Growth and Distribution of Amphioctopus fangsiao (d’Orbigny, 1839–1841) in Haizhou Bay, Yellow Sea

PANG YumengTIAN Yongjun,FU CaihongREN Yiping,and WAN Rong

Growth and Distribution of(d’Orbigny, 1839–1841) in Haizhou Bay, Yellow Sea

PANG Yumeng1), TIAN Yongjun1),2),3),*, FU Caihong4), REN Yiping1),3), and WAN Rong5)

1),,266003,2),,266100,3),,266071, China 4),,,V9T 6N7,5),,201306, China

Octopus fisheries have prospered in many areas of the world ocean over the last six decades. Despite degradation and overexploitation of Chinese coastal ecosystems, octopus has become a stable Chinese domestic fishery species. Among the octopus species in the Bohai and Yellow, East and South China Seas,(d’Orbigny [in Férussac & d’Orbigny], 1839–1841) plays an increasingly important role both economically and ecologically. However, no systematic research has been conducted on its biology and population dynamics in the China Seas. In this study, we characterized the growth and distribution ofin Haizhou Bay, Yellow Sea based on four years of trawl survey data. As the results,is characterized by allometric growth and an overall sex ratio of 0.97 with a slight male bias. Small octopus can be observed through a whole year, suggesting thatmay have an extended or continuous spawning season.may migrate short distances along with seasonal changes and coastal currents, considering they overwinter in the offshore water and spawn in the inshore water. In addition to fishing pressure, annual variations in the population structure and biomass appeared to be influenced by ambient water temperature. These results provide basic biological information for a better understanding of the population dynamics and the ecological importance of

; cephalopod, Haizhou Bay; growth; spatial distribution

1 Introduction

While many fish species have been heavily exploited and thus depleted worldwide, cephalopods have taken ad- vantage of changing environmental conditions and expanded their populations over the last two decades (Doubleday., 2016). The coastal cephalopod catch in the China Seas (Bohai Sea, Yellow Sea, East China Sea, and South China Sea) has generally increased along with awarming environment since 2000, although rates of change are species-dependent (Pang., 2018). Octopus in the China Seas play an increasingly important role in the Chi- nese coastal cephalopod fisheries. Their contribution to catch has increased in recent years (Fig.1) at a rate that is similar to global octopus catch over the last two decades (FAO, 2012).

The most common octopus species in Chinese coastal areas is, an important commercial species in the Chinese cephalopod fishery that has overtaken golden cuttlefish () and common Chi- nese cuttlefish (de Rochebrune) over the last century.is mainly distributed along coastal areas of the Western Pacific and is commonly seen from Japanese waters to the China Seas. Coastal octopus is cultured using the cage and otter trawl methods. In the 1970s,catch during early spring comprised 85% of the annual cephalopod yield in the China Seas (Dong, 2014). However, due to poor species identification in octopus fisheries, the exact number ofcaught from year to year is unavailable.

Previous research onis rather limited and has focused on population genetics analysis and embryonic development for aquaculture purposes (Lu., 2010;Dong, 2014). Tank culturing experiments indicate that ma- turation is affected by temperature, food availability and photoperiod (Dong, 2014). Geographical isolation distinguishes multiple stocks due to limited mobility (Lu., 2010). It is unclear how many stocks exist in the China Seas. Despite the increasing proportion of octopus catch in recent years, studies on natural populations ofare generally lacking and the mechanism of their do-minance in some coastal areas is unclear.

Fig.1 (A) Catch ratio of squid, cuttlefish, and octopus in the Chinese coastal fishery; (B) Catch of octopus in the Chinese coastal fishery.

Haizhou Bay is a shallow open coastal area in the west southern Yellow Sea (Fig.2). This area is an important spawning and nursery ground for many fish species (Tang., 2011; Pang., 2015), and one of the most productive fishery grounds in the China Seas (Tang., 2011; Zhang, 2013). However, Haizhou Bay has become degraded in recent decades as a result of long-term high fishing pressure (Su., 2015). This study was initiated to present a general view on the biology of thepopulation in Chinese coastal areas, and specifically to characterize the subpopulation in Haizhou Bay. This is the first study to describe thepopulation growth and distribution pattern in an over-exploited ecosystem.

Fig.2 Location and sampling design for the survey in Hai- zhou Bay, China. The five strata (encircled by bold broken lines) are divided based on depth, current, and substrate.

2 Materials and Methods

2.1 Sampling Survey

Octopus samples were collected using a 300 hp survey vessel with a single bottom trawl in Haizhou Bay (Fig.2) and its vicinity waters (119˚20΄E–121˚10΄E, 34˚20΄N–35˚40΄N) from 2011 to 2015 (except for 2012). Five seasonal bottom trawl surveys were conducted in 2011, including March and May (spring), July (summer), Septem- ber (autumn), and December (winter). Surveys were only conducted in May and October from 2013 to 2015, which represent spring and autumn. During all surveys, trawling speed was set at 2–3 knots for approximately 60min tows. In 2011, trawl net width was 25m, cod end mesh size was 17mm, and net height was 6 m. From 2013 to 2015, trawl net width was 12m, and trawl net height was 1.2m. The survey area included 76 grids (10΄×10΄ each) divided into five strata (A–E) based on depth, current, and substrate (Fig.2). The numbers of grids randomly selected in each stratum were 3, 5, 3, 9, and 4, respectively, during each survey.

The total number ofwas counted and all specimens were weighed. Environmental data including sur- face and bottom water temperatures, surface and bottom water salinities, and the depth were measured by a conductivity, temperature, and depth profiler at the same time and were recorded for each tow. Asis a holobenthic species, we used the bottom water temperature data for further analysis.

2.2 Biological Measurements

A total of 1389individuals were selected randomly from each cruise during the four years of surveys (915, 275, 98, and 101 for 2011, 2013, 2014, and 2015, respectively). The total length and dorsal mantle length were measured to the nearest mm, while the total weight and mantle weight were measured to the nearest gram. Additionally, the gender of 759 individuals in the survey of 2011 were identified by the structure of their reproductive system (López-Peraza., 2013).

2.3 Statistical Analysis

The sex ratio of each sampling month in 2011 was calculated by dividing the number of females with the number of males. Deviation of the sex ratio from 1:1 was checked using the chi-square test with 1 degree of freedom (Microsoft Excel; Microsoft Inc., Redmond, WA, USA).-values are presented to indicate a deviation from an equal sex ratio.

The relationship between dorsal mantle length () and total weight () was determined using the following equation:

whereis the coefficient of the arithmetic length-weight relationship andis the exponent of the length-weight relationship reflecting an isometric (=3) or allometric (≠3) growth pattern (Froese, 2006). Length-weight relationships were determined for males and females, respectively. Length-weight relationships were also compared among the five surveys in 2011 to observe seasonal variation.data were grouped in 10mm bins, and the frequency distribution was modeled using a bimodal distribution for each cruise from 2011 to 2015 (Aizawa, 1999). Peaks of the length distributions from all surveys were used to describe the growth pattern of thepo- pulation by each year.

To calculate catch per unit effort (CPUE), trawl duration was standardized to 60min with a tow speed of 2 knots for each survey. To compare data from different years and stations, we defined the fishing effort as per standard net mouth area, and thewas estimated as the catch weight per standard net mouth area. The units forare kilograms per area (kgkm−2). The spatial distribution ofin spring (May) and autumn (September/Octo- ber) from each sampling year was identified using Arc-GIS 10.2 to display the annual variation. The reported ma- ximum size ofis 80mm(Villanueva., 2016); thus, we roughly divided our samples into small individuals (<40mm) and large individuals (>40mm) by half of the maximum. Similarly, the seasonal change in spatial distribution ofwas compared between small and large individuals using the 2011 data to elucidate possible migration.

3 Results

3.1 Length-Weight Relationship

The female to male ratio across all years was 0.97:1. The sex ratio by month did not deviate significantly from 1:1, with only a slight bias toward males in July (chi-square test,=1,=0.997).The length-weight relationships for males and females were (Fig.3):

.

Table 1 Seasonal length-weight relationships of Amphioctopus fangsiao collected in 2011

Thelength-weight relationships also changed seasonally (Table 1). The allometric coefficient () ranged from 1.98 (autumn) to 2.64 (early spring), while parameterchanged from 1.3 (early spring) to 16.1 (autumn).

3.2 Mantle Length (ML) Distribution

Thes of octopus were roughly distributed in a Gau- ssian manner (Fig.4). In 2011, two distinct length class peaks were identified in March, with one at 30mmand another at 70mm. The majority of individuals in May were around 60mm, but another small group of individuals grew from 20 to 40mmin July, to 50mmin September, and 60mmin December. As the largest size group of octopus appeared around March, we speculate that spring is the main spawning season for this species. Different length distribution modes were obser- ved in spring and autumn of other years, suggesting that growth varies by year. We suspect that the life span of this species is around 1 year, and in a year we observed more or less linear growth of(Fig.5).

Fig.4 Seasonal distribution of Amphioctopus fangsiao mantle length for all surveys in 4 years (biological data are unavailable for spring 2014).

Fig.5 Somatic growth of Amphioctopus fangsiao in a year.

3.3 Annual and Seasonal Variations in the Spatial Distribution of A. fangsiao

Based on the four 1-year surveys in spring (May) and autumn (Sept/Oct), the octopus population was distrib- uted around the entire bay with relatively stable popula- tion abundance (Fig.6).

The 2011 survey suggested strong seasonal changes in the spatial distribution for small (<40mm) and large (>40mm) individuals (Fig.7). Small octopus appear- ed in early spring near the coast, whereas the majority of large individuals remained in the outer water (A). As water temperature gradually increased, small octopuses started to occur near the shore, and were rarely found offshore (B). The number of octopus declined greatly due to death after spawning in the summer, and the proportion of small octopus increased (C). Small-size individuals kept grow- ing and spread into the entire bay in September (D). Most of the octopus developed into large individuals in Decem- ber, and only a few small octopus occurred at that time (E).

Average water temperature was positively related with the proportion of small individuals in the spring and au- tumn groups (Figs.8A–D). The autumn groups had a high- er proportion of small individuals than the spring groups during all 4 years (Figs.8C, D). In contrast, a possible ne- gative relationship was found between autumnand ambient water temperature and the proportion of the small catch (Figs.8B, D, F). The springwas high in 2011, but low in the other years despite relatively high tempera- tures in 2014 and 2015 (Figs.8A, E).

4 Discussion

Due to rapid warming and over-exploitation in the Chi- na Seas (Pang., 2018), Haizhou Bay has become a degraded ecosystem with depleted fish resources (Tang., 2011; Pang., 2015). However,, oc- cupying a relatively high trophic level and preying on a wide range of small fishes, bivalves, and crustaceans (Huang, 2004), has taken advantage of changing environmental conditions and maintained a stable population (Pang., 2018).

4.1 Growth, Body Condition, and the Spawning Season

Variations in the cephalopod sex ratio could be explain- ed by a combination of migration and post-spawning mor- tality. We did not observe a significant sex ratio bias in, which is common in many other octopus spe- cies (Mangold, 1983). A slight bias towards males in July might be caused by the death of a large number of females after spawning. The2value of the length-weight relation- ship for male and female octopus was relatively low, as growth is easily affected by changing environmental condi- tions (Semmens., 2004). This result is similar to other species, like common octopus, without a sex bias (Silva., 2002; Otero., 2007). Growth offol-lowed an allometric pattern as inferred by the-value with- out a significant difference between males and females (Von Boletzky and Villanueva, 2014).

Fig.6 Annual variation in the Amphioctopus fangsiao spatial distribution during spring and autumn; pies indicate the catch per unit effort (CPUE) values (kgkm−2).

Fig.7 Seasonal changes in the spatial distribution of Amphioctopus fangsiao by size (small: ML<40mm; large: ML>40mm) in 2011. Shaded areas refer to the number of small octopus, and dashed areas show the number of large octopus.

Fig.8 Annual changes in spring and autumn average water temperature (A, B), proportion of small (ML<40mm) (C, D) and catch per unit effort (CPUE) (E, F) during spring and autumn in Haizhou Bay.

Previous studies indicated that the spawning season ofis mainly in spring (Dong, 2014). Energy con- sumption of female octopus increased greatly during thespawning season (Von Boletzky and Villanueva, 2014), which might be the reason that the majority of individuals in May were smaller than those in March of 2011 (Figs.4 and 7). At the end of the spawning season, few individuals are left in the water, and juveniles start to appear in early summer (July 2011). In autumn, the population significantly increases with the pulse of new recruitment (Sep- tember 2011), and continues to grow in winter (December 2011). However, small individuals (<40mm) could be observed all year around in our surveys, even in winter, suggesting that octopus may have an extended spawning season or more than one spawning peak like(Patterson, 1988; Silva., 2002).Threereproductive strategies have been reported in different geographical areas (Katsanevakis and Verriopoulos, 2006), and countless unsynchronized spawning scenarios occur because of its phenotypic plasticity (Garofalo., 2010; Angeles-Gonzalez., 2017). Therefore, we hypo- thesized that this natural population ofhas a comparatively protracted spawning season which is from early spring to late autumn. Although the peaks in the lengthdistribution for the same month changed every year, growth ofdisplayed a possible linear trend from early spring to winter. Further research on age identification of this species is required to uncover the growth pattern.

Physical condition of cephalopod species varies largely due to different development stages, food availability, go- nad development, and environmental changes (Forsythe., 1987, 1988; Semmens., 2004; Pecl and Jackson, 2008). In the present study, the length-weight relationship changed with life stage during different seasons, which was reflected by theandvalues (Table 1). Generally, parameterrepresents the nutritional condition of an individual (Anderson and Gutreuter, 1983), anddescribes the growth pattern (Ricker, 1975). Spawning is a high energy-cost activity and, as expected, the physical con- dition of octopus is the poorest in spring (from March 2011), following nearly isometric growth. The physical con- dition was high due to the recruitment of juvenile octopus in summer (July 2011) and arrived the peak in autumn with extreme allometric growth (September 2011). The phy-sical condition declined and the growth slowed down when migration began in winter (December 2011) and maturation started. The growth pattern and physical condition varied greatly throughout the year. These observations indicate that this octopus species should spawn mainly in spring.

4.2 Seasonal Changes in the Distribution of Small Octopus

The migration pattern of octopus species could be different from that of other fish species. As octopus crawl on the bottom, migration is merely a short-distance movement. There are no accurate records on migration of this species, while similar species, such as common octopus, has been postulated to conduct a spawning migration from offshore to inshore waters in some areas (Guerra, 1981).

Asis a holobenthic species, it might also migrate from offshore water to inshore water through its life based on our results. Mature individuals may migrate to inshore areas for spawning during spring. Then the lar- vae and juveniles grow and develop during the summer and autumn, migrating from inshore to offshore. In winter, the majority of octopus move to offshore water for overwintering along the cold Yellow Sea Coastal Current. How- ever, further studies on recruitment and spatial distribution of spawners are needed to identify nursery and spawn- ing grounds of this species in the Yellow Sea.

4.3 Potential Effects of Water Temperature on Population Growth and Biomass

Average water temperature can lead to the annual vari- ation in growth and biomass of fishes, particularly for fast-growing species with high adaptability. High water temperature can accelerate all aspects of the life cycle of octopus in nature if food is not limited, including hatching rate, growth, maturation, and embryonic development (Forsythe and Hanlon, 1988; Segawa and Nomoto, 2002; Semmens., 2004). Although no statistical analysis was conducted in this study, potential association between the water temperature and the population growth and bio- mass could be observed, which can serve as a reference for future studies.

In our study, temperatures in 2011 and 2015 were high- er than in 2013 and 2014. Catches in autumn may have been negatively related to water temperature. Population size in autumn was mainly determined by new hatchlings in spring. The low frequency of small individuals but highin autumn 2014 suggests that there were more large individuals, which may be due to the extended spawning season in a cold environment. However, thedata were not associated with water temperature in spring, when the majority of spawning occurs. The spawning migration began early and mature individuals came inshore in the warm spring of 2011, while spawning activity may have started late in the cold springs of 2013 and 2014. The po- pulation had not recovered in spring 2015, which may have been caused by uncharacteristically late spawning during the cold 2014.

As seasonal population size and frequency of smallindividuals might be affected by relevant water temperature, we suggest that temperature is the main factor affecting the natural population dynamics of octopus (Forsythe and Hanlon, 1988; Angeles-Gonzalez., 2017). Additionally, other factors, such as light, food quality, and water currents (Forsythe and Van Heukelem, 1987; Ro- berts and van der Berg, 2002), as well as initial hatchling size and sex ratio are also crucial to the natural dynamics of octopus (Leporati, 2007). Therefore, life history traits, such as age, growth, and maturation, should be further studied to better understand the natural population dy-namics. In addition, the influence of fishing activity shouldbe included as a key factor in future work. This will ensure the accurate fishery data and the executive fishery management measures will be implemented in Haizhou Bay, Yellow Sea.

Acknowledgements

This research was partially supported by the National Key R&D Program of China (Nos. 2018YFD0900902, 2018YFD0900903),the National Natural Science Foundation of China (Nos. 41861134037, 41930534), and the ‘Fundamental Research Funds for the Central Universities’ to Ocean University of China (Nos. 201762015, 2018 2201). We thank Dr. Robert Boenish (University of Maine) for proofreading this manuscript and giving many valuable suggestions.

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