Changes of group construction accompanying with growth and maturity in blue-barred parrotfish (Scarus ghobban), and influences of the fishing targeting the immature group to the stock

Regional Studies in Marine Science 7 (2016) 32–42

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Changes of group construction accompanying with growth and maturity in blue-barred parrotfish (Scarus ghobban), and influences of the fishing targeting the immature group to the stock Akihiko Ebisawa a,b,∗ , Kiyoaki Kanashiro a,c , Itaru Ohta a , Masato Uehara a , Hiroyuki Nakamura a,d a

Okinawa Prefectural Fisheries Research and Extension Center, 1528 Kiyan, Itoman, Okinawa, 901-0354, Japan

b

Yaeyama branch station of the Okinawa Prefectural Fisheries Research and Extension Center, 828-2 Kabira, Ishigaki, Okinawa, 907-0453, Japan

c

2-208-19 Syuri Ishimine-cho, Naha, Okinawa, 903-0804, Japan

d

Fisheries Section, Okinawa Prefecture Government, 1-2-2 Izumizaki, Naha, Okinawa, 900-8570, Japan

highlights • • • • •

We revealed the reproduction, growth and group construction of Scarus ghobban. All individuals belonging in groups composed by only female were immature year round. Females belonging to sexually mixed groups matured year round. We collected the body size of the species in commercial catches for 19 years long. Cohort size, SSB and %SPR were estimated for it stock evaluation.

article

info

Article history: Received 16 April 2015 Received in revised form 19 January 2016 Accepted 30 January 2016 Available online 3 May 2016 Keywords: Blue-barred parrotfish Scarus ghobban Life history variable Reproduction All female group Cohort size fluctuation %SPR

abstract Reproductive biology and growth characteristics of the Blue-barred Parrotfish (Scarus ghobban) were revealed for the purpose of the stock evaluation. Based on both of these findings and body size data in commercial catches accumulated during 19 years, age components in the catch and cohort size were estimated via virtual population analysis for the northern area of the Okinawa Islands population. The population was composed of two separate groups, one of which was a all female group whose members’ ovaries were immature year-round, and the other was a male and female mixed group, of which the majority of females were mature year-round. Fish were mainly up to 3 years of age in the all female group and older than 2 years in the sexually mixed group. Although the majority of females in the sexually mixed group matured year-round, a portion of the rest of the immature females showed evidence of prior maturation, suggesting that each female in the group experienced periods of spawning and resting repeatedly without a seasonal pattern. The fishery at the studied area has mostly targeted the all female group to be about 85% of total numbers; thus, the fishing pressure to mature females was revealed to be very small. However, the VPA highlighted that the most individuals up to 3 years of age belonging to the all female group died either by fishing or naturally. Thus, a few individuals attained sexual maturity in each cohort. Extremely high fishing pressure against the mature age groups shortly added during the study period, thereafter spawning stock biomass (SSB) and %SPR rapidly decreased, the latter to the level of about 20%, beyonding the biological reference point. Cohort sizes during the years 1994–2012 have fluctuated in magnitude twice, and those of latter half period, coincide to both SSB and %SPR decreases, were smaller than those of earlier half but were stable without any trend of decreases. © 2016 Elsevier B.V. All rights reserved.

∗ Corresponding author at: Yaeyama branch station of the Okinawa Prefectural Fisheries Research and Extension Center, 828-2 Kabira, Ishigaki, Okinawa, 9070453, Japan. Tel.: +81 0980 88 2255; fax: +81 0980 88 2114. E-mail address: [email protected] (A. Ebisawa). http://dx.doi.org/10.1016/j.rsma.2016.01.012 2352-4855/© 2016 Elsevier B.V. All rights reserved.

A. Ebisawa et al. / Regional Studies in Marine Science 7 (2016) 32–42

1. Introduction Parrotfishes from the family Labridae have been utilized as important food resources in tropical or subtropical regions including Okinawa, southwestern Japan. The main fishing gear for parrotfishes in Okinawa up to the middle of 1970s was mostly net gear such as gill net, drive-in nets, and spear fishing without using a hookah or scuba. After the introduction of night spear fishing using a hookah/scuba at late 1970s, the catch volume of parrotfishes increased drastically (Anonymous, 1973, 1975, 1981, 1986, 1993, 1999, 2001, 2005). Okinawan fishermen were able to use all of the Okinawa fishing grounds without any restriction in choice before 1980. However, due to overfishing, the increased catch was only temporary. Many fishermen, researchers and persons in the fisheries administration began to think about the need for stock management at a time of rapid decreases in fish resources. In about 1980, Okinawa fishing grounds were divided into 27 blocks and spear fishermen with a hookah or scuba could only use the restricted fishing ground block next to their residence. Although annual rings were thought to be unformed on otoliths, on scales, and on vertebrates in fishes distributed in tropical to subtropical waters, the formation in these fishes was revealed and the growths of many tropical fishes was estimated (Loubens, 1978, 1980). After that, biological information aimed at enabling stock evaluation started to accumulate on commercially important species in Okinawa waters. Biological research was carried out from 1990 to 1992 on blue-barred parrotfish (Scarus ghobban), a highly valuable parrotfish species, and fragments in the reproductive characteristics were revealed (Ebisawa et al., 1999). According to the research, the initial-phase female group inhabits the inner ward of relatively large bay areas on Okinawa Island, and all members in the group are immature annually. Terminal-phase males are never captured in the area, but small number are captured in areas facing the open sea, away from the bay areas, or in the deep, outer-mouth parts of the bays. Initial-phase females captured with terminal-phase males showed sexual maturation without specific seasonality. However, entire aspects of their reproductive biology have not yet been revealed due to the insufficient number of mature specimens in the sample. These aspects indicated the complexity of their reproductive characteristics in the population. From the view point of their fishery, the majority of catches are conducted using nighttime spear fishing, gill nets, and, occasionally, set nets, mainly in the inner-ward of relatively large bay areas on Okinawa Island. Accordingly, the commercial catch of the species in the Okinawa area is composed mostly of young, immature initialphase individuals, with very few mature females and terminalphase individuals (Ebisawa et al., 1999). This finding indicated to us that many mature females and terminal-phase males may inhabit areas where fishing is seldom conducted. However, the evaluation was deferred due to the insufficient amount of both biological information and accumulated statistics. Fisheries in coral reef waters are often small scale but there are many kinds of fishing gear targeting numerous kinds of species. Fish components in catch differ significantly in the choice of fishing grounds of the day even by the same fishermen using the same fishing gear. Scales of fishing gear operation also differ such as operated by individual (spear-fishing), or by a few persons (gill nets), or by more than ten members (drive-in nets) for targeting the same resources in Okinawa. Therefore, the introduction of the concept of fishing effort into analysis seems to be difficult, as well as the standardization of the fishing effort between different fishing gear. Thus, stock evaluation using catch volume and fishing effort only is unsuitable for fisheries where various kinds of fishing gear and different scales in the operation of the gear co-exist within the same resource. Estimation of the survival rate based on age

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components in commercial catch or fishery independent surveys may enable stock evaluation after dividing the survival rate into fishing and natural mortalities, although the evaluation is only one aspect since it never gives us the trends of both the recruitment and the biomass. Virtual population analysis (VPA) is a valid tool for this situation, although it requires relatively long periods of statistics such as the amount of catch in each age class, or alternatively the body size component, the catch volume and the growth of the species. Most of the commercial catch in Okinawa is sold by auction conducted by a fishery cooperative to which the fishermen belong. When the body sizes and commercial values are similar, different species within the same group such as grouper, emperor, snapper, and parrotfish are often combined, weighed, and sold within the individual fishermen’s catch. Therefore, the body size and catch volume of the target species, which are essential for stock evaluation, have to be collected at these auction markets. Catch statistics started to be gathered at late 1980s by assuming the analysis via VPA at major fish auction markets in the Okinawa prefecture. Coral reef fisheries highly dependent on protogynous hermaphrodite fishes such as Epinephlinae, Lethrinidae, and Labridae, usually catch larger body size individuals selectively due to their higher commercial value, or fishing gear selectivity, or management plan. Biological, ecological, and evolutional effects of sizeselective or sex-selective fisheries have gradually been revealed in the last decade (Alonze and Mangel, 2004; Fenberg and Roy, 2008; Kendall and Quinn, 2013). This selective fishing of young, immature blue-barred parrotfish in Okinawa is the opposite situation to the usual coral reef fishery targeting protogynous hermaphrodite fishes, and thus it is quite meaningful to reveal the effect of these fisheries on the resource. The goals of this study were (1) to reveal the complex reproductive biology of S. ghobban by adding new specimens of IP and TP individuals captured simultaneously, (2) to re-analyze its life history parameters, such as growth, longevity, sexual maturity, and sexuality, in relation to age, (3) to estimate the amount of catch at each age based on the life history parameters and statistics accumulated to date, (4) to estimate the trends of number recruited and biomass, and (5) to evaluate the current specific fishery of the species in which young immature individuals are mostly targeted.

2. Materials and methods 2.1. Biological data analysis Specimens were collected monthly from April 1990 to November 1992 and August 1998 to March 2002 by purchasing commercial catches at the Nago Fishery Cooperative, where most commercial catches from the area north of Okinawa Islands (Fig. 1) are gathered to sell at auction. When purchasing specimens, we asked fishermen about the fishing gear used as well as location and depth of capture. We also recorded whether initial- and terminalphase fish were captured simultaneously or not by the fishermen. Specimens were kept on ice during transportation to the laboratory, where fork length (LF ) and standard length (LS ) to the nearest 0.1 cm and body weight (WB ) to the nearest 1.0 g were measured and body color (initial phase [IP] or terminal phase [TP]) was recorded. The sex was determined based on the external appearance of the gonads, which were weighed to the nearest 0.1 g (WG ) and fixed in Bouin solution. The gonad somatic index (GSI) was calculated as 100 × WG /WB . Sagittal otoliths were extracted from each specimen and stored in paper envelopes in dry conditions until otolith processing.

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A. Ebisawa et al. / Regional Studies in Marine Science 7 (2016) 32–42

Fig. 1. Map of the north area of Okinawa Island, where the most of the Blue-barred parrotfish (Scarus ghobban) specimens were collected. Depths shallower than 30 m are densely shaded, and those between 30 and 50 m are lightly shaded. Major habitats of all female group which is composed by only initial phase individuals at the catch are indicated red and the locations of sexually mixed group collected in the specimens are indicated blue. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

2.1.1. Stage classification in ovarian maturity A piece of gonad about 5 mm thick was dissected from a randomly chosen position in the middle 70% of the longitudinal direction of either lobe after 1 or 2 d of organ fixation. For histological preparation, all of the gonad pieces were embedded in paraffin wax, sectioned into 6-µm thick slices, and stained with Mayer’s haematoxylin and eosin. The stage of ovarian development was determined from the most advanced stage of the oocyte in the ovary based on histological observation. The stages of oocyte development followed the classification of Yamamoto and Yamazaki (1956) (i.e., the chromatin nucleus, early peri-nucleolus [EPN], late peri-nucleolus [LPN], yolk vesicle [YV], primary yolk globule, secondary yolk globule, tertiary yolk globule, migratory nucleus, pre-maturation, maturation, ripe, and atretic stages [At]). Maturity stages were combined as follows: the primary and secondary yolk globule stages to the early yolk globule stage (EYG), and, with this correspondence, the tertiary yolk globule stage to the late yolk globule stage (LYG) and from the migratory nucleus to the ripe stage to the hydrated stage (HY). In ovaries from the late yolk globule to hydrated stages, the presence of post-ovulatory follicles (POFs) was recorded. Presence of muscle and connective tissue bundles (MCTBs) (Shapiro et al., 1993) and brown bodies (BBs) (Sadovy and Shapiro, 1987) was also confirmed. Ovarian maturity stage lower than YV is determined to be immature and that higher than EYG to be mature in the analysis. 2.1.2. Otolith processing and aging protocol Each otolith was embedded in epoxy resin, transversely sectioned about 450 µm thick with the core included, mounted on a slide glass in medium (Eukitt: O. Kindler), and covered with a cover glass. Reflected light observations with a binocular microscope revealed translucent and opaque zones alternating around the core (Fig. 2). The opaque zones were counted as growth rings; the observer was unaware of the specimen details (i.e., body size, month collected, and sex). Whether the outermost edges were opaque or translucent was also determined. Otolith pictures of the first observation were recorded using a Polaroid PDMCIe with 1600 × 1200 pixels and 24-bit color depth. Second and third observations were performed at intervals longer than one week by the same reader based on the otolith picture without

Fig. 2. Sectioned otolith picture of Blue-barred parrotfish (Scarus ghobban), indicating five obvious opaque zones shown by red allows and 6th very thin opaque zone at the edge. Collected on July 30th 1998 with 38.0-cm-LF female individual. Scale bar is 1 mm. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

providing the reader the previous data. When the number of growth rings matched all three readings, no further readings were performed; when the number of two readings coincided, one additional reading was performed. When a total of three readings agreed, the number of growth rings was considered to be determined; if three concurrent readings were not obtained, the otolith was excluded from further analysis. However, otoliths that had more than 10 growth rings but no agreement in three readings were included in later analyses using a median number of four readings. Since the spawning period extends year-round and the period of growth-ring development occurs during summer, details of which are shown in the result sections, the period of age addition was determined to be July–December, the same as the period of growth-ring formation. The age of specimens collected from July to December with a new growth ring formed on the otolith edge is determined by the number of growth rings present, but for those collected during the same period that lack a newly formed growth ring, the age is given as the number of growth rings plus one. For specimens collected from January to June, the age is given as the number of growth rings minus 0.5. Growth parameters in the von Bertalanffy growth equation were estimated by nonlinear regression (SPSS for Windows, release 7.5.2, SPSS) for the age and LF datasets of the specimens. 2.1.3. Group category in specimens Specimens were classified into two groups: one that was collected from the catches of only IP individuals (all female group) and one collected from both IP and TP individuals

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Fig. 3. Monthly changes of sectioned otolith edge condition of Blue-barred parrotfish (Scarus ghobban) collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. Open and black bars indicate translucent and opaque edge, respectively. Number in each bar indicates sample size.

captured simultaneously (sexually mixed group). In addition to these two groups, a few individuals belonging to ‘sampled solo individuals’ and ‘sampled without group information’, which have no information to classify into either two groups, were obtained. Analyses of reproductive biology and estimation of growth equations were performed separately for the all female group, females in the sexually mixed group (mixed females), and males. The relationships of ovarian maturation or sex ratios with respect to body size/age were estimated solely within the sexually mixed group. 2.2. Demographic analysis The LF to the nearest to 1.0 cm below the length were measured and body color recorded of all S. ghobban at the Nago Fishery Cooperative from July 1994 to June 2013 twice a week each week. The measurements were recorded separately by each fisherman, allowing for classification of these data into either the all female or sexually mixed group. Length data were summed from January to June and from July to December in the three sexually categorized groups: all female, females in sexually mixed group (mixed females), and males. Age components were estimated as follows: lengths of each age of the three groups were premised to be normally distributed around the calculated length of their growth equations; standard deviations of the normal distribution, which were obtained by the nonlinear regression estimating growth parameters, were considered to be unique in all age groups; and age components in the commercial catch were calculated by Hasselblad iteration method (Hasselblad, 1966). Annual age components in commercial catches were summed through the three sexually categorized groups and two periods (July–December and January–June). We evaluate the stock condition via VPA. VPA is calculated based only on age components in catch, and is thus free from the fishing effort. However, the estimated population numbers of the last few years are severely affected by the values of terminal F . Because the frequency of measurements was constant through the study period and the number of fishermen who caught S. ghobban was stable in recent years, terminal F was chosen in order to coincide the trends of both the estimated population numbers and number of individuals measured by the market survey. Demographic numbers were calculated using Pope’s approximation (Pope, 1972), with the natural mortality coefficient being 0.3, following methods of Hoenig (1983) based on the maximum age in our specimens of 14 years, using the number of individuals we measured at the market survey. Therefore, the demographic number is relative value of the whole population; thus, hereafter we use relative demographic number instead. Cohort size was determined by the relative demographic number at 1 year of age for each cohort, and mortal factors and numbers of

Fig. 4. Monthly changes in ovarian maturity stage of Blue-barred parrotfish (Scarus ghobban) collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. (a), all female group which is composed by only initial phase individuals at the catch; (b), females in the sexually mixed group which is composed by both initial and terminal phase individuals at the catch; and (c), number of mature ovaries with or without post-ovulatory follicles (POF) in the sexually mixed group. Number in each bar in (a) and in (b) indicate sample size. EPN—early perinucleolus stage, LPN—late peri-nucleolus stage, YV—yolk vesicle stage, EYG—early yolk globule stage, LYG—late yolk globule stage, Hy—hydrated stage, At—atretic stage, and Tr—transitional from ovary to testis.

each cohort were calculated. In order to judge the current fishery status of the species in the studied area, spawning stock biomass (SSB) and %SPR (spawner per recruit), the rates of decreases in SSB from the initial SSB were calculated. At the calculation of SSB, a rate between all female and sexually mixed groups in each age (mixing rate at age i: MRi) that is not available in the present study is necessary. Therefore, two sets of imaginary determined these values listed in Table 3 and all other necessary parameters obtained in the biological data analysis section were used for the calculation in SSB. Initial SSB (SSB without fishing) was calculated using average cohort size from 1994 to 2000 with the age components changing only M (0.3), and all parameters in Table 3 with two set of MRi patterns. Datasets combined with a SSB value in a year and the cohort size of the next year from 1994 to 2012 were employed so that evaluate the SSB—recruitment relationship. 3. Results 3.1. Biological data analysis A total of 302 specimens comprising 254 IP and 48 TP individuals was obtained (Table 1). Among the 254 IP specimens, 249 specimens had an ovary, three specimens had transitional gonads, and two specimens could not be sexed due to abnormally small gonads. All 48 TP specimens had secondary testes. Body sizes in the all female group ranged from 23.9 to 42.5 cm LF ; the LF of females in the sexually mixed group ranged from 28.1 to 57.0 cm, and the LF of males was 37.9–62.3 cm.

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A. Ebisawa et al. / Regional Studies in Marine Science 7 (2016) 32–42 Table 1 Number of blue-barred parrot fish (Scarus ghobban) specimens in each sexual and sampling categories collected in the northern area of Okinawa Island, in southwestern Japan from April 1990 to March 2002. Specimens were classified into two groups: one that was collected from the catches of only female individuals (all female) and one collected from both male and female individuals captured simultaneously (sexually mixed). Sampled solo individual and no group information at the capture were also added in the sampling types. Sexual category

Color phase

Sampling type All female

Sexually mixed

Sampled sole

No group information

Total

Female Sex unidentified Transitional Male

Initial Initial Initial Terminal

128 1

109 1 3 41

3

9

5

2

249 2 3 48

reading occurrences due to a disagreement among the first three, 62 specimens had total agreement with three readings and thus were included in analyses. Four specimens who had more than 10 growth zones but were not obtained from three instances of agreement were given median numbers and thus were included in analyses. Altogether, among a total of 276 obtained otolith specimens, the number of growth zones was determined for 203 specimens, and the remaining 73 specimens were excluded from the age-based analysis. The oldest female specimen was 14.5 years old with a body size of 42.2 cm LF , and the oldest male was 13.5 years old with a 47.5-cm LF . The von Bertalanffy growth equation using all sexual groups was computed as LF t = 48.5(1 − e−0.389(t +1.1) ). 3.1.2. Seasonal changes in gonadal maturation

Fig. 5. Monthly transitions of average gonad somatic index (GSI) values (small horizontal line) of Blue-barred parrotfish (Scarus ghobban) collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. (a), all female group which is composed by only initial phase individuals at the catch; (b), immature females the maturity stage of which is lower than yolk vesicle stage in the sexually mixed group which is composed by both initial and terminal phase individuals at the catch; (c), mature females the maturity stage of which is higher than early yolk globule stage in the sexually mixed group; and (d), testes. Vertical lines indicate ±SD.

3.1.1. Period of growth-ring formation and number of otoliths successfully aged Number of translucent-edge otoliths dominated from November to May, and, conversely, opaque-edge otoliths dominated from July to October (Fig. 3). Thus, the opaque band was determined to be formed during the summer to autumn seasons. Among the 302 specimens, pairs of otoliths for 26 specimens were completely broken at capture (spear-fishing) and thus were excluded. There was agreement concerning the number of growth zones determined during the first three readings for 137 specimens. After the four

Almost all ovaries in the all female group were in the EPN stage except for one individual obtained in March that was in the LPN stage. No ovary later than the YV stage appeared in the group throughout the year (Fig. 4(a)). Monthly average GSIs were also all smaller values (less than 0.2%), with a slight peak from March to May (Fig. 5(a)). Age and body size ranges of the all female group were 1–4 years old and 23–43 cm LF , respectively (Fig. 6(a), (e)). Although no female specimens in the sexually mixed group were obtained in April, May, and September, HY-stage ovaries were obtained in all the other months except at December in this group (Fig. 4(b)). However, some females in this group were immature, such as those in the EPN, LPN, and YV stages. Average GSIs of immature females in this group ranged from 0.1% to 0.3%, with the highest values in June (Fig. 5(b)). Many of these immature ovaries (ca. 43%) had some characteristics of prior maturation, such as possessing MCTBs and BBs, with relatively wide cross-sections of ovaries compared to those in the all female group (Fig. 7). Although average GSIs of mature females were the highest in June at about 4.0%, no obvious seasonal changes were observed (Fig. 5(c)). The POFs were observed in mature ovaries in January, February, June, November, and December (Fig. 4(c)). Age and body size ranges of immature females in the sexually mixed group were 2–6 years old and 29–57 cm LF , respectively (Fig. 6(b), (f)), and those of mature females were 2–14 years old and 29–49 cm LF , respectively (Fig. 6(c), (g)). The relationships between age/body size and ovarian maturation (OM), including currently mature and post-mature individuals in the sexually mixed group, were obtained as follows: OM = (1 + e0.679−0.599Age )−1 and OM = (1 + e4.15−0.143LF )−1 (Fig. 8). Average GSIs of males exhibited no seasonal changes with smaller values (less than 0.2%) (Fig. 5(d)). Age and body size ranges of males were 2–13.5 years old and 39–63 cm LF , respectively (Fig. 6(d), (h)). Thus far, these results suggest that all individuals in the all female group were immature year-round and that some portion of females in the sexually mixed group were mature year-round, with no seasonality for spawning.

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Fig. 6. Age and length components of Blue-barred parrotfish (Scarus ghobban) collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. only initial phase individuals at the catch; (b) and (f), immature females the maturity stage of which is lower than yolk vesicle stage in the sexually mixed group which is composed by both initial and terminal phase individuals at the catch; (c) and (g), mature female the maturity stage of which is higher than early yolk globule stage in the sexually mixed group; (d) and (h), male.

between age/body size and sex ratio (RS) were calculated as RS = 1−(1+e2.60−0.393age )−1 after the exclusion of the 14-year-old’s data point and RS = 1 −(1 + e12.9−0.285LF )−1 , respectively. However, the indicated relationships between RS and age and RS and body size were not for the entire population, because the ratio between the all female and sexually mixed groups is still unknown.

Fig. 7. Histological appearance of an immature ovary of Blue-barred parrotfish (Scarus ghobban) belonging to the sexually mixed group showing evidence of prior maturation by muscle and connective tissue bundle (MCTB) (black arrow) and brown bodies (Bbs) (red arrows) located outside of MCTB. Measurements: 41.9cm-LF and 3.44-g-WG , collected on November 13th, 1998. Scale bar is 500 µm. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

3.1.3. Transitional style from ovary to testis Three hermaphroditic gonad body sizes ranging from 37.3 to 45.9 cm LF were obtained within the sexually mixed group. Transition from ovary to testis was categorized as ‘undelimited type 2’ following from Sadovy and Shapiro (1987), likewise other scarid and labrid species (Candi et al., 2004; Warner, 1975; Robertson et al., 1982). In the relationship between age and sex ratio, though the ratios shifted to females 2–3 years of age, at which numbers of specimens were numerous, and decreased to zero in those 10 years of age, the ratios between 4 and 9 years of age were rather invariant, at about 50% (Fig. 9(a)). In addition, the oldest individual was female. On the contrary, sex ratios sharply decreased with the increase of body size in the sexually mixed group (Fig. 9(b)). The relationships

3.1.4. Growth patterns with respect to sexual group and sex Average body sizes of same-age individuals among the all female group, females in the sexually mixed group, and males were larger in decreasing order of males, females in the sexually mixed group, and the all female group (Fig. 10). Growth equations in the three groups are listed in Table 2. Relationships between LS and LF and WB and LF were obtained as follows: LS = 0.86LF − 1.01(r 2 = 0.99) (LF and LS in cm)

WB = 0.01105L3F .16 (r 2 = 0.98) (WB in g; LF in cm).

3.2. Demographic analysis 3.2.1. Cohort size and mortality factors during the study period Body sizes of a total of 42,436 S. ghobban, consisting of 36,014 individuals in the all female group, 3559 females in the sexually mixed group, and 2863 males, were measured at the Nago Fishery Cooperative auction market during 1994–2013. The number of individuals measured annually (July to the following June) was largest (about 3300) during 1995–1996 and was lowest (about 1300) during 2005–2006 (Fig. 11), following the obvious trend that these numbers were higher in the earlier half and lower in the latter half of the observed periods. Total numbers of females in the sexually mixed group and males were relatively larger during

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Fig. 8. Plots of ovarian maturity rate with age (a) and size (LF ) (b) in the sexually mixed group of Blue-barred parrotfish (Scarus ghobban) collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. Ovary is determined to be mature not only the stage being higher than early yolk globule, but also showing the evidence of prior maturation in immature ovary such as the presence of muscle and connective tissue bundle (MCTB) or brown body (BB).

Fig. 9. Plots of sex ratios with age (a) and size (LF ) (b) of Blue-barred parrotfish (Scarus ghobban) in the sexually mixed group, which is composed by both initial and terminal phase individuals at the catch, collected from April 1990 to March 2002 at north of Okinawa Island, southwestern Japan. × mark in A at the age 14 was omitted in the regression estimation.

Table 2 Growth parameters of the von Bertalanffy growth equation in each sexual and group category of blue-barred parrot fish (Scarus ghobban) collected in the northern area of Okinawa Island, in southwestern Japan from April 1990 to March 2002. Specimens were classified into two groups: one that was collected from the catches of only female individuals (all-female group) and one collected from both male and female individuals captured simultaneously (sexually mixed group). Mean square is the value obtained by the estimation of growth parameters by non-linear regression and used to convert from length frequency data to age frequency for each group and sexual category. Group and sexual type

L

k

t0

All-female group Female in sexually mixed group Male

36.0 42.3 55.7

2.07 0.68 0.37

−0.73 −0.80

0.60

n

Mean square

r2

Remarks

86 82 23

9.2 23.8 30.7

0.16 0.17 0.25

Specimens younger than 8.0 years of age used

Table 3 Life history variables employed for calculating Spawning Stock Biomass (SSB), and the percent of Spawner per Recruit (%SPR). Mri values in this table are virtually determined so as to calculate SSB, whereas other parameters were obtained in the biological section of this study. Formula SSB = Σ ni ∗ MRi ∗ RSi ∗ OMi ∗ WB i (i is from 1 to 15) %SPR = SSB/SSBF =0 Symbol Ni: Population number in i years of age Mri: Rate of the sexually mixed group in i years of age pattern a: MR1 = 0.1, MR2 = 0.7, MR3 = 0.95, MR4 = 0.98, MR5 ∼= 1.0 pattern b: MR1 = 0.05, MR2 = 0.2, MR3 = 0.6, MR4 = 0.95, MR5 ∼= 1.0 Rsi: Sex ratio of the sexually mixed group in i years of age Rsi = 1 − (1 + e2.60−0.39i )−1 Omi: Ovarian maturity rate of female in the sexually mixed group in i years of age Omi = (1 + e0.679−0.599i )−1 WB i: Body weight of female in the sexually mixed group in i years of age WB i = 1.105 × 10−5 × LF i3.16 LF i = 42.3 × (1 − e−0.68(i+0.73) )

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Table 4 Weights (kg) of the Blue-barred parrotfish (Scarus ghobban) in each sexual and group category measured at the surveyed fish auction market by constant sampling rate through the whole years. Yeara

1994

1995

1996

1997

1998

1999

2000

2001

2002

2003

All female Mixed female Male Total

1227 120 274 1622

1627 403 590 2619

1453 212 392 2056

1537 124 238 1899

1794 185 276 2255

1506 219 365 2089

1739 244 365 2348

1611 224 461 2296

1240 742 919 2901

1203 370 621 2194

Yeara

2004

2005

2006

2007

2008

2009

2010

2011

2012

All female Mixed female Male Total

742 190 334 1265

720 144 394 1257

850 179 396 1425

1055 136 261 1452

1720 198 271 2189

958 125 255 1337

876 157 344 1377

957 97 232 1287

1075 226 348 1649

a

From the July of the indicated year to the next June.

Fig. 10. Growth curves and plots of age and average LF in 0.5-years of age interval groups of Blue-barred parrotfish (Scarus ghobban) in male and two types of female group: one that was collected from the catches of only initial phase individuals (all female group; closed square and dashed line) and one collected from both initial and terminal phase individuals captured simultaneously (sexually mixed group; female, cross and broken line; male, asterisk and continuous line). Vertical line on symbol indicate ±SD. Symbols without vertical lines indicate a single sample.

1995–1996 and 2002–2004, although the percentages of the totals were small. Percentage of females in the sexually mixed catch was highest (about 66%) during 1998–1999 and the lowest (about 45%) during 2004–2005, with an average of 55% throughout all years. Annual total weight calculated from body sizes was the highest at about 2.9t in 2002 and was the lowest at about 1.3t in 2004, 2005, and 2009 although the trend of the changes was approximately same as that of the number of individuals (Table 4). The relative demographic number estimated by VPA was the largest at about 6100 for the 1999 cohort and was the smallest at about 2800 for the 2012 cohort (Fig. 12). Cohort sizes from 1994 to 2002 varied, ranging from 3700 to 6100, but they were stable at lower levels (less than 3600) from 2003 to 2012, except for the 2007 cohort. Both fishing mortality in the all female group and natural mortality up to age 3 were the largest mortality factors, attesting to about 79%–88% of total deaths for each cohort throughout all years. Fishing mortalities to ages older than six increased drastically and attained the maximum among all year classes in year 2002, however, those to two years of age were usually the highest for all other years (Fig. 13). 3.2.2. Transitions of %SPR, and SSB—recruitment relationship %SPR decreased suddenly from 2002 to 2004 after the stable transitions from 1994 to 2001 in both patterns a and b, respectively (Fig. 14). The smallest values in %SPR observed in 2004 in pattern a and b were 22%, and 18%, respectively. %SPR have started to increase after 2005 and attained the levels of 2002 in 2012, the levels of that were 30% and 26% in pattern a and b, respectively.

Fig. 11. Transition of the number of Blue-barred parrotfish (Scarus ghobban) (bar) and the rate of initial-phase individuals in the sexually mixed catch (line) measured at the Nago Fishery Cooperative where the most of the commercial catch at the north area of the Okinawa Island are gathered to sell auction. All S. ghobban landed at the day were measured from July 1994 to June 2013 in a frequency of twice a week every week, distinguishing each fisherman’s catch separately with classifying the body color either initial-phase only (all female group) or both initial- and terminalphases mixed (mixed female) in the catch. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Positive correlations between SSBs and recruitments (cohort sizes) were observed and regression coefficients were significant in both patterns a and b (p < 0.01) (Fig. 15). Chronological transitions in SSB and recruitment plots were confined within a limited area until 2001. Although the SSB’s continual decrease toward 2004 was observed, cohort size were rather stable between 2000 and 2012 at about 3000–3500 individuals except for 2007 cohort which was about 1.4 times larger than the stabled levels. 4. Discussion 4.1. Biological analysis The biological characteristics of the species discovered in this research are summarized as follows. The opaque zone formed in the otolith was more obscure than in other parrotfish species. Although the species exhibits protogynous hermaphroditism, the maximum age of both sexes being about 15 years old indicates that not all females change into male. A very small number of females change into males before sexual maturation. The body sizes of males are larger than those of females in the same age groups. These characteristics are nothing special and are often observed in

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Fig. 12. Transition of the cohort sizes (number of individuals at one year of age) of Blue-barred parrotfish (Scarus ghobban) estimated by VPA as well as mortal factors and numbers with respect to sexual and group category of each cohort at the north area of the Okinawa Island population. Blue, fishing mortality at all female group stage; orange, fishing mortality of female at the sexually mixed group stage; yellow, fishing mortality at male; green, natural morality up to three years of age; brown, natural mortality after four years of age; light blue, number surviving at the end of June 2013. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 13. Changes of the fishing mortality to each age group of Blue-barred parrotfish (Scarus ghobban) estimated by VPA at the north area of the Okinawa Island population during the study period.

Fig. 14. Changes of %SPR (Spawning Per Recruit) during the study period assuming under two types of shift pattern on age from all female group to sexually mixed group.

other parrotfish species (Robertson and Warner, 1978; Choat et al., 1996; Grandcourt, 2002; Taylor and Choat, 2014). On the other hand, the following two characteristics seem to be unique for bluebarred parrotfish: One is the existence of an annually immature allfemale group, and the other is that females in the sexually mixed group spawn without any seasonality.

Fig. 15. Relationship between SSB (Spawning stock biomass) and cohort size at the next year, assuming under the two types of shift pattern on age from all female group to sexually mixed group. Numbers in the figure indicate cohort year. Because cohort sizes in pattern a and pattern b are the same, the difference of the two patterns are fundamentally in those of SSB.

Many fish family are known to have different habitats between juvenile and adult stages (Gillanders et al., 2003). In protogynous hermaphrodite fishes which have different habitats between juvenile and adult stages, all individuals found at their juvenile habitat seem to be immature female, thus they are the same as all female group in the present study. Many females remaining extremely large body size at their juvenile habitat seem to be the specific characteristics in the blue-barred parrotfish. In addition, there were many immature females who had matured previously in the sexually mixed group. These two findings suggest that female sexual maturity is controlled not simply by attaining a certain size and age during a certain season but also by other factors, such as the males participation, or hierarchical order within the social group (Kuwamura, 1984), or necessity for a long resting period for subsequent spawning. A small (240 mm LF ), young (1 year of age), and ripe female individual and a larger (350 mm LF ) and older (3 years of age) resting female individual co-existed in the Solomon population (Sabetian, 2010), which may indicate the presence of a long resting period for their spawning. A larger number of immature individuals in the largest body size class under seasonally sampled specimens appeared in the Taiwan population (Shao, 2002), which suggests the presence of both the all female group and the long resting period for spawning, similar to the Okinawa population. When female maturity is not controlled by a hierarchical order within their social group, the rate of numbers of mature and

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immature individuals theoretically corresponds to the rate of the period between spawning and resting under the assumption that there is no recruitment of immature individuals into the group. Age components in the all female group were dominated mostly by ages younger than 3 with very few numbers of age 4. Using individuals older than 4 years of age, the percent of mature individuals in the sexually mixed group accounted for about 74%, corresponding to three months of a resting period each year. There are many fish species reported to skip spawning during their spawning season (Secor, 2007; Rideout and Tomkiewicz, 2011; Skjæraasen et al., 2012), mainly due to nutrient conditions of individuals (Rideout et al., 2006). The long resting period observed in S. ghobban in this study may relate to the balance of energy for both consumption for reproduction and accumulation for subsequent reproduction. 4.2. Demographic analysis The relative demographic numbers in this study were calculated based on the direct numbers of body size measurements. Sampling rates of size measurements of about 33% throughout the entire study period enabled the conversion to whole numbers being caught in the area by multiplying numbers by three. The majority of the commercial catches of the species were from the all female group, with very few from the sexually mixed group. Thus, commercial catches of the sexually mature females were very sparse. These facts might infer that the fishing of the species caused fewer impacts on the conservational use of the stock on the surface. However, the mortality number obtained by VPA showed that about 80% of each cohort was dead either by fishing at the all female group stage or by natural causes up to age 3. Hence, very few individuals were thought to survive until the stage of full sexual maturation. Shift of individuals from all female group to sexually mixed group occurred younger in pattern a than in pattern b, thus SSB values were estimated larger in pattern a. %SPRs were the lowest values at about 22% and 18% in pattern a and in pattern b, respectively in 2004. These values were lower than the default biological reference point at about 30% (Mace and Sissenwine, 1993). The sudden decrease in %SPR after 2002 seems to be the result of the extreme larger fishing mortality to older individuals in 2002, however, the large fishing mortality to those ages did not continue to the successive years. Since the cohort sizes after 2004 being stable, %SPR began to increase favorably after 2004. Two plausible reasons of the stable cohort size whilst the decreases of %SPR are suggested: a—replenishment of egg, fry or juvenile from the outside of survey area has been occurred; b—%SPR has been still higher than the biological reference point of the species. Major habitat of the species is not only the survey area but also extending to the adjoining Kin- and Nakagusuku-Bay areas. At these bay areas, major target of the species were mostly all female group with much smaller amounts of TP males than the survey area (Ebisawa and Nakamura, 2010). Therefore, mature females also seem to have been rarely caught at these bay areas. Since the demographic survey at these bay areas has not been conducted before 2008, it was uncertain that the similar intensive increases of the fishing pressure toward older age group might also occurred at these bay areas or not. Because the habitat of the spawnable adult of the species extended to these bay areas, one of a cause of the stable cohort sizes observed at the surveyed area after 2002 might be in the a. The biological reference point in %SPR in the species is to be obtained empirically, accumulation of the demographic data covering the whole habitat of the species at the Okinawa Island area should be necessary. It is worth for attention that increases of fishing pressure toward older fishes may decrease the SSB dramatically in fishery

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where young individuals are mainly harvested. Although it is not determined to be the cause of the reduced cohort sizes by the decrease of %SPR, continual monitoring for the population dynamics of the species will be necessary. 5. Conclusion This research was conducted in order to reveal the reproductive characteristics of Blue-barred parrotfish Scarus ghobban which have still yet unknown such as the existence of both annually immature female group and annually mature group co-exist at around Okinawa waters, and to reveal the impact of fishery where young immature individuals are mostly caught, by selecting the study area at the north area of the Okinawa Island. The annually immature individuals are all female and are mainly composed younger than three years of age inhabiting innerward of relatively large bay area. The other mature groups inhabit deeper zone of the bays or the open sea adjacent to the bays being mixed with both sex. Individuals belonging to annually immature group are thought to join mature group in accordance with their growth. These all female immature groups are thought to be formed by the results of the combination of both the habitat difference between juvenile and adult and the protogynous hermaphroditism in its sexuality. Within the male and female mixed group, females having mature ovary appeared year round without any seasonality, however, females having resting ovary coexisted year round as well. Both facts strongly suggest that each female in the group spawn (nine month) and rest (three month) repeatedly with her own schedule. Commercial fishery in Okinawa are targeting the all female immature group, thus fishing pressure to sexually mixed mature group have been very small. However, VPA revealed that approximately 80% of each cohort have died up to three years of age, before the full sexual maturity by either fishing or naturally. During the 19 years of the study period, heavy fishing pressure toward mature and older age group was observed at one year, after that the SSB and %SPR suddenly decreased and the latter to the levels about 20%, below the biological reference point at about 30%. The heavy fishing pressure to the older aged group lasted only the year and the numbers recruited into the stock thereafter were stable, thus SSB and % SPR recovered favorably. The phenomena we observed suggests following two ideas; one is the possibility of replenishment of egg, fry, or juveniles have been occurred to study area from not only the study area but also the outside: the other one is the level of the biological reference point of the species is tolerable lower than the default point at about 30% in %SPR. On the other side, SSB and %SPR are suggested to be suddenly decreased by even the short-term increases of fishing pressure toward older and mature fish in the fishery where young and immature fishes being mostly targeted. Acknowledgments This research was partially supported by the ‘‘Morphometric Survey of Important Fishery Resources in Seas Adjacent to the Okinawa Islands’’ and ‘‘Research on Biological Characters of Dominant Species of Coral Reefs around the Okinawa Islands’’ both being commissioned by the Japan Fisheries Agency. Many fishermen working in the area north of Okinawa Island provided all the necessary information concerning the specimens at capture. The staff members of Nago Fishery Cooperative encouraged us at the long period of the body size measurements for the demographic survey. We gratefully acknowledge all of these persons.

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