusae, which had already prevailed in offshore waters, might have exerted significant predation pressure on A. aurita. Similar intra-jellyfish interactions between Aurelia spp. (which are primarily of inshore origin), and predatory genera such as Chrysaora, Cyanea and Pelagia (which are mostly of offshore origin), may occur in many coastal waters. Acknowledgments

Fig. 8. Schematic diagram of the spatiotemporal dispersion of planktonic Aurelia aurita in northern Harima Nada controlled by physical and biological factors. Ephyrae released from strobilating polyps in port enclosures are dispersed offshore by physical processes. However, post-ephyra stages are subjected to predation by Chrysaora pacifica medusae prevailing at offshore (i.e. D2 to D5) stations. D1–D5: approximate locations of sampling stations (also see Fig. 1).

We thank T. Kurihara, L. Dong, H. Kobayashi and Boze Fisheries Cooperatives for their assistance during our field surveys. Our gratitude is also extended to K. Yamashita and M. Takao for providing unpublished data and Naomi Yoder for editing our English. This study was partially supported by a grant from the Agriculture, Forestry and Fisheries Research Council, Japan (Project name: STOPJELLY).

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