- Email: [email protected]
Seasonal and interannual variation in the density of visible Apostichopus japonicus (Japanese sea cucumber) in relation to sea water temperature
Estuarine, Coastal and Shelf Science 229 (2019) 106384
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Seasonal and interannual variation in the density of visible Apostichopus japonicus (Japanese sea cucumber) in relation to sea water temperature
T
Kenji Minamia,∗,1, Reiji Masudaa, Kohji Takahashia, Hideki Sawadaa, Hokuto Shirakawab, Yoh Yamashitaa a b
Field Science Education and Research Center, Kyoto University, Nagahama, Maizuru, Kyoto, 625-0086, Japan Field Science Center for Northern Biosphere, Hokkiado University, Hakodate, Hokkaido, 040-0051, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Biomass Resource management Resource surveys Japanese sea cucumber Water temperature
Apostichopus japonicus (Japanese sea cucumber) is of ecological and economic importance in the coastal waters of Japan. To assess the apparent abundance of A. japonicus, density data of visible A. japonicus are required; however, the activity of this species on the sea floor changes with variations in sea water temperature. For example, at high sea water temperatures, A. japonicus takes shelter in the gaps of rocks or oyster shells. This change in its visibility on the sea floor makes it difficult to determine the apparent abundance of this species. In the present study, we aimed to clarify the optimal survey timing to assess the apparent abundance of A. japonicus based on the relationship between the density of visible A. japonicus and sea water temperature. Between 2010 and 2013, we evaluated how the density (ind. 100 m−2) of visible A. japonicus changes with sea water temperature in an area preferred by these organisms, Maizuru Bay, Kyoto, Japan, every 2 weeks. Seasonal changes in the density were consistent with seasonal variations in sea water temperature. Density increased when sea water temperature decreased and was at a maximum at minimum sea water temperatures. In addition, the density tended to change significantly over a short period. In some cases, the density after the lowest sea water temperature in March 2011 declined by half from 65 to 27 in just 2 weeks. Owing to considerable variations in the density of visible A. japonicus, we believe it is important to establish the appropriate survey timing to quantify the apparent abundance of this species, with our data suggesting that surveys should be performed during the season with the lowest sea water temperatures. Furthermore, at the lowest sea water temperatures in 2010, 2011, 2012, and 2013, the maximum densities were 99.0 (9.1 °C), 65.0 (9.7 °C), 41.3 (9.8 °C), and 8.7 (8.9 °C), respectively. Over 4 years, the density decreased to approximately 10% of that in the year with the peak density. Considering this decrease, it is suggested that A. japonicus in Maizuru Bay is overfished. Therefore, it is possible that the density of visible A. japonicus at the lowest sea water temperatures provides useful information for assessing the apparent abundance of this species.
1. Introduction The Japanese sea cucumber Apostichopus japonicus is distributed along the coastal sea area of northeastern Asia and is the dominant holothuroid species from Hokkaido to Kagoshima in Japan (Choe, 1963; Takahashi, 2003). This species is a deposit feeder that consumes diatoms, detritus, and bacteria mixed with sediments on the seabed, and assimilates about 50% of the organic carbon and nitrogen in the sediment (Tanaka, 1958; Choe, 1963). Therefore, A. japonicus plays an important ecological role as a consumer, and is involved in improving
the sea floor sediment in coastal waters. In addition, A. japonicus is a high-value fishery product in Japan. For example, in 2010, A. japonicus products from the waters of Hokkaido, Japan, were traded for approximately 3400 yen per kilogram (fresh weight - Fisheries Agency: http://www.market.jafic.or.jp/suisan/, Accessed 4 Apr 2018). Furthermore, the processed products, such as dried A. japonicus (75,000 yen per dry weight in kilograms), are high value commodities (Commercial dealer: http://www.namakoya.com/, Accessed 12 March 2019). However, a recent increase in demand for sea cucumbers worldwide has led to increased fishing pressure, with a decline in
Abbreviations:Region, Japan, Kyoto, Maizuru Bay (35 29.3833 N, 135 22.1167 E) ∗ Corresponding author. Estuary Research Center, Shimane University, Matsue, Shimane, 690-8504, Japan. E-mail address: [email protected] (K. Minami). 1 Present Address: Estuary Research Center, Shimane University, Matsue, Shimane, 690–8504, Japan. https://doi.org/10.1016/j.ecss.2019.106384 Received 30 July 2018; Received in revised form 12 August 2019; Accepted 16 September 2019 Available online 19 September 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
contour line at 2.7 m (depth at first survey, 2 February 2010, Tide 128 cm) and depth and location remained the same for each subsequent survey. The transect was located on the silt bottom areas close to the location of the oyster shell reefs (approximately 1–5 m from the oyster shell reef). The number of A. japonicus individuals in the transect line was counted. Only the A. japonicus visible on the surface of the seafloor, including partially visible individuals were counted. We did not turn over rocks or oyster shells and look into gaps of rocks or oyster shells. A. japonicus individuals completely hidden in rock crevices or oyster shells were not counted. The density (ind./100 m2) of visible A. japonicus was calculated from the number of counted individuals. The sea water temperature of the bottom layer was measured using a calibrated temperature sensor from a diving computer at the survey start time (TUSA IQ-850, Tabata Co. Ltd, Tokyo Japan). Between February 2010 and September 2013, the survey was conducted every two weeks. The density (response variable) was compared with sea water temperature, tidal depth, rate of tidal change and survey time (explanatory variable) between years by fitting a generalized linear model (GLM) using a gamma family with a model link function equal to log in R version 3.4.1 (R Core Team, 2017). The tidal depth, tidal change, and time are environmental factors that may affect the density, other than sea water temperature in areas preferred by A. japonicus (Choe, 1963; Yamaguchi et al., 2016). The survey time was the survey start time. The tidal depth was the depth corrected by tide at the survey start time. The tidal change was the amount of change in the tide depth over the 1 h period preceding the start time. Tidal data is that for the Maizuru bay station (Japan Meteorological Agency: http://www.data.jma.go.jp/kaiyou/db/ tide/suisan/, Accessed 12 March 2019). Because each survey took only 20–30 min, explanatory variables were constant throughout the survey and we used a single value (the initial conditions) for each survey as explanatory variables. The four explanatory variables were independent of each other, as demonstrated by the index variance inflation factor (VIF) for examining the multicollinearity; VIF values for this group of variables were all less than 10. The information-theoretic approach was used in model selection (Burnham and Anderson, 2002). This approach allows the “best” model to be selected and also ranks the remaining models. Akaike's Information Criterion (AIC) value was calculated for all models. Delta AIC (ΔAIC) was calculated as the difference in AIC between all models and the best model in the set. Models with AIC differences of less than two have substantial support (Burnham and Anderson, 2002), and individual models were selected based on AIC. The best-fit model was selected as the minimum AIC model. The body length (L) and width (B) of the ventral surface of A. japonicus were measured underwater using a ruler when the sea water temperature at the lowest point in 2010, 2011, and 2012. We were not able to calculate the standard body length in 2013, as the sampling number was low and their shapes were bent. L was the mid-line from the tip to the end of the body, and B was the central width of the body, excluding the papillae and parapodia. Individuals that were straight were selected, because measurements of A. japonicus with a bent body produce large errors when calculating the standard body length (Le). Since this survey was conducted in silt bottom areas of the boundary area, with few structures and relatively flat sea bottoms, the shape over 80% of A. japonicus in our survey area was almost straight shape, regardless of the large and small sizes of A. japonicus. Standard body lengths were calculated using L and B, as follows (Yamana et al., 2011):
resources being reported in various parts of Japan (Purcell et al., 2010). Owing to the ecological and economic contributions of sea cucumbers and their declining abundance, it is important for fisheries scientists and environmental managers to accurately quantify the apparent abundance of A. japonicus to ensure their sustainability in coastal areas. Therefore, a quantitative estimation of A. japonicus density is required to provide an index of apparent abundance. Various resource surveys have been conducted in Japan, such as that calculated from CPUE (catch per dredge-net) against cumulative catch (Matsumiya, 1984), and from the catch against dredged area (Sano et al., 2011). However, the life history of A. japonicus, which is closely associated with sea water temperature, makes it difficult to estimate population density in dredge-based surveys. Specifically, sea water temperature regulates their behavioral patterns through the year (Arakawa, 1990; Kashio et al., 2016). Aestivation is a special type of dormancy that allows A. japonicus to survive during periods of high sea water temperatures (Yuan et al., 2007). During periods of high sea water temperature, A. japonicus take shelter in gaps of rocks and oyster shells (Yamana et al., 2008; Nakahara et al., 2018). When the sea water temperature begins to decrease, A. japonicus becomes more active. Therefore, the density of visible A. japonicus on the sea floor fluctuates considerably during the year. Seasonal variations in their visibility make it difficult to determine the apparent abundance of A. japonicus if surveys are conducted at different times. Thus, it is important to conduct surveys at times when A. japonicus are most visible to quantify their abundance accurately. However, only a limited number of studies have examined seasonal change in the density of visible A. japonicus in relation to sea water temperature. Therefore, the optimal timing of surveys to assess the apparent abundance of A. japonicus has not been clearly documented. In the present study, we aimed to understand seasonal changes in the density of visible A. japonicus and their association with sea water temperature and other possible environmental parameters. Between 2010 and 2013, we documented the density and seawater temperature in Maizuru Bay, Kyoto, Japan, every 2 weeks. We used this information to identify the optimal timing of surveys to assess the apparent abundance of A. japonicus. 2. Materials and methods The survey was conducted in the coastal waters of Maizuru Bay, Japan (Fig. 1). Maizuru Bay is located in the temperate zone in the Sea of Japan and is a semi-closed bay. Average salinity in our survey area was 31.9 ± 0.8 (SD) in 2011, and salinity remained stable through the years of our study (2010–2013), during which no large salinity changes were reported. It is an important fishing ground for A. japonicus. The fishing season is from November to March. Areas where the sea floor is less than 2 m deep in the survey area are largely covered by oyster shells, except for small areas with an exposed silt bottom and areas along quay walls. The deeper areas of the survey area were composed of muddy silt with scattered small rocks. A. japonicus were captured using a beam trawl mainly in Maizuru Bay deeper than the oyster shell reefs. In addition, small structures, such as an artificial fish reefs (width 1 m, length 1 m, height 1 m), are scattered on the sea bottom in the survey areas located 10–30 m distant from the coastline. Therefore, A. japonicus could not be fished using a beam trawl in the survey area. A. japonicus has three ventral color types (red, green, and black). In Maizuru Bay, the ventral color of this species is mainly green. A. japonicus prefers to inhabit the boundary area of the silt bottom and oyster shell reef, which contains large quantities of sediment and provides refuge (Hamano et al., 1989; Goshima et al., 1994). In the survey area, several such boundary areas were present. In these boundary areas, direct observation using SCUBA was conducted during the daytime to estimate visible A. japonicus density. To manage quantitative data, an area of 300 m2 (150 × 2 m = 300 m2) was set as a belt transect line in the survey area (Fig. 1). The belt transect followed the depth
1
Le = 5.30 + 2.01 × (L × B )
2
(1)
3. Results Fig. 2 shows visible A. japonicus density versus sea water temperature in Maizuru Bay. The maximum density (2010: 99.0 ind. 100 m−2, 2011: 65.0 ind. 100 m−2, 2012: 41.3 ind. 100 m−2, 2013: 8.7 ind. 100 m−2) was observed during February and March (Table 1). 2
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Fig. 1. Study area. Solid line indicates the survey belt transect line.
The average sea water temperature on days when A. japonicus was observed again on the sea floor was 15.0 ± 2.7 °C over the 4 years of the survey. The visible A. japonicus density increased with decreasing sea water temperature. Density was compared with sea water temperature, tidal depth, tidal change, and survey time between years by GLM. A best-fit model was selected from a set of models (Table 2). The model with only sea water temperature was selected as the best model in all survey years. Fig. 3 shows the relationship between the visible A. japonicus density and sea water temperature estimated by GLM (Table 3). Between 2010 and 2013, a consistent trend was observed for visible A. japonicus density with increasing/decreasing sea water temperature. After 2010, the maximum density of A. japonicus in Maizuru Bay decreased each year (Fig. 2). The density in 2013 (8.7 ind. 100 m−2 ± 3.9) was less than 1/10 of that observed in 2010 (99.0 ind. 100 m−2 ± 50.5). During the season with maximum density (from February to March), the average standard body length of A. japonicus in 2010, 2011, and 2012 was 16.0 ± 3.2 cm (11.4–23.3 cm), 18.9 ± 4.3 cm
Thereafter, the density rapidly decreased from the maximum density. At the end of June, no A. japonicus individuals were found on the sea floor. During this period, A. japonicus takes shelter in the gaps of rocks and oyster shells. From the middle of December, we observed A. japonicus on the sea floor (2010: 0.3 ind. 100 m−2, 2011: 1.0 ind. 100 m−2, 2012: 0.3 ind. 100 m−2, 2013: no data), and the density then increased rapidly until February. On the other hand, when A. japonicus density was at a maximum (February and March), the sea water temperature was 9.4 °C ± 0.4 (SD) (2010: 9.1 °C, 2011: 9.7 °C, 2012: 9.8 °C, 2013: 8.9 °C), after which the sea temperature increased slowly. In August and September, the sea water temperature was highest (2010: 31.0 °C, 2011: 29.5 °C, 2012: 30.9 °C, 2013: 31.6 °C); thereafter, it decreased from the highest sea water temperature (Fig. 2). During February and March, the sea water temperature became lowest. In this period, A. japonicus density was observed as the highest. A. japonicus density decreased with increasing sea water temperature. In particular, the average sea water temperature when the density became zero during the four survey years was 24.7 ± 3.2 °C (Table 1).
Fig. 2. Density of visible Apostichopus japonicus versus sea water temperature in Maizuru Bay, Japan, between 2010 and 2013. Solid line indicates the density of A. japonicus. Dotted line indicates the sea water temperature. Closed squares and circles indicate the observed values. 3
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Maizuru Bay, individuals taking refuge in oyster shells and rock crevices were observed again on the sea floor when the sea water temperature decreased in the fall and was < 15.0 °C ± 2.7 °C. The relationship between the visible A. japonicus density and sea water temperature was consistent with that reported for the seasonal activity of A. japonicus in a previous study. Therefore, visible A. japonicus density changes with changing sea water temperature. Furthermore, since the relationship between density and sea water temperature was strong, it is considered that the model of density could be expressed with only sea water temperature. In addition, during aestivation, the digestive ability of A. japonicus is low, with limited feeding and weight loss (Choe, 1963). Therefore, after aestivation A. japonicus needs to feed to recover the lost weight. For recovery and growth, the digestive ability of A. japonicus increases with decreasing sea water temperature and is accompanied by an increase in food consumption (Choe, 1963). Thus, as sea water temperatures decrease, the behavioral activity of A. japonicus after aestivation is activated, with higher numbers of A. japonicus emerging from crevices to the sea floor to seek food. Conversely, as the sea water temperature increases, the digestive ability and behavioral activity of A. Japonicus decreases leading up to aestivation (Choe, 1963). Particularly, after spring from April to June, which is the breeding season in Maizuru Bay, the density of A. japonicus individuals decreases as more of them take refuge in crevices. Therefore, from these differences in the activity of A. Japonicus with the change in sea water temperature, it is considered that the visible A. japonicus density on the sea floor is greatest when sea water temperature is the lowest. Visible A. japonicus density also tended to change significantly over short periods of time (Fig. 2). For example, the density (ind. 100 m−2) found after the lowest sea water temperature in March 2011 dropped by half from 65 to 27 in only 2 weeks. Furthermore, the density before the lowest sea water temperature in January 2012 doubled from 57 to 124 in only 2 weeks. Owing to this rapid change in detectability on the sea bottom, there is a risk that the apparent abundance of A. japonicus is underestimated in surveys. Therefore, an appropriate time for surveys must be selected to assess the apparent abundance of A. japonicus. The visible A. japonicus density increased when the sea water temperature decreased. The density was highest when the sea water temperature was lowest. This trend was observed every year for approximately 4 years (Fig. 3). The visible A. japonicus density at the lowest sea water temperature in a single year could be used to assess the apparent abundance of A. japonicus. Therefore, to assess the apparent abundance, surveys that monitor the density on the sea floor should be conducted when the sea water temperature is low. In addition, the resource survey of A. japonicus is currently conducted using dredge-nets in Japan (Matsumiya, 1984; Sano et al., 2011). The obtained density data by dredge-net is the number of A. japonicus individuals per unit area of the surface of the seafloor. It is similar to the visible A. japonicus density in which the density on the surface of the sea floor is calculated. However, the resource survey did not consider the seasonal changes of A. japonicus on the surface of the sea floor with accompanying sea water temperature change, as obtained in the present study. Therefore, depending on the timing of the survey, the resource abundance may be underestimated. In the future, it would be necessary to consider the seasonal changes of A. japonicus on the surface of the seafloor owing to sea water temperature, in such resource surveys. However, in cold zones, compared with temperate zones, such as Maizuru Bay, where the minimum sea water temperature (8.1 °C) is lower than that documented in this study, the influence of low sea water temperature on the density should be examined further. Moreover, the surveys were conducted during the daytime in this study. However, A. japonicus has been found to move actively at night (Yamaguchi et al., 2016). It might be that the density of visible A. japonicus individuals at night is closer to the actual resource than that in the day. Therefore, to estimate the resource condition of A. japonicus, it would also be necessary to clarify the survey timing considering diurnal activity. Note that this study was not designed to be a random survey that
Table 1 Trend in the density of visible Apostichopus japonicus and sea water temperature in each season. Density of visible individuals (ind. 100m−2) Feb–Mar.
Mar–Jun.
Jun–Dec.
Dec–Feb.a
Year
(Maximum)b
(Decrease)
(Completely hidden)
(Increase)
2010 2011 2012 2013
99.0 65.0 41.3 8.7
99.0–3.0 65.0–1.3 19.0–0.3 2.7–0.0
None None None None
0.3–51.0 1.0–41.3 0.3–8.7 no data
Feb–Mar.
Mar–Jun.
Jun–Dec.
Dec–Feb.a
Year
(Avg 9.4 ± SD 0.4)c
(Increase)
(Avg 24.7 ± SD 3.2)d
(Decrease)
2010 2011 2012 2013
9.1 9.7 9.8 8.9
9.1–23.8 9.7–22.0 10.6–19.2 9.8–24.8
23.8 29.5 23.1 22.5
13.6–9.0 18.1–9.6 13.2–8.1 no data
Sea water temperature (°C)
a
February of the following year. Maximum density of Apostichopus japonicus. c Sea water temperature when the density of Apostichopus japonicus was maximum. d Sea water temperature when the density of Apostichopus japonicus was zero. b
Table 2 Highest ranked generalized linear models in each survey years using AIC-based model selection for the density of visible Apostichopus japonicus. The table also shows sea water temperature (TEMP), tidal depth (DEPTH), tidal change (CHANGE), survey time (TIME) and AIC differences (ΔAIC). Year
Model
2010
TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP
2011
2012
2013
+ CHANGE + TIME + TIME + CHANGE + DEPTH + CHANGE + DEPTH + TIME
AIC
ΔAIC
48.8 49.9 50.2 44.8 45.1 45.2 51.8 52.7 52.9 29.9 31.0 31.1
0.0 1.1 1.4 0.0 0.3 0.4 0.0 0.9 1.1 0.0 1.1 1.2
(11.4–26.8 cm), and 18.8 ± 3.8 cm (12.2–27.8 cm), respectively (Fig. 4). In 2010, the body length primarily ranged from 10 to 15 cm. In comparison, in 2011 and 2012, the body length primarily ranged from 15 to 20 cm. The percentage of individuals with body lengths from 10 to 15 cm decreased across years; namely, for 2010, 2011, and 2012, the percentage of individuals with 10–15 cm body length was 44%, 22%, and 13%, respectively.
4. Discussion Seasonal variation in visible A. japonicus density was consistent with seasonal variation in sea water temperature (Fig. 2). The sea water temperature was 24.7 °C ± 3.2 °C when A. japonicus individuals were taking shelter in rock crevices or oyster shells. This result was consistent with the sea water temperature (24.5–25.5 °C) during the period when A. japonicus shifts to aestivation (Choe, 1963; Yang et al., 2005). When the sea water temperature begins to decrease during fall, A. japonicus that took refuge in oyster shells and rocks emerge onto the sea floor (Choe, 1963). A previous study (Choe, 1963) also reported that the sea water temperature during the activity period was < 17.5–19 °C. In 4
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Fig. 3. Relationships between the density of visible Apostichopus japonicus and sea water temperature in (a) 2010, (b) 2011, (c) 2012, and (d) 2013. Grey circles indicate the observed values. Solid line indicates the regression curve estimated by a generalized linear model (GLM). Dashed line indicates the confidence interval.
standard body length 18 cm) in Maizuru Bay to conserve this resource. When small individuals are caught using fishing gear, they are released into the sea. However, despite efforts to avoid catching small A. japonicus, between 2010 and 2012, the frequency of individuals with a small standard length (10–15 cm) decreased appreciably (Fig. 4). It is possible that large individuals are overfished and reproduction is decreasing and therefore, the A. japonicus population in Maizuru Bay is decreasing. From 2010 (157 t) to 2013 (57 t), the catch per year in Maizuru Bay decreased by about 100 t (Fisheries Agency, 2015). Therefore, we suggested that the number of A. japonicus individuals in Maizuru Bay was decreasing possibly due to overfishing. By monitoring visible A. japonicus density when sea water temperature is at its lowest, any decrease or increase in density may be objectively estimated. In addition, it might be possible that other information, such as standard body length could be used to understand the variations in A. japonicus density. Visible A. japonicus density at the lowest sea water temperature provided useful information for assessing the apparent abundance of this species.
Table 3 Results of the generalized linear model (GLM) comparing the density of visible Apostichopus japonicus and sea water temperature (TEMP). Year
Variable
Estimate
Standard error
t value
Pr(> |t|)
2010
Intercept TEMP Intercept TEMP Intercept TEMP Intercept TEMP
10.156 −0.491 8.718 −0.465 7.948 −0.432 4.675 −0.271
0.975 0.046 0.743 0.037 0.920 0.050 0.875 0.044
10.420 −10.600 11.740 −12.620 8.639 −8.672 5.345 −6.112
1.54 × 10−8 1.22 × 10−8 2.00 × 10−10 5.52 × 10−11 2.02 × 10−7 1.92 × 10−7 8.17 × 10−5 1.99 × 10−5
2011 2012 2013
*** *** *** *** *** *** *** ***
***p < 0.001.
could quantify the A. japonicus population in this region. The measurements of density in this study were focused on a specific area preferred by A. japonicus, and A. japonicus that were present but completely hidden in rock crevices or oyster shells were not counted. Therefore, the measured density cannot be used to reflect the overall density in Maizuru Bay. However, multi-year comparable indicators in a habitat preferred by A. japonicus could provide a qualitative understanding of the abundance of this species. Visible A. japonicus density was highest in 2010 and lowest in 2013. Over four years, the density decreased to approximately 10% of that in the year with peak density. Thus, the density in the area preferred for A. japonicus of Maizuru Bay noticeably decreased. Furthermore, fishermen mainly catch large A. japonicus individuals and avoid catching smaller individuals (< 100 g,
Funding This study was financially supported by the Coastal Ecosystem Complex Project of the Ocean Resource Use Promotion Technology Development Program, MEXT of Japan and Maizuru City.
5
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
providing support in conducting this study. References Arakawa, Y., 1990. A Handbook on the Japanese Sea Cucumber. Midori Shobo, Tokyo, pp. 1–90 (in Japanese). Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. Springer-Verlag, New York. Choe, S., 1963. Study of Sea Cucumber: Morphology, Ecology and Propagation of Sea Cucumber. Kaibundo Publishing House, Tokyo 219 pp. (in Japanese). Fisheries Agency, 2015. The research of fisheries marketing. Available at: http://www. market.jafic.or.jp/suisan/.htm, Accessed date: 1 March 2015. Goshima, S., Fujiyoshi, Y., Ide, N., Ruth, U.G., Nakao, S., 1994. Distribution of Japanese common sea cucumber, Stichopus japonica in Lagoon Saroma. Suisan zoshoku 42, 261–266 (in Japanese). Hamano, T., Amio, M., Hayashi, K., 1989. Population dynamics of Stichopus japonicus Selenka (Holothuroidea, Echinodermata) in an intertidal zone and on the adjacent subtidal bottom with artificial reefs for Sargassum. Suisan zoshoku 37, 179–186 (in Japanese). Kashio, S., Yamana, Y., Furukawa, N., Uekusa, R., Goshima, S., 2016. Seasonal microhabitat use patterns in Japanese sea cucumber Apostichopus japonicus in Funka Bay, Hokkaido, northern Japan. Aquacult. Sci. 64, 371–378. Matsumiya, Y., 1984. Analysis of the sea cucumber population in Omura Bay, Nagasaki prefecture. Bull. Fac. Fish. Nagasaki Univ. 55, 1–8 (in Japanese). Nakahara, K., Tokaji, H., Nakayama, R., Goshima, S., 2018. Aestivation of the Japanese sea cucumber Apostichopus japonicus revealed by field experiment in Funka Bay, Hokkaido, Japan. Jpn. J. Benthol. 72, 94–100 (in Japanese). Purcell, S.W., Lovatelli, A., Vasconcellos, M., Ye, Y., 2010. Managing sea cucumber fisheries with an ecosystem approach. In: Alessandro, L., Marcelo, V., Yimin, Y. (Eds.), FAO Fisheries and Aquaculture Technical Paper. FAO of the United Nations, Rome 157 pp. R development core team, 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statstical computing, Vienna Austria. Sano, M., Maeda, K., Takayanagi, S., Wada, M., Hatanaka, K., Motomae, S., Kikuchi, H., Miyashita, K., 2011. Stock assessment of sea cucumber Apostichopus armata in coastal areas of northern Hokkaido estimated from dredge-net catch data. Nippon Suisan Gakkaishi 77, 999–1007 (in Japanese). Takahashi, K., 2003. Apostichopus japonicus (Selenka). In: Ueda, Y., Maeda, K., Shimada, H., Takami, T. (Eds.), Fisheries and Aquatic Life in Hokkaido. Hokkaido Shimbun Press, Sapporo, pp. 408–409 (in Japanese). Tanaka, Y., 1958. Feeding and digestive processes of Stichopus japonicus. Bull. Fac. Fish. Hokkaido Univ. 9, 14–28. Yamaguchi, M., Masuda, R., Yamashita, Y., 2016. Diel activity of the sea cucumber Apostichopus japonicus is affected by the time of feeding and the presence of predators but not by time-place learning. Fish. Sci. 82, 29–34. Yamana, Y., Hamano, T., Goshima, S., 2008. Individual tracking to specify the aestivation site of adult sea cucumber Apostichopus japonicus on a jetty in Yoshimi Bay, western Yamaguchi Prefecture, Japan. Plankton and Benthos Res. 3, 235–239. Yamana, Y., Goshima, S., Hamano, T., Yusa, T., Furukawa, Y., Yoshida, N., 2011. Formulae to estimate standard body length for regional forms of the sea cucumber Apostichopus japonicus in Japan. Nippon Suisan Gakkaishi 77, 989–998 (in Japanese). Yang, H., Yuan, X., Zhou, Y., Mao, Y., Zhang, T., Liu, Y., 2005. Effect of body size and water temperature on food consumption and growth in the sea cucumber Apostichopus japonicus (Selenka) with special reference to aestivation. Aquacult. Res. 36, 1085–1092. Yuan, X., Yang, H., Wang, L., Zhou, Y., Zhang, T., Liu, Y., 2007. Effects of aestivation on the energy budget of sea cucumber Apostichopus japonicus (Selenka). Acta Echologica Sinica 27, 3155–3161.
Fig. 4. Frequency distribution of the standard body length of Apostichopus japonicus in Maizuru Bay, Japan, during the period with low sea water temperature (February to March) in (a) 2010, (b) 2011, and (c) 2012.
Declarations of interest None. Acknowledgments We thank the Fisheries Cooperation Association of Kyoto for
6
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Seasonal and interannual variation in the density of visible Apostichopus japonicus (Japanese sea cucumber) in relation to sea water temperature
T
Kenji Minamia,∗,1, Reiji Masudaa, Kohji Takahashia, Hideki Sawadaa, Hokuto Shirakawab, Yoh Yamashitaa a b
Field Science Education and Research Center, Kyoto University, Nagahama, Maizuru, Kyoto, 625-0086, Japan Field Science Center for Northern Biosphere, Hokkiado University, Hakodate, Hokkaido, 040-0051, Japan
A R T I C LE I N FO
A B S T R A C T
Keywords: Biomass Resource management Resource surveys Japanese sea cucumber Water temperature
Apostichopus japonicus (Japanese sea cucumber) is of ecological and economic importance in the coastal waters of Japan. To assess the apparent abundance of A. japonicus, density data of visible A. japonicus are required; however, the activity of this species on the sea floor changes with variations in sea water temperature. For example, at high sea water temperatures, A. japonicus takes shelter in the gaps of rocks or oyster shells. This change in its visibility on the sea floor makes it difficult to determine the apparent abundance of this species. In the present study, we aimed to clarify the optimal survey timing to assess the apparent abundance of A. japonicus based on the relationship between the density of visible A. japonicus and sea water temperature. Between 2010 and 2013, we evaluated how the density (ind. 100 m−2) of visible A. japonicus changes with sea water temperature in an area preferred by these organisms, Maizuru Bay, Kyoto, Japan, every 2 weeks. Seasonal changes in the density were consistent with seasonal variations in sea water temperature. Density increased when sea water temperature decreased and was at a maximum at minimum sea water temperatures. In addition, the density tended to change significantly over a short period. In some cases, the density after the lowest sea water temperature in March 2011 declined by half from 65 to 27 in just 2 weeks. Owing to considerable variations in the density of visible A. japonicus, we believe it is important to establish the appropriate survey timing to quantify the apparent abundance of this species, with our data suggesting that surveys should be performed during the season with the lowest sea water temperatures. Furthermore, at the lowest sea water temperatures in 2010, 2011, 2012, and 2013, the maximum densities were 99.0 (9.1 °C), 65.0 (9.7 °C), 41.3 (9.8 °C), and 8.7 (8.9 °C), respectively. Over 4 years, the density decreased to approximately 10% of that in the year with the peak density. Considering this decrease, it is suggested that A. japonicus in Maizuru Bay is overfished. Therefore, it is possible that the density of visible A. japonicus at the lowest sea water temperatures provides useful information for assessing the apparent abundance of this species.
1. Introduction The Japanese sea cucumber Apostichopus japonicus is distributed along the coastal sea area of northeastern Asia and is the dominant holothuroid species from Hokkaido to Kagoshima in Japan (Choe, 1963; Takahashi, 2003). This species is a deposit feeder that consumes diatoms, detritus, and bacteria mixed with sediments on the seabed, and assimilates about 50% of the organic carbon and nitrogen in the sediment (Tanaka, 1958; Choe, 1963). Therefore, A. japonicus plays an important ecological role as a consumer, and is involved in improving
the sea floor sediment in coastal waters. In addition, A. japonicus is a high-value fishery product in Japan. For example, in 2010, A. japonicus products from the waters of Hokkaido, Japan, were traded for approximately 3400 yen per kilogram (fresh weight - Fisheries Agency: http://www.market.jafic.or.jp/suisan/, Accessed 4 Apr 2018). Furthermore, the processed products, such as dried A. japonicus (75,000 yen per dry weight in kilograms), are high value commodities (Commercial dealer: http://www.namakoya.com/, Accessed 12 March 2019). However, a recent increase in demand for sea cucumbers worldwide has led to increased fishing pressure, with a decline in
Abbreviations:Region, Japan, Kyoto, Maizuru Bay (35 29.3833 N, 135 22.1167 E) ∗ Corresponding author. Estuary Research Center, Shimane University, Matsue, Shimane, 690-8504, Japan. E-mail address: [email protected] (K. Minami). 1 Present Address: Estuary Research Center, Shimane University, Matsue, Shimane, 690–8504, Japan. https://doi.org/10.1016/j.ecss.2019.106384 Received 30 July 2018; Received in revised form 12 August 2019; Accepted 16 September 2019 Available online 19 September 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
contour line at 2.7 m (depth at first survey, 2 February 2010, Tide 128 cm) and depth and location remained the same for each subsequent survey. The transect was located on the silt bottom areas close to the location of the oyster shell reefs (approximately 1–5 m from the oyster shell reef). The number of A. japonicus individuals in the transect line was counted. Only the A. japonicus visible on the surface of the seafloor, including partially visible individuals were counted. We did not turn over rocks or oyster shells and look into gaps of rocks or oyster shells. A. japonicus individuals completely hidden in rock crevices or oyster shells were not counted. The density (ind./100 m2) of visible A. japonicus was calculated from the number of counted individuals. The sea water temperature of the bottom layer was measured using a calibrated temperature sensor from a diving computer at the survey start time (TUSA IQ-850, Tabata Co. Ltd, Tokyo Japan). Between February 2010 and September 2013, the survey was conducted every two weeks. The density (response variable) was compared with sea water temperature, tidal depth, rate of tidal change and survey time (explanatory variable) between years by fitting a generalized linear model (GLM) using a gamma family with a model link function equal to log in R version 3.4.1 (R Core Team, 2017). The tidal depth, tidal change, and time are environmental factors that may affect the density, other than sea water temperature in areas preferred by A. japonicus (Choe, 1963; Yamaguchi et al., 2016). The survey time was the survey start time. The tidal depth was the depth corrected by tide at the survey start time. The tidal change was the amount of change in the tide depth over the 1 h period preceding the start time. Tidal data is that for the Maizuru bay station (Japan Meteorological Agency: http://www.data.jma.go.jp/kaiyou/db/ tide/suisan/, Accessed 12 March 2019). Because each survey took only 20–30 min, explanatory variables were constant throughout the survey and we used a single value (the initial conditions) for each survey as explanatory variables. The four explanatory variables were independent of each other, as demonstrated by the index variance inflation factor (VIF) for examining the multicollinearity; VIF values for this group of variables were all less than 10. The information-theoretic approach was used in model selection (Burnham and Anderson, 2002). This approach allows the “best” model to be selected and also ranks the remaining models. Akaike's Information Criterion (AIC) value was calculated for all models. Delta AIC (ΔAIC) was calculated as the difference in AIC between all models and the best model in the set. Models with AIC differences of less than two have substantial support (Burnham and Anderson, 2002), and individual models were selected based on AIC. The best-fit model was selected as the minimum AIC model. The body length (L) and width (B) of the ventral surface of A. japonicus were measured underwater using a ruler when the sea water temperature at the lowest point in 2010, 2011, and 2012. We were not able to calculate the standard body length in 2013, as the sampling number was low and their shapes were bent. L was the mid-line from the tip to the end of the body, and B was the central width of the body, excluding the papillae and parapodia. Individuals that were straight were selected, because measurements of A. japonicus with a bent body produce large errors when calculating the standard body length (Le). Since this survey was conducted in silt bottom areas of the boundary area, with few structures and relatively flat sea bottoms, the shape over 80% of A. japonicus in our survey area was almost straight shape, regardless of the large and small sizes of A. japonicus. Standard body lengths were calculated using L and B, as follows (Yamana et al., 2011):
resources being reported in various parts of Japan (Purcell et al., 2010). Owing to the ecological and economic contributions of sea cucumbers and their declining abundance, it is important for fisheries scientists and environmental managers to accurately quantify the apparent abundance of A. japonicus to ensure their sustainability in coastal areas. Therefore, a quantitative estimation of A. japonicus density is required to provide an index of apparent abundance. Various resource surveys have been conducted in Japan, such as that calculated from CPUE (catch per dredge-net) against cumulative catch (Matsumiya, 1984), and from the catch against dredged area (Sano et al., 2011). However, the life history of A. japonicus, which is closely associated with sea water temperature, makes it difficult to estimate population density in dredge-based surveys. Specifically, sea water temperature regulates their behavioral patterns through the year (Arakawa, 1990; Kashio et al., 2016). Aestivation is a special type of dormancy that allows A. japonicus to survive during periods of high sea water temperatures (Yuan et al., 2007). During periods of high sea water temperature, A. japonicus take shelter in gaps of rocks and oyster shells (Yamana et al., 2008; Nakahara et al., 2018). When the sea water temperature begins to decrease, A. japonicus becomes more active. Therefore, the density of visible A. japonicus on the sea floor fluctuates considerably during the year. Seasonal variations in their visibility make it difficult to determine the apparent abundance of A. japonicus if surveys are conducted at different times. Thus, it is important to conduct surveys at times when A. japonicus are most visible to quantify their abundance accurately. However, only a limited number of studies have examined seasonal change in the density of visible A. japonicus in relation to sea water temperature. Therefore, the optimal timing of surveys to assess the apparent abundance of A. japonicus has not been clearly documented. In the present study, we aimed to understand seasonal changes in the density of visible A. japonicus and their association with sea water temperature and other possible environmental parameters. Between 2010 and 2013, we documented the density and seawater temperature in Maizuru Bay, Kyoto, Japan, every 2 weeks. We used this information to identify the optimal timing of surveys to assess the apparent abundance of A. japonicus. 2. Materials and methods The survey was conducted in the coastal waters of Maizuru Bay, Japan (Fig. 1). Maizuru Bay is located in the temperate zone in the Sea of Japan and is a semi-closed bay. Average salinity in our survey area was 31.9 ± 0.8 (SD) in 2011, and salinity remained stable through the years of our study (2010–2013), during which no large salinity changes were reported. It is an important fishing ground for A. japonicus. The fishing season is from November to March. Areas where the sea floor is less than 2 m deep in the survey area are largely covered by oyster shells, except for small areas with an exposed silt bottom and areas along quay walls. The deeper areas of the survey area were composed of muddy silt with scattered small rocks. A. japonicus were captured using a beam trawl mainly in Maizuru Bay deeper than the oyster shell reefs. In addition, small structures, such as an artificial fish reefs (width 1 m, length 1 m, height 1 m), are scattered on the sea bottom in the survey areas located 10–30 m distant from the coastline. Therefore, A. japonicus could not be fished using a beam trawl in the survey area. A. japonicus has three ventral color types (red, green, and black). In Maizuru Bay, the ventral color of this species is mainly green. A. japonicus prefers to inhabit the boundary area of the silt bottom and oyster shell reef, which contains large quantities of sediment and provides refuge (Hamano et al., 1989; Goshima et al., 1994). In the survey area, several such boundary areas were present. In these boundary areas, direct observation using SCUBA was conducted during the daytime to estimate visible A. japonicus density. To manage quantitative data, an area of 300 m2 (150 × 2 m = 300 m2) was set as a belt transect line in the survey area (Fig. 1). The belt transect followed the depth
1
Le = 5.30 + 2.01 × (L × B )
2
(1)
3. Results Fig. 2 shows visible A. japonicus density versus sea water temperature in Maizuru Bay. The maximum density (2010: 99.0 ind. 100 m−2, 2011: 65.0 ind. 100 m−2, 2012: 41.3 ind. 100 m−2, 2013: 8.7 ind. 100 m−2) was observed during February and March (Table 1). 2
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Fig. 1. Study area. Solid line indicates the survey belt transect line.
The average sea water temperature on days when A. japonicus was observed again on the sea floor was 15.0 ± 2.7 °C over the 4 years of the survey. The visible A. japonicus density increased with decreasing sea water temperature. Density was compared with sea water temperature, tidal depth, tidal change, and survey time between years by GLM. A best-fit model was selected from a set of models (Table 2). The model with only sea water temperature was selected as the best model in all survey years. Fig. 3 shows the relationship between the visible A. japonicus density and sea water temperature estimated by GLM (Table 3). Between 2010 and 2013, a consistent trend was observed for visible A. japonicus density with increasing/decreasing sea water temperature. After 2010, the maximum density of A. japonicus in Maizuru Bay decreased each year (Fig. 2). The density in 2013 (8.7 ind. 100 m−2 ± 3.9) was less than 1/10 of that observed in 2010 (99.0 ind. 100 m−2 ± 50.5). During the season with maximum density (from February to March), the average standard body length of A. japonicus in 2010, 2011, and 2012 was 16.0 ± 3.2 cm (11.4–23.3 cm), 18.9 ± 4.3 cm
Thereafter, the density rapidly decreased from the maximum density. At the end of June, no A. japonicus individuals were found on the sea floor. During this period, A. japonicus takes shelter in the gaps of rocks and oyster shells. From the middle of December, we observed A. japonicus on the sea floor (2010: 0.3 ind. 100 m−2, 2011: 1.0 ind. 100 m−2, 2012: 0.3 ind. 100 m−2, 2013: no data), and the density then increased rapidly until February. On the other hand, when A. japonicus density was at a maximum (February and March), the sea water temperature was 9.4 °C ± 0.4 (SD) (2010: 9.1 °C, 2011: 9.7 °C, 2012: 9.8 °C, 2013: 8.9 °C), after which the sea temperature increased slowly. In August and September, the sea water temperature was highest (2010: 31.0 °C, 2011: 29.5 °C, 2012: 30.9 °C, 2013: 31.6 °C); thereafter, it decreased from the highest sea water temperature (Fig. 2). During February and March, the sea water temperature became lowest. In this period, A. japonicus density was observed as the highest. A. japonicus density decreased with increasing sea water temperature. In particular, the average sea water temperature when the density became zero during the four survey years was 24.7 ± 3.2 °C (Table 1).
Fig. 2. Density of visible Apostichopus japonicus versus sea water temperature in Maizuru Bay, Japan, between 2010 and 2013. Solid line indicates the density of A. japonicus. Dotted line indicates the sea water temperature. Closed squares and circles indicate the observed values. 3
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Maizuru Bay, individuals taking refuge in oyster shells and rock crevices were observed again on the sea floor when the sea water temperature decreased in the fall and was < 15.0 °C ± 2.7 °C. The relationship between the visible A. japonicus density and sea water temperature was consistent with that reported for the seasonal activity of A. japonicus in a previous study. Therefore, visible A. japonicus density changes with changing sea water temperature. Furthermore, since the relationship between density and sea water temperature was strong, it is considered that the model of density could be expressed with only sea water temperature. In addition, during aestivation, the digestive ability of A. japonicus is low, with limited feeding and weight loss (Choe, 1963). Therefore, after aestivation A. japonicus needs to feed to recover the lost weight. For recovery and growth, the digestive ability of A. japonicus increases with decreasing sea water temperature and is accompanied by an increase in food consumption (Choe, 1963). Thus, as sea water temperatures decrease, the behavioral activity of A. japonicus after aestivation is activated, with higher numbers of A. japonicus emerging from crevices to the sea floor to seek food. Conversely, as the sea water temperature increases, the digestive ability and behavioral activity of A. Japonicus decreases leading up to aestivation (Choe, 1963). Particularly, after spring from April to June, which is the breeding season in Maizuru Bay, the density of A. japonicus individuals decreases as more of them take refuge in crevices. Therefore, from these differences in the activity of A. Japonicus with the change in sea water temperature, it is considered that the visible A. japonicus density on the sea floor is greatest when sea water temperature is the lowest. Visible A. japonicus density also tended to change significantly over short periods of time (Fig. 2). For example, the density (ind. 100 m−2) found after the lowest sea water temperature in March 2011 dropped by half from 65 to 27 in only 2 weeks. Furthermore, the density before the lowest sea water temperature in January 2012 doubled from 57 to 124 in only 2 weeks. Owing to this rapid change in detectability on the sea bottom, there is a risk that the apparent abundance of A. japonicus is underestimated in surveys. Therefore, an appropriate time for surveys must be selected to assess the apparent abundance of A. japonicus. The visible A. japonicus density increased when the sea water temperature decreased. The density was highest when the sea water temperature was lowest. This trend was observed every year for approximately 4 years (Fig. 3). The visible A. japonicus density at the lowest sea water temperature in a single year could be used to assess the apparent abundance of A. japonicus. Therefore, to assess the apparent abundance, surveys that monitor the density on the sea floor should be conducted when the sea water temperature is low. In addition, the resource survey of A. japonicus is currently conducted using dredge-nets in Japan (Matsumiya, 1984; Sano et al., 2011). The obtained density data by dredge-net is the number of A. japonicus individuals per unit area of the surface of the seafloor. It is similar to the visible A. japonicus density in which the density on the surface of the sea floor is calculated. However, the resource survey did not consider the seasonal changes of A. japonicus on the surface of the sea floor with accompanying sea water temperature change, as obtained in the present study. Therefore, depending on the timing of the survey, the resource abundance may be underestimated. In the future, it would be necessary to consider the seasonal changes of A. japonicus on the surface of the seafloor owing to sea water temperature, in such resource surveys. However, in cold zones, compared with temperate zones, such as Maizuru Bay, where the minimum sea water temperature (8.1 °C) is lower than that documented in this study, the influence of low sea water temperature on the density should be examined further. Moreover, the surveys were conducted during the daytime in this study. However, A. japonicus has been found to move actively at night (Yamaguchi et al., 2016). It might be that the density of visible A. japonicus individuals at night is closer to the actual resource than that in the day. Therefore, to estimate the resource condition of A. japonicus, it would also be necessary to clarify the survey timing considering diurnal activity. Note that this study was not designed to be a random survey that
Table 1 Trend in the density of visible Apostichopus japonicus and sea water temperature in each season. Density of visible individuals (ind. 100m−2) Feb–Mar.
Mar–Jun.
Jun–Dec.
Dec–Feb.a
Year
(Maximum)b
(Decrease)
(Completely hidden)
(Increase)
2010 2011 2012 2013
99.0 65.0 41.3 8.7
99.0–3.0 65.0–1.3 19.0–0.3 2.7–0.0
None None None None
0.3–51.0 1.0–41.3 0.3–8.7 no data
Feb–Mar.
Mar–Jun.
Jun–Dec.
Dec–Feb.a
Year
(Avg 9.4 ± SD 0.4)c
(Increase)
(Avg 24.7 ± SD 3.2)d
(Decrease)
2010 2011 2012 2013
9.1 9.7 9.8 8.9
9.1–23.8 9.7–22.0 10.6–19.2 9.8–24.8
23.8 29.5 23.1 22.5
13.6–9.0 18.1–9.6 13.2–8.1 no data
Sea water temperature (°C)
a
February of the following year. Maximum density of Apostichopus japonicus. c Sea water temperature when the density of Apostichopus japonicus was maximum. d Sea water temperature when the density of Apostichopus japonicus was zero. b
Table 2 Highest ranked generalized linear models in each survey years using AIC-based model selection for the density of visible Apostichopus japonicus. The table also shows sea water temperature (TEMP), tidal depth (DEPTH), tidal change (CHANGE), survey time (TIME) and AIC differences (ΔAIC). Year
Model
2010
TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP TEMP
2011
2012
2013
+ CHANGE + TIME + TIME + CHANGE + DEPTH + CHANGE + DEPTH + TIME
AIC
ΔAIC
48.8 49.9 50.2 44.8 45.1 45.2 51.8 52.7 52.9 29.9 31.0 31.1
0.0 1.1 1.4 0.0 0.3 0.4 0.0 0.9 1.1 0.0 1.1 1.2
(11.4–26.8 cm), and 18.8 ± 3.8 cm (12.2–27.8 cm), respectively (Fig. 4). In 2010, the body length primarily ranged from 10 to 15 cm. In comparison, in 2011 and 2012, the body length primarily ranged from 15 to 20 cm. The percentage of individuals with body lengths from 10 to 15 cm decreased across years; namely, for 2010, 2011, and 2012, the percentage of individuals with 10–15 cm body length was 44%, 22%, and 13%, respectively.
4. Discussion Seasonal variation in visible A. japonicus density was consistent with seasonal variation in sea water temperature (Fig. 2). The sea water temperature was 24.7 °C ± 3.2 °C when A. japonicus individuals were taking shelter in rock crevices or oyster shells. This result was consistent with the sea water temperature (24.5–25.5 °C) during the period when A. japonicus shifts to aestivation (Choe, 1963; Yang et al., 2005). When the sea water temperature begins to decrease during fall, A. japonicus that took refuge in oyster shells and rocks emerge onto the sea floor (Choe, 1963). A previous study (Choe, 1963) also reported that the sea water temperature during the activity period was < 17.5–19 °C. In 4
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
Fig. 3. Relationships between the density of visible Apostichopus japonicus and sea water temperature in (a) 2010, (b) 2011, (c) 2012, and (d) 2013. Grey circles indicate the observed values. Solid line indicates the regression curve estimated by a generalized linear model (GLM). Dashed line indicates the confidence interval.
standard body length 18 cm) in Maizuru Bay to conserve this resource. When small individuals are caught using fishing gear, they are released into the sea. However, despite efforts to avoid catching small A. japonicus, between 2010 and 2012, the frequency of individuals with a small standard length (10–15 cm) decreased appreciably (Fig. 4). It is possible that large individuals are overfished and reproduction is decreasing and therefore, the A. japonicus population in Maizuru Bay is decreasing. From 2010 (157 t) to 2013 (57 t), the catch per year in Maizuru Bay decreased by about 100 t (Fisheries Agency, 2015). Therefore, we suggested that the number of A. japonicus individuals in Maizuru Bay was decreasing possibly due to overfishing. By monitoring visible A. japonicus density when sea water temperature is at its lowest, any decrease or increase in density may be objectively estimated. In addition, it might be possible that other information, such as standard body length could be used to understand the variations in A. japonicus density. Visible A. japonicus density at the lowest sea water temperature provided useful information for assessing the apparent abundance of this species.
Table 3 Results of the generalized linear model (GLM) comparing the density of visible Apostichopus japonicus and sea water temperature (TEMP). Year
Variable
Estimate
Standard error
t value
Pr(> |t|)
2010
Intercept TEMP Intercept TEMP Intercept TEMP Intercept TEMP
10.156 −0.491 8.718 −0.465 7.948 −0.432 4.675 −0.271
0.975 0.046 0.743 0.037 0.920 0.050 0.875 0.044
10.420 −10.600 11.740 −12.620 8.639 −8.672 5.345 −6.112
1.54 × 10−8 1.22 × 10−8 2.00 × 10−10 5.52 × 10−11 2.02 × 10−7 1.92 × 10−7 8.17 × 10−5 1.99 × 10−5
2011 2012 2013
*** *** *** *** *** *** *** ***
***p < 0.001.
could quantify the A. japonicus population in this region. The measurements of density in this study were focused on a specific area preferred by A. japonicus, and A. japonicus that were present but completely hidden in rock crevices or oyster shells were not counted. Therefore, the measured density cannot be used to reflect the overall density in Maizuru Bay. However, multi-year comparable indicators in a habitat preferred by A. japonicus could provide a qualitative understanding of the abundance of this species. Visible A. japonicus density was highest in 2010 and lowest in 2013. Over four years, the density decreased to approximately 10% of that in the year with peak density. Thus, the density in the area preferred for A. japonicus of Maizuru Bay noticeably decreased. Furthermore, fishermen mainly catch large A. japonicus individuals and avoid catching smaller individuals (< 100 g,
Funding This study was financially supported by the Coastal Ecosystem Complex Project of the Ocean Resource Use Promotion Technology Development Program, MEXT of Japan and Maizuru City.
5
Estuarine, Coastal and Shelf Science 229 (2019) 106384
K. Minami, et al.
providing support in conducting this study. References Arakawa, Y., 1990. A Handbook on the Japanese Sea Cucumber. Midori Shobo, Tokyo, pp. 1–90 (in Japanese). Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. Springer-Verlag, New York. Choe, S., 1963. Study of Sea Cucumber: Morphology, Ecology and Propagation of Sea Cucumber. Kaibundo Publishing House, Tokyo 219 pp. (in Japanese). Fisheries Agency, 2015. The research of fisheries marketing. Available at: http://www. market.jafic.or.jp/suisan/.htm, Accessed date: 1 March 2015. Goshima, S., Fujiyoshi, Y., Ide, N., Ruth, U.G., Nakao, S., 1994. Distribution of Japanese common sea cucumber, Stichopus japonica in Lagoon Saroma. Suisan zoshoku 42, 261–266 (in Japanese). Hamano, T., Amio, M., Hayashi, K., 1989. Population dynamics of Stichopus japonicus Selenka (Holothuroidea, Echinodermata) in an intertidal zone and on the adjacent subtidal bottom with artificial reefs for Sargassum. Suisan zoshoku 37, 179–186 (in Japanese). Kashio, S., Yamana, Y., Furukawa, N., Uekusa, R., Goshima, S., 2016. Seasonal microhabitat use patterns in Japanese sea cucumber Apostichopus japonicus in Funka Bay, Hokkaido, northern Japan. Aquacult. Sci. 64, 371–378. Matsumiya, Y., 1984. Analysis of the sea cucumber population in Omura Bay, Nagasaki prefecture. Bull. Fac. Fish. Nagasaki Univ. 55, 1–8 (in Japanese). Nakahara, K., Tokaji, H., Nakayama, R., Goshima, S., 2018. Aestivation of the Japanese sea cucumber Apostichopus japonicus revealed by field experiment in Funka Bay, Hokkaido, Japan. Jpn. J. Benthol. 72, 94–100 (in Japanese). Purcell, S.W., Lovatelli, A., Vasconcellos, M., Ye, Y., 2010. Managing sea cucumber fisheries with an ecosystem approach. In: Alessandro, L., Marcelo, V., Yimin, Y. (Eds.), FAO Fisheries and Aquaculture Technical Paper. FAO of the United Nations, Rome 157 pp. R development core team, 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statstical computing, Vienna Austria. Sano, M., Maeda, K., Takayanagi, S., Wada, M., Hatanaka, K., Motomae, S., Kikuchi, H., Miyashita, K., 2011. Stock assessment of sea cucumber Apostichopus armata in coastal areas of northern Hokkaido estimated from dredge-net catch data. Nippon Suisan Gakkaishi 77, 999–1007 (in Japanese). Takahashi, K., 2003. Apostichopus japonicus (Selenka). In: Ueda, Y., Maeda, K., Shimada, H., Takami, T. (Eds.), Fisheries and Aquatic Life in Hokkaido. Hokkaido Shimbun Press, Sapporo, pp. 408–409 (in Japanese). Tanaka, Y., 1958. Feeding and digestive processes of Stichopus japonicus. Bull. Fac. Fish. Hokkaido Univ. 9, 14–28. Yamaguchi, M., Masuda, R., Yamashita, Y., 2016. Diel activity of the sea cucumber Apostichopus japonicus is affected by the time of feeding and the presence of predators but not by time-place learning. Fish. Sci. 82, 29–34. Yamana, Y., Hamano, T., Goshima, S., 2008. Individual tracking to specify the aestivation site of adult sea cucumber Apostichopus japonicus on a jetty in Yoshimi Bay, western Yamaguchi Prefecture, Japan. Plankton and Benthos Res. 3, 235–239. Yamana, Y., Goshima, S., Hamano, T., Yusa, T., Furukawa, Y., Yoshida, N., 2011. Formulae to estimate standard body length for regional forms of the sea cucumber Apostichopus japonicus in Japan. Nippon Suisan Gakkaishi 77, 989–998 (in Japanese). Yang, H., Yuan, X., Zhou, Y., Mao, Y., Zhang, T., Liu, Y., 2005. Effect of body size and water temperature on food consumption and growth in the sea cucumber Apostichopus japonicus (Selenka) with special reference to aestivation. Aquacult. Res. 36, 1085–1092. Yuan, X., Yang, H., Wang, L., Zhou, Y., Zhang, T., Liu, Y., 2007. Effects of aestivation on the energy budget of sea cucumber Apostichopus japonicus (Selenka). Acta Echologica Sinica 27, 3155–3161.
Fig. 4. Frequency distribution of the standard body length of Apostichopus japonicus in Maizuru Bay, Japan, during the period with low sea water temperature (February to March) in (a) 2010, (b) 2011, and (c) 2012.
Declarations of interest None. Acknowledgments We thank the Fisheries Cooperation Association of Kyoto for
6