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Article

Beak Microstructure Estimates of the Age, Growth, and Population Structure of Purpleback Flying Squid (Sthenoteuthis oualaniensis) in the Xisha Islands Waters of the South China Sea

by
Ziyue Chen
1,
Huajie Lu
1,*,
Wei Liu
2,
Kai Liu
1 and
Xinjun Chen
1,3,4,5,6
1
College of Marine Sciences, Shanghai Ocean University Shanghai, Shanghai 201306, China
2
Hainan Academy of Ocean and Fisheries Science, Haikou 570100, China
3
The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
4
National Distant-Water Fisheries Engineering Research Center, Shanghai Ocean University, Shanghai 201306, China
5
Key Laboratory of Oceanic Fisheries Exploration, Ministry of Agriculture, Shanghai 201306, China
6
Scientific Observing and Experimental Station of Oceanic Fishery Resources, Ministry of Agriculture and Rural Affairs, Shanghai 201306, China
*
Author to whom correspondence should be addressed.
Fishes 2022, 7(4), 187; https://doi.org/10.3390/fishes7040187
Submission received: 5 July 2022 / Revised: 23 July 2022 / Accepted: 23 July 2022 / Published: 26 July 2022
(This article belongs to the Section Biology and Ecology)
Browse Figures
Versions Notes

Abstract

:
This study aimed to explore the feasibility of using an upper beak microstructure to estimate the age of purpleback flying squid (Sthenoteuthis oualaniensis). From these microstructures, the age and growth of squid caught from January to March and May to August in 2018, 2019, and 2020 in the waters surrounding the Xisha Islands in the South China Sea were determined. We found three typical growth zones (the hood region, crest region, and axis), abnormal increments (checks), and erosion in the beak examination. The average dorsal mantle length (ML) of males and females was 112.13 (±15.23 mm) and 119.67 mm (±24.50 mm), respectively, and no squid were older than 10 months. The peak hatching dates, according to back calculations, were from October to January of the next year. All sampled squid belonged to the autumn/winter cohort. Significant sex differences were found in the relationship between ML and age in squid with similar growth patterns. Exponential models best described the relationships of ML with age and body weight (BW) for both sexes. However, a linear model best described the relationship between age and upper rostrum length (URL). The maximum absolute daily growth rates (AGR) of BW were reached during days 240–270 for both sexes. The maximum AGRs in ML were reached during days 180–210 and 240–270 for males and females, respectively. The period of 120–150 days (4–5 months) was considered the sub-adult stage of S. oualaniensis in the Xisha Islands waters of the South China Sea. This study confirmed that the beak microstructure provides good age estimates for purpleback flying squid (S. oualaniensis).

1. Introduction

The purpleback flying squid, Sthenoteuthis oualaniensis, is one of the most abundant commercial resources of oceanic cephalopods and predominantly inhabits warmer waters in the subequatorial and equatorial Indo-Pacific Ocean [1]. The northwestern Indian Ocean and Arabian Sea are thought to be high-density areas for this important oceanic resource, as determined by a preliminary investigation conducted by the former Union of Soviet Socialist Republics (USSR) from the 1960s to the 1980s [2,3]; initially, commercial investigation and exploitation were undertaken by Chinese squid jigging vessels from 2003 to 2005 [4]. The total biomass of S. oualaniensis is estimated to be 5–7 million tons in the subtropical and tropical Pacific Ocean, and it is usually randomly caught as bycatch [1]. Despite its wide geographic distribution in the western Pacific Ocean, this resource has been inadequately exploited; in the past 40 years, it has been caught only in waters around China’s Taiwan Province and Okinawa, including by small-scale commercial jigging fisheries and local artisanal fisheries [1,5]. However, a recent survey detected more than 1 million tons of total S. oualaniensis biomass through an acoustic survey in the South China Sea, demonstrating considerable potential to sustain relatively ample yields [6]. In the South China Sea, S. oualaniensis have been mostly caught and stored as bycatch by Chinese fishing vessels equipped with light traps and falling nets in recent years, a relatively inadequate exploitation and utilization of this abundant resource [7,8].
Previous studies have generally established the fishery biology characteristics of S. oualaniensis in different areas, including its population structure, age and growth, diet and behavior, reproduction, and ecology. Because of its complex population structure and wide geographic distribution, several different intraspecific forms have been divided on the basis of distinct differences in mature body size, dorsal photophores, and life span [1,9]. S. oualaniensis is an active predator with a wide feeding spectrum in marine ecosystems; it feeds on small fishes and crustaceans and even demonstrates considerable cannibalism [1,4,10,11]. Along with its high daily dietary intake, S. oualaniensis exhibits a rapid growth rate over its short life span [1,11,12]. Moreover, S. oualaniensis is frequently found in the diet of predatory fishes, marine mammals, and birds [1,11,12]. As this species serves as both prey and predator, it may link trophic levels in the marine ecosystem [13,14,15].
In cephalopods, the beak is the feeding organ and is embedded in the muscle of the buccal mass [16]. Because of its composition (consisting of protein and chitin fibers), the beak is one of the few hard structures in cephalopods and is characterized by resistance to erosion, a stable shape, and a stiff structure [16,17]. Studies of the fishery biology and ecology of cephalopods found that the beak can help to determine taxonomy, age and growth patterns, and pigmentation, as well as to estimate biomass [18,19,20,21]. Previous growth studies have summarized the morphological characteristics and growth patterns of S. oualaniensis statoliths [22,23,24,25,26,27], but fewer studies have explored the growth pattern and pigmentation of S. oualaniensis beaks [28,29,30,31,32].
It is difficult to feed these short-lived oceanic squids under artificially experimental conditions [33]. This particular issue increased the difficulty for us to deeply understand the details of their growth pattern and whole life history. It is necessary to explore the age and growth information for sufficient development of this fishery resource. Estimating age and growth patterns could provide valuable information and a basis for fishery biology, ecology, and resource management. This age and growth information could apply for fishery biology, ecology, and stock assessment management, which includes size-at-age, maturity, and life-history parameters [34]. Environmental information was also closely related to the age and growth pattern, and it clearly reflected in the growth rate of squids in time-specific stage [34]. Differences of age structures and growth patterns were easily found between different populations and life stages, especially in S. oualaniensis [1]. Because of different body length forms and their complicated population structures of squids, estimating the age structures and growth patterns of squids with the length-frequency method is inaccurate [34]. However, clear daily growth increments are obvious in sections of squid statoliths, eye lenses, and beaks [35,36,37]. In general, previous age and growth studies mostly analyzed the statoliths of cephalopods, but studies on cephalopod beaks are relatively scarce. Early studies on the age and growth pattern of squids mainly analyzed periodically deposited increments in the statolith microstructure [38]. In recent years, the number of growth studies has increased, paralleling the gradual increase in the exploitation of important commercial species, especially ommastrephid and loliginid squids [34,35,39]. Many previous studies have examined the age and growth pattern of statolith microstructures among many species of squids in the last several decades, including Dosidicus gigas, Ommastrephes bartramii, and Sthenoteuthis pteropus [35,40,41,42]. These studies have suggested that age and growth patterns provide valuable information on the life history of cephalopods.
Compared with tiny statoliths, it is much easier to extract beaks from squid heads without destroying them. Additionally, beak specimens may be more conveniently preserved in the long term [33,43]. To decrease the high failure rate caused by the tiny size of the statolith, identification of a substitute aging tool is needed [44]. In squid beaks, a daily concentric increment in the lateral wall surface (LWS) can be clearly observed and is thought to represent 1 day in the larval stage [36]. Age estimations according to daily increments in the LWS of the beak are more convenient than those of statoliths [45]. Additionally, many clear periodic longitudinal light and dark bands have been found in the rostrum sagittal section (RSS) of beaks [46]. The RSS is usually used to estimate age because age estimation from this section is more accurate than that of the LWS [45]. Records of environmental events and life history information are obviously reflected by stress marks [47]. The upper beak is more suitable for age estimations than the lower beak because the lower beak usually exhibits erosion during the feeding period [48]. The erosion of RSS is often caused by feeding behavior; however, the dorsal region of the hood may be used instead to eliminate bias in the estimation [45]. Examination of octopus beak microstructure revealed that each daily increment in the RSS corresponds to one day in life history [49]. The daily RSS increments have also been applied in growth studies of D. gigas and O. bartramii; in these species, the number of beak increments was closely related to the number of statolith increments [39,43,48]. Therefore, the upper beak is considered a tool for estimating the age and describing the growth pattern of cephalopods [20].
In our study, we explored the age and growth pattern of S. oualaniensis found in the waters surrounding the Xisha Islands in the South China Sea with examinations of the upper beak microstructure. This study is the first to use beak microstructure as a tool based on age back-calculation to estimate age, identify hatching groups, and analyze the growth pattern of S. oualaniensis. Growth patterns were evaluated according to the relationships between mantle length (ML) and body weight (BW), as well as between age and ML and BW growth rates. To establish a basis for this species’ fishery biology, ecology, and life history, it is essential to obtain an in-depth understanding of its age and growth pattern in the South China Sea. This study will provide valuable information for age estimation research and the efficient exploitation of S. oualaniensis, which is an important squid resource in the South China Sea.

2. Materials and Methods

2.1. Squid Sampling

A total of 1460 squid samples were randomly caught and collected in the survey by the Chinese fishing vessels Qiong Sanya 72106 and Qiong Sanya 72060 (equipped with light traps and falling nets) in the waters surrounding the Xisha Islands in the South China Sea (12°18′ N–18°46′ N, 110°10′ E–115°58′ E) from January to March and May to August in 2018, 2019, and 2020 (Figure 1). All squid samples were immediately frozen on the ship and dissected in the laboratory.

2.2. Fishery Biology Measurements

Fishery biology data were observed and measured after squid were thawed in the laboratory; mantle length (ML) and body weight (BW) were measured to the nearest 1 mm and 1 g, respectively. Samples were categorized in terms of sex according to the morphological characteristics of the gonads previously established, and 5 age stages were identified (immature: Ⅰ and Ⅱ; maturing: Ⅲ; mature: Ⅳ and Ⅴ) [30,43,50]. The upper and lower beaks were removed from the buccal mass of the head, cleaned, and then preserved with 75% alcohol solution. The following 12 morphological variables, namely, upper hood length (UHL), upper crest length (UCL), upper rostrum length (URL), upper rostrum width (URW), upper lateral wall length (ULWL), upper wing length (UWL), lower hood length (LHL), lower crest length (LCL), lower rostrum length (LRL), lower rostrum width (LRW), lower lateral wall length (LLWL), and lower wing length (LWL), were measured to the nearest 0.1 mm by a Vernier caliper [30,48].

2.3. Beak Processing and Aging

We selected upper beaks from the samples to avoid bias during age estimation as much as possible because lower beaks are more frequently eroded during feeding behavior [48]. All age increments appear on the focal plane of the hood of the beak. We selected the rostrum sagittal section (RSS) instead of the lateral wall surface (LWS) for precise estimation [45]. After cleaning the upper beak with water, the RSS was cut into two unequal pieces by a cutter bar; the larger piece was immobilized and gradually hardened in a plastic mold with cakey epoxy [48]. The focal plane sample was sanded with different types of coarse sandpapers (grit: 120, 600, 1200, and 2000) and polished with smooth sandpaper (2400) with aluminum oxide solution to remove scratches, until the age ring increments on the surface of the sample were clearly observed.
Different parts of the RSS were observed under an Olympus microscope, and images were captured by a charge-coupled device (CCD) at different magnifications (10×, 20×, 40×, 100×, 200×, and 400×). Then, an intact picture was compiled in Photoshop CS 24.0 for the age estimation. The age information of each sample was extracted by two observers. To decrease the bias in age estimation, measurements were considered the effective age when differences in the mean age determined by two observers were less than 10% [30,48]. Given the results of previous studies that compared age estimates collected from cephalopods maintained in artificial feeding conditions and statolith increments with daily beak increments in several species, age and growth patterns can be reliably determined from daily beak increments [20,36,45,46,49]. Additionally, daily beak increments have been successfully used to explore the growth pattern of ommasterphid species in recent years [43,48,51]. Therefore, we explored the growth pattern of S. oualaniensis in the South China Sea near the Xisha Islands based on daily beak RSS increments and back calculations of the hatching dates.

2.4. Data Analysis

An analysis of covariance (ANCOVA) was used to evaluate whether there were sex differences in ML, BW, and URL growth patterns. We established and selected the optimal growth models to quantify the relationships of ML, BW, and URL with age in S. oualaniensis:
Linear function [48,52]:
y = a + b t
Power function [34,48]:
y = a t b
Exponential function [48]:
y = a e b t
Logarithmic function [48]:
y = a ln t + b
where y is ML (mm)/BW (g) at age t; t is age (in days); and a and b are the parameters to be estimated.
The Akaike information criterion (AIC) was used to compare the 4 types of models. The optimal model was determined and selected based upon the minimum AIC value [35]. The absolute daily growth rate (AGR, mm/d or g/d) and instantaneous growth rate (IGR, %/d) of ML and BW were estimated for each 30-day interval. The AGR and IGR were calculated with the following functions [35,53]:
AGR = S 2 − S 1 t 2 − t 1
IGR = ln S 2 − l n S 1 t 2 − t 1
where S1 and S2 represent the mean ML or BW at the beginning t1 and end t2 of the time interval, respectively.
All statistical analyses were calculated with RStudio 3.6.0, SPSS 25.0, and Excel 2016; the pictures were processed in Photoshop 2020.

3. Results

3.1. Microstructure of the Rostrum Sagittal Section (RSS)

The microstructure characteristics of the RSS of S. oualaniensis are shown in Figure 2a. The dark and light bands indicate the daily increments; relatively wide internals are clearly shown on the hood region, and narrower intervals are displayed in the lateral wall region (Figure 2b). It is also easy to identify an inner axis along the boundary between the hood region and lateral wall region, which runs from the rostrum tip to the prong (Figure 2b). Longitudinal increments on the plane of the hood region could be observed more clearly than those on the lateral wall region, which differed in width, patterns, and direction (Figure 2c). The widest internal increments on the RSS were found in the middle region. Each increment in the middle of the inner axis was thicker than the increments at the rostrum tip and prong (Figure 2e). Many distinguishing increments (referred to as the “check” increments) were markedly different from the typical increments (Figure 2e). Additionally, several paler sub-daily increments could be found between the daily increments (Figure 2d). The rostrum tip was often eroded by feeding, preventing the counting of daily increments from the rostrum tip for age estimation (Figure 2e). In terms of the beak pigmentation, the color in the rostrum tip was darker than that in the middle and posterior parts, and the color of the hood region was darker than that of the lateral wall region.

3.2. Mantle Length and Body Weight

The mantle length (ML) of males ranged from 79 to 153 mm (mean ML: 112.13 ± 15.23 mm), with the majority (80.15%) of samples in the range of 91–130 mm. Female ML ranged from 79 to 200 mm (mean ML: 119.67 ± 24.50 mm), with the majority (76.86%) of samples in the range of 91–130 mm (Figure 3). For maturing and mature squids, the ML of males ranged from 86 to 153 mm and that of females ranged from 115 to 198 mm. The MLs of mature males and females mainly ranged from 70 to 150 mm and from 110 to 210 mm, respectively.
The body weight (BW) of males ranged from 17 to 154 g (mean BW: 66.97 ± 29.60 g), with the majority (85.30%) of samples in the range of 0–100 g. Female BW ranged from 18 to 433 g (mean BW: 83.59 ± 68.66 g), with the majority (82.14%) of samples in the range of 0–100 g (Figure 4).

3.3. Age Structure

We successfully estimated the age of 578 beaks (male: 283; female: 295) through examination of daily increments in beak microstructure. Total ages ranged from 97 to 287 days (mean age: 171.29 ± 30.18 days), with the majority (87.32%) of samples in the range of 120–210 days (Figure 5).
Male ages ranged from 97 to 287 days (mean age: 168.37 ± 29.31 days), with the majority (88.24%) of samples in the range of 120–210 days. Female ages ranged from 111 to 280 days (mean age: 174.12 ± 30.85 days), with the majority (72.42%) of samples in the range of 150–240 days (Figure 5).
Maturing and mature males were found in every age range, especially at 120–210 days, and maturing and mature females were found at 120–270 days. Females accounted for less than 50% of the total samples (21.35%) (Figure 6).

3.4. Hatching Date and Hatching Group

The back-calculated hatching dates ranged from May to February. The obvious peak hatching period ranged from October to January of the next year (83.33%).
Specifically, the hatching dates of males ranged from May to February, and those of females ranged from June to February. The peak hatching periods for both males and females ranged from October 2017–2019 to January 2018–2020 (males: 80.15%; females: 86.43%). In this study, most samples belonged to the autumn–winter hatching group (Figure 7).

3.5. Growth Patterns

There were significant sex differences in ML (f = 0.935, p < 0.05) but no sex differences in BW and URL (f = 0.145, p < 0.05 and f = 1.040, p < 0.05, respectively).
The age–ML relationships for males and females were both best described by exponential growth models, as they had the lowest Akaike information criterion (AIC) values. The age–BW relationship was best described by the exponential growth model (Figure 8, Table 1), while the age–URL relationship was fitted with the linear growth model (Figure 8, Table 1). The ML–age, BW–age, and URL–age relationships were as follows:
Male ML–age growth model:
ML   = 70.44 e 0.0029 × a g e   r 2 = 0.5164 ,   n = 283  
Female ML–age growth model:
ML   = 65.27 e 0.0035 × a g e   r 2 = 0.5569 ,   n = 295
BW–age growth model:
BW = 16.74 e 0.0084 × a g e   r 2 = 0.5324 ,   n = 578
URL–age growth model:
URL = 0.0123 × a g e − 265.4640   r 2 = 0.5124 ,   n = 578

3.6. Growth Patterns

The growth rate patterns of ML and BW differed between males and females in this study. For males, the maximum absolute daily growth rate (AGR) was 0.36 mm/day for ML during 180–210 days and 0.88 g/day for BW during 240–270 days (Figure 9a). The maximum instantaneous growth rate (IGR) was 0.30 for ML during 120–150 days and 0.90 for BW during 180–210 days (Figure 10a). For females, the maximum AGR was 0.79 mm/day for ML and 1.3 g/day for BW during 240–270 days (Figure 9b). The maximum IGR was 0.50 for ML from 210–240 days and 1.10 for BW from 240–270 days (Figure 10b).

3.7. Age at Maturity

The male-to-female ratio was 1:1.04. A logistic model was used to describe the relationship between the age at the first mature stage in males and females. Males reached the first mature stage more quickly than females for a given size [30]. Specifically, males reached the first mature stage at 128 days, and females reached the first mature stage at 152 days (Figure 11).

4. Discussion

4.1. Beak Microstructure

The usefulness of the beak for determining fishery biology information for cephalopods has been demonstrated; in particular, the upper beak is used to analyze age and growth patterns [36,43,46,48]. In the present study, clear growth increments comprised of light and dark bands were distributed on both sides of the inner axis of the beak; these growth increments exhibited different widths, patterns, and directions on each side. There were significant differences in the direction and width of growth increments between the crest region and lateral wall region. These two increments were joined at the inner axis and regularly displayed in a V pattern. Even though one increment on the lateral wall surface (LWS) can also reflect one day of life history, the rostrum sagittal section (RSS) of the beak is considered to provide a more precise measurement for estimating the age and growth pattern [20,36,45]. Wider intervals between increments in the crest region provide more accurate age estimations than the overlapped narrow intervals in the lateral wall region, although the lateral wall region has lighter pigmentation that allows increments to be more clearly identified [54]. Each increment width in the hood region reflects the growth rate during the early and later stages of life [45]. Narrow increment widths in the rostrum tip and wider increment widths in the middle to the prong could be easily observed in our RSS samples. These patterns demonstrate a faster growth rate in early life history and slower growth in later life history [45].
During feeding, the rostrum tip usually exhibits substantial erosion, which can bias the accuracy of age estimation. However, this problem can be solved by counting the number of increments from the dorsal edge of the hood [45]. Since sub-daily increments may confuse the count, daily increments should be identified carefully to avoid overestimation of the age of S. oualaniensis. In this study, obvious checks were displayed in the rostrum tip and prong; these increments were easily observed and could be distinguished from typical increments. These checks were mostly displayed at early and later stages of life (Figure 2e) and may be evidence of specific events or environmental events that influenced the growth of squids, including periods of environmental change, specific life history stages, and attacks from predators, especially occurring in early and later life [55]. Environmental factors and stress can produce interruptions and delays in beak growth. Thus, the growth pattern of increments was influenced by both external factors and endogenous rhythms [43,56]. Similar increments and checks have also been found in the beak microstructures of other cephalopods and have been applied to studies on the relationships between growth patterns and environmental factors [43,47,48].

4.2. Age Structure and Hatching Group

According to their daily age and capture date, we back-calculated the hatching dates of the S. oualaniensis collected in this study. We found that the ages ranged from 97 to 287 days (less than 1 year), which is similar to the typical life span of other ommastrephidae species [35,42,43,48,57]. The majority of males were 120 to 210 days old (life span: 4–7 months), and the majority of females were 150 to 240 days old (life span: 5–8 months) (Figure 6a,b). In this species, males reach maturity more quickly than females of the same age [58], a phenomenon also common in other Ommastrephidae species [59,60]. Previous studies have estimated the life span of S. oualaniensis in other areas of the South China Sea with statolith increments; these life spans have mostly been 1–4 months, except for squid collected in the western waters of the Philippines (life span: 95–275 days, 3–9 months) [23,24,26,27,61]. For example, the life span of squid in the Bashi Channel, the eastern tropical Pacific Ocean, the northern Pacific Ocean, and the Bay of Bengal is approximately 2–6 months (53–155 days, 84–168 days, 52–186 days, and 40–120 days, respectively) [22,25,62,63] (Table 2). In addition, squid in the western waters of the Philippines have an estimated life span of 3–9 months (95–275 days) [23]. However, the life span of the giant form of this species that inhabits the northwestern Indian Ocean and Arabian Sea is 4–9 months (120–270 days) [4] and 7 months (203 days), respectively [64] (Table 2). The age structure in our results was approximately half a year, belonging to the dwarf form. This result is also similar to the age structures of forms caught in the Bashi Channel, eastern tropical Pacific Ocean, and western waters of the Philippines [22,23,62,63].
We found that the peak hatching period of males and females occurred from October to January. Therefore, the squid in this study belonged to the autumn–winter hatching group. However, the hatching period of S. oualaniensis in the South China Sea in previous studies lasted throughout the year, with peaks from January to March and from July to August (spring/summer/winter hatching groups) [23,26,27,32,61]. Additionally, summer/autumn hatching groups were described in the Bay of Bengal and northern Pacific Ocean from July to October and from May to September [22,25]. Spring and summer hatching groups of S. oualaniensis in the northwestern Indian Ocean and Arabian Sea have been recorded, but mixed groups (consisting of four seasons) were also observed along the southwestern coast of India and in Taiwanese waters [4,5,58]. However, the peak hatching periods in the South China Sea, Bashi Channel, eastern tropical Pacific Ocean, and southeastern Arabian Sea were distributed in January, February, and December, representing the winter hatching groups [62,63,65,66] (Table 2).
Body size, food availability, and environmental factors can induce obvious changes in the growth patterns and life spans of squids [67]. Lower temperatures, as in cool high-latitude waters, decrease the growth rate and delay squid maturation. Likewise, higher temperatures, as in warm low-latitude waters, facilitate growth and maturation and reduce life spans [67,68]. Because of the wide distribution and complicated population structures of S. oualaniensis, differences in growth patterns and life spans were caused by variation in marine environment factors [1,69]. The spawning season of S. oualaniensis has a long duration (1–3 months); after the last spawning, females keep feeding and growing to build up energy for the next spawning [1,70]. There is also evidence that the hatching dates of S. oualaniensis vary. If more mature females are sampled in a given area, this could indicate that the area serves as a spawning ground [71]. According to our results, we suggest that the waters around the Xisha Islands are not the spawning grounds of the autumn–winter hatching group, because mature squid accounted for less than 50% of the total samples [63,71].
Table
Table 2. Summary data on S. oualaniensis age, peak hatching period and hatching groups in the studied areas.
Table 2. Summary data on S. oualaniensis age, peak hatching period and hatching groups in the studied areas.
Study AreaAge (Days)Peak Hatching PeriodHatching GroupCitation
South China SeaMedium form: 38–126
Dwarf form: 42–71		Medium form: Jan–Mar Dwarf form: MarWinter/spring[26]
South China SeaMedium form: 48–125
Dwarf form: 44–95		Medium form: Jul–Aug; Jan
Dwarf form: Aug; Jan		Summer/winter[61]
South China SeaMedium form: 30–135
Dwarf form: 44–81		Jul–AugSummer[27]
South China SeaMales: 135–259
Females: 95–275 d		-Prolonged spawning season
South China Sea--Winter[24]
Bashi ChannelMales: 62–128
Females: 53–155 d		DecWinter
Eastern tropical Pacific Ocean84–168Jan–FebWinter[62]
Northern Pacific Ocean52–186May–SepSummer/autumn[22]
Bay of BengalMales: 40–114
Females: 63–120		Jul–OctSummer/autumn
Northwestern Indian Ocean120–270Mar–MaySpring[4]
Arabian Sea203MaySummer[64]
Southeastern Arabian Sea-DecWinter[65]
Southwestern India-Medium form: Mar–Apr; Aug–Dec
Dwarf form: Feb–Apr; Aug–Nov		Spring/summer/winter[58]
Taiwanese waters-Jun; Sep; Feb–MarSpring/summer/autumn/winter[5]
This studyMales: 121–210
Females: 151–240		Oct–JanAutumn/winter

4.3. Growth Models, Growth Rates, and Maturity

We found a significant sex difference in the relationship between mantle length (ML) and age. From our results, we concluded that the ML–age and body weight (BW)–age relationships were both optimally described by exponential growth models and that the linear growth model best described the upper rostrum length (URL)–age relationship. Previous studies have used various growth models for S. oualaniensis. For example, logistic growth models were used to fit the ML–age relationships of both sexes in the Bashi Channel and of males in the South China Sea [61,62]. Linear, power, exponential, and logarithmic growth models were also used to fit the ML–age relationship of other forms in different areas [22,26,61,63]. Similarly, logistic, linear, and power growth models were adopted to describe the BW–age relationship of other forms in different areas [22,61,62]. However, the BW–age relationship was fitted by exponential growth models in our study, similar to the relationships in D. gigas and O. bartramii [35,40,48]. We also found that the URL increased with increasing daily age, similar to the pattern in O. bartramii [48]; increases in size might promote the feeding ability of squids later in life history. This pattern of URL–age demonstrated that the beak grew steadily in this life stage, instead of at a fast rate of growth; therefore, the growth model of URL–age was not fitted into exponential or power growth model which represented rapid growth patterns.
These differences in growth models, especially the ML–age relationship, are obviously affected by variation in environmental factors caused by the wide distribution and complex population structures of S. oualaniensis [67,69]. Previous studies have confirmed that the ML–age growth models of D. gigas from different areas show obvious variation as well [35,40]. Based on these studies, we suggest that there is variation in models of S. oualaniensis growth depending on the area. Sexual asynchrony in growth rates was reflected in the ML–age relationship and distribution of maturity stages; we found more maturing and mature males and females in early and late life, respectively. Additionally, we found more females with larger sizes (in terms of ML and BW). From the ML–age relationship, it appears that males and females exhibited similar growth rates before 130 days of age, but the ML of females grew more rapidly after 130 days of age. This finding indicates that this age is the inflection point of transformation in the ML growth pattern between males and females. We also suggest that this age may mark the first maturity stage of S. oualaniensis in the Xisha Islands waters of the South China Sea. In our study, these models could only be used to analyze the growth relationships during the sub-adult and adult stages; they could not be used for the paralarval and juvenile stages because of the absence of samples.
In our study, all females under 120 days old were immature. From our results, males and females reached the first mature stage at 128 days (4 months) and 152 days (5 months), respectively. The age at first maturity in S. oualaniensis from the eastern tropical Pacific Ocean and Bashi Channel (3–4 months) is similar to our results [62,63]. Moreover, similar patterns were found in D. gigas [59,72,73], Illex coindetii [74,75], and Illex argentinus [76]. These results of the first mature stage confirmed that there was sexual asynchrony in the reproduction of males and females. The AGR for male ML was 0.27 mm/day and 0.36 mm/day during 120–150 days and 180–210 days, respectively; the AGR of female ML was 0.32 mm/day and 0.79 mm/day during 150–180 days and 240–270 days, respectively. The AGR of male BW was 0.69 g/day and 0.88 g/day during 180–210 days and 240–270 days, respectively, and that of female ML was 0.60 g/day and 1.30 g/day during 180–210 days and 240–270 days, respectively. The AGR of male ML increased only during 120–210 days and then gradually decreased. The AGR of female ML increased less than males during 120–210 days, but it rapidly increased during 210–270 days. These AGR patterns confirmed the obvious sex differences in the growth of S. oualaniensis. Two similar peaks of AGRs of male and female BW were identified: high values during 180–210 days and 240–270 days and low values during 210–240 days. In terms of the life history of S. oualaniensis, the paralarval stage is suggested to last approximately 60 days (2 months), followed by the juvenile stage after this stage. Compared to the slower growth rates of the head and body, squid in the paralarval stage exhibit higher growth rates for their arms and fins [65]. Therefore, our finding that the AGRs of ML and BW were lower at 120 days old reflects greater hysteresis in the growth rates of the body compared to those of the arm and fins. Additionally, oceanographic features greatly influence the distribution of cephalopod paralarvae [77]. Because of their poor migratory ability, paralarvae prefer to distribute along the continental shelf edge to feed. Upon the rapid development of their fins, improving their migratory ability, squid can migrate from the continental shelf edge into oceanic waters in the juvenile stage [65]. This transition also marks the improved development for feeding ability of its arms, allowing S. oualaniensis to transition among prey items and exhibit cannibalistic behavior in the juvenile stage [65]. After this point, we observed that the AGRs of BW increased greatly during 120–210 days because individuals were able to obtain more food from hunting after changing habitat and prey. In addition, a rapid increase in BW was caused by the development of gonads during 120–210 days. Therefore, we suggested that the paralarval stage finished at approximately 60 days (2 months), followed by the juvenile stage until 120 days of age (4 months). After the juvenile stage, squid enter the sub-adult stage, and this is the age of squid collected in this study.
Males of this species mature faster than females [1]. The reproductive strategy for S. oualaniensis females is intermittent multi-batch spawning, and studies have confirmed that these females can spawn continuously during the long spawning season (1–3 months) [1,70]. During the spawning period, the energy is redistributed to primarily provide for the development of gonads instead of body growth, even though the body continues growing at a lower rate, especially detected at maturity stage for tropical species [1,70,78,79]. We observed a gradual decrease in male ML and BW during 180–210 days. Then, BW obviously increased because the development of male gonads was rapid at 210–240 days, but ML continued to exhibit a gradual decrease. These patterns suggest that the growth of male ML gradually stagnated and that the gonads grew continuously during days 210–240. The AGR of ML differed between males and females. Females continue feeding and growing after one spawning behavior. Continuous feeding during 210–240 days of age provides energy for the next spawning [1]; as larger body size is closely correlated with fecundity; females should continue to grow to increase their fecundity [80]. This growth pattern differed from that of males.

5. Conclusions

In this study, we have summarized all the results of studies on the age and growth patterns of S. oualaniensis. The age and ML ranges in this study indicate that our S. oualaniensis samples belong to the autumn/winter hatching group and dwarf form in the South China Sea. We confirmed that the subadult stage occurred at approximately 120–150 days of age (4–5 months). These results suggest that S. oualaniensis males and females may first mature at 128 days and 152 days (4–5 months), respectively. After first reproduction, squids grow and feed until the next spawning season (from 210–270 days of age, 7–9 months) in the Xisha Islands waters of the South China Sea. Different age structures, growth patterns, and maturation were caused by its complicated population structure. Our results could provide the basic information for only dwarf form of S. oualaniensis in the South China Sea. It is helpful to apply size and age data into assessment management of the dwarf form. However, the growth information could be affected by different sizes and samplings, and also our growth models were not suitably applied to analyze the relationships in early life stage because of the absence of smaller individuals. In the future, we need to expand the sampling area time to obtain, as far as possible, the individuals in the early stage. Meanwhile, exploring and comparing the growth pattern of medium form is also important work for us. These studies would be favorable and helpful for the exploitation and assessment management of resources of S. oualaniensis in the South China Sea.

Author Contributions

Conceptualization, Z.C. and H.L.; methodology, Z.C., H.L.; software, K.L.; formal analysis, Z.C. and K.L.; investigation, K.L.; resources, H.L. and W.L.; data curation, H.L.; writing—original draft preparation, Z.C.; writing—review and editing, H.L. and X.C.; supervision, H.L. and X.C.; project administration, H.L. and W.L.; funding acquisition, H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Key Research and Development Program of China (2019YFD0901402) and National Natural Science Funding of China (NSFC41506184).

Institutional Review Board Statement

The study was conducted according to the guidelines of the Code of Ethics of the University Department of Marine Studies; we only used specimens obtained from the surveys that were already dead.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

Support for four scientific surveys made by “QiongSanyaYu 72106” and “QiongSanyaYu 72060” is gratefully acknowledged. We would like to thank to the teachers and students from the laboratory of Shanghai Ocean University for their work and help in sample collection and biological analysis, and for the valuable comments on the revision of the paper.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Site of investigations and samples for S. oualaniensis.
Figure 1. Site of investigations and samples for S. oualaniensis.
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Figure 2. The microstructure of the S. oualaniensis rostrum sagittal section (RSS). (a) The RSS of the upper beak; (b) microstructure of the RSS; (c) characteristic increments in the hood region and crest region; (d) daily and sub-daily increments; and (e) checks and erosion of the rostrum tip.
Figure 2. The microstructure of the S. oualaniensis rostrum sagittal section (RSS). (a) The RSS of the upper beak; (b) microstructure of the RSS; (c) characteristic increments in the hood region and crest region; (d) daily and sub-daily increments; and (e) checks and erosion of the rostrum tip.
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Figure 3. Distribution of mantle lengths according to maturity stage for S. oualaniensis (a) males and (b) females.
Figure 3. Distribution of mantle lengths according to maturity stage for S. oualaniensis (a) males and (b) females.
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Figure 4. Distribution of body weights in both sexes of S. oualaniensis.
Figure 4. Distribution of body weights in both sexes of S. oualaniensis.
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Figure 5. Age distribution of S. oualaniensis individuals of different sexes.
Figure 5. Age distribution of S. oualaniensis individuals of different sexes.
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Figure 6. Age distribution by maturity stage for S. oualaniensis (a) males and (b) females.
Figure 6. Age distribution by maturity stage for S. oualaniensis (a) males and (b) females.
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Figure 7. Hatching date distribution of S. oualaniensis individuals of different sexes.
Figure 7. Hatching date distribution of S. oualaniensis individuals of different sexes.
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Figure 8. The mantle length–age, body weight–age, and upper rostrum length–age relationships in S. oualaniensis.
Figure 8. The mantle length–age, body weight–age, and upper rostrum length–age relationships in S. oualaniensis.
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Figure 9. Absolute growth rates (AGRs) of mantle length and body weight for S. oualaniensis (a) males and (b) females.
Figure 9. Absolute growth rates (AGRs) of mantle length and body weight for S. oualaniensis (a) males and (b) females.
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Figure 10. Instantaneous growth rates (IGRs) of mantle length and body weight for S. oualaniensis (a) males and (b) females.
Figure 10. Instantaneous growth rates (IGRs) of mantle length and body weight for S. oualaniensis (a) males and (b) females.
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Figure 11. Age at first maturity for S. oualaniensis males (128 d) and females (152 d).
Figure 11. Age at first maturity for S. oualaniensis males (128 d) and females (152 d).
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Table
Table 1. Parameters of the linear, power, exponential and logarithmic growth models fitted to S. oualaniensis mantle length (ML)–age, body weight (BW)–age, and upper rostrum length (URL)–age data.
Table 1. Parameters of the linear, power, exponential and logarithmic growth models fitted to S. oualaniensis mantle length (ML)–age, body weight (BW)–age, and upper rostrum length (URL)–age data.
Growth ModelLinearPowerExponentialLogarithmic
r2AICr2AICr2AICr2AIC
Male-ML0.5154760.78660.3009810.61650.5164760.50680.4990765.3126
Female-ML0.5411844.25010.4769862.56380.5569839.33560.5015855.8462
BW0.51211940.69800.39022002.21600.53241928.97600.47551960.6230
URL0.5124−265.46400.4693−250.12300.4977−265.27400.4827−257.1940
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MDPI and ACS Style

Chen, Z.; Lu, H.; Liu, W.; Liu, K.; Chen, X. Beak Microstructure Estimates of the Age, Growth, and Population Structure of Purpleback Flying Squid (Sthenoteuthis oualaniensis) in the Xisha Islands Waters of the South China Sea. Fishes 2022, 7, 187. https://doi.org/10.3390/fishes7040187

AMA Style

Chen Z, Lu H, Liu W, Liu K, Chen X. Beak Microstructure Estimates of the Age, Growth, and Population Structure of Purpleback Flying Squid (Sthenoteuthis oualaniensis) in the Xisha Islands Waters of the South China Sea. Fishes. 2022; 7(4):187. https://doi.org/10.3390/fishes7040187

Chicago/Turabian Style

Chen, Ziyue, Huajie Lu, Wei Liu, Kai Liu, and Xinjun Chen. 2022. "Beak Microstructure Estimates of the Age, Growth, and Population Structure of Purpleback Flying Squid (Sthenoteuthis oualaniensis) in the Xisha Islands Waters of the South China Sea" Fishes 7, no. 4: 187. https://doi.org/10.3390/fishes7040187

APA Style

Chen, Z., Lu, H., Liu, W., Liu, K., & Chen, X. (2022). Beak Microstructure Estimates of the Age, Growth, and Population Structure of Purpleback Flying Squid (Sthenoteuthis oualaniensis) in the Xisha Islands Waters of the South China Sea. Fishes, 7(4), 187. https://doi.org/10.3390/fishes7040187

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