Reproductive biology and growth of the deep-water shrimp Solenocera melantho in the East China Sea.
Li, Hui Yu
Cheng, Jia Hua
Li, Sheng Fa
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: August, 2012 Source Volume: 31 Source Issue: 3|
|Topic:||Event Code: 310 Science & research|
|Product:||Product Code: 0913080 Shrimp NAICS Code: 114112 Shellfish Fishing SIC Code: 0913 Shellfish|
|Geographic:||Geographic Scope: China Geographic Code: 9CHIN China|
ABSTRACT Reproductive biology, size at sexual maturity, and growth
of the deep-water shrimp Solenocera melantho were studied in the East
China Sea. The spawning season continues from July to November, with
peaks during late August to November. Size at sexual maturity
([CL.sub.50]), determined from the proportions of ovigerous females and
of females with maturing ovaries, was estimated at 28.7 mm. The sex
ratio was close to 1:1, with males slightly more abundant than females.
Parameters of growth were estimated by the modified von Bertalanffy
growth function, incorporating seasonal variation in growth. Females
grew faster and reached a larger size at age than males (K = 1.14/y and
[L.sub.[infinity]] = 46.75 mm in carapace length for females, and K =
1.26/y and [L.sub.[infinity]] = 33.6 mm in carapace length for males).
Maximum life span was estimated at 2.43 y for females and 2.20 y for
males. The S. melantho population in the East China Sea has different
values of asymptotic length and growth coefficients in comparison with
other local populations of this species.
KEY WORDS: deep-water shrimp, Solenocera melantho, reproduction, size at sexual maturity, growth
Shrimp of the genus Solenocera mostly inhabit offshore waters ranging from the midcontinental shelf to the ocean floor with depths of 60-1,000+ m (Holthuis 1980, Perez & Kenslery 1997). Currently, 14 species of Solenocera have been reported in the world, and 9 species occur in the China Sea (Holthuis 1980, Liu & Zhong 1986, Perez & Kenslery 1997, Song et al. 2006). As a result of the lack of availability of specimens, little attention has been given to the study of its fishery, its biology, and its ecology (Chalayondeja & Tanoue 1971, Sunkumaran 1978, Demestre & Abello 1993, Ohtomi & Irieda 1997, Ohtomi et al. 1998, Dineshbabu & Manissery 2008, Villalobos-Rojas & Wehrtmann 2011).
The deep-water mud shrimp, Solenocera melantho De Man, 1907, belonging to the Solenoceridae family, is widely distributed from the Indo-West Pacific region to the Pacific coast of southern Japan (Ohtomi & Irieda 1997, Perez & Kenslery 1997, Ohtomi et al. 1998, Xue & Song 2004, Oh et al. 2005). Off the coast of the East China Sea and the Yellow Sea, the deep-water mud shrimp is one of the most important decapod crustacean species in terms of total number of individuals and biomass, and prefers soft (mud and sandy-mud) bottoms at a depth of 60-100 m (Li et al. 2009, Xue & Song 2004). In China, the deep-water mud shrimp has been exploited commercially since the mid 1980s, and has developed into one of the main target species for beam trawls and bottom trawls (Xue & Song 2004).
Information about the reproductive biology of a species is one of the most important aspects in evaluating the harvesting strategies of exploited populations. Studies of the reproductive biology of S. melantho have been reported in Kagoshima Bay, Japan, and Geomun Island, Korea, and suggest that the reproductive characteristics of this species have geographical differences (Ohtomi & Irieda 1997, Ohtomi et al. 1998, Oh et al. 2005). In the East China Sea, brief studies on distribution and biological characteristics of S. melantho have been conducted by Xue and Song (2004); however, detailed studies on the reproductive biology of the species are evidently lacking. This article examines the reproductive biology through determination of the spawning season, the sex ratio, size at sexual maturity, and growth.
MATERIALS AND METHODS
Specimens were collected from the East China Sea by a 35-m beam trawl with 25.0-mm mesh cod end (Fig. 1). The sampling was conducted once or twice a month from June 2009 to May 2010.
Samples were fixed for 24 h in 10% neutral formalin and then transferred to 70% ethanol for storage. Sex was determined by the presence of the petasma for males or the thelycum for females (Ohtomi et al. 1998). Carapace length (CL; from the posterior margin of the orbit to the middorsal posterior edge of the carapace) and the total length (TL; from the posterior margin of the orbit to the median margin of the telson) were measured using vernier calipers (TESA-CAL IP67) to the nearest 0.1 mm. In a representative subsample, the CL of each specimen was also measured. Shrimp were weighed with an electric balance (AWH-SIH) to the neared 0.01 g.
The CL-weight relationships were based on the regression BW = a[CL.sub.b], where BW is the body weight in grams, CL is the carapace length in millimeters, and a and b are the constants for each sex separately. Comparison of the slopes (b) of the length-weight regression by sex was made by ANCOVA.
For each female, the whole gonads were removed and the ovary stages were identified according to illustrations of size and color of the ovary by Ohtomi et al. (1998). Three main stages of development were observed: (1) undeveloped (ovary transparent, oocyte oogonium), (2) developing (ovary cream, oocyte early, middle, or late nucleolus) and (3) early ripe or ripe (ovary yellow or dark yellow, yolk granule or premature). After blotting to remove excess water, the wet weight of ripe ovaries was determined by weighing to the nearest 0.001 g using an electronic balance (OHAUS). The gonadosomatic index (GSI) was calculated as follows:
GSI = 100 X GW/BW (1)
where GW is wet gonadal weight in grams and BW is wet body weight in grams.
[FIGURE 1 OMITTED]
Size at sexual maturity was determined by the proportion of females with early ripe or ripe ovaries. The proportion of mature females by size was fitted to a logistic equation:
P = 1/(1 + exp(a + bCL)) (2)
where P is the predicted mature proportion, and a and b are the estimated coefficients of the logistic equation. Parameters were estimated by correlation analysis of P and CL after linearization. Size at sexual maturity ([CL.sub.50]), corresponding to a proportion of 0.5 sexually mature individuals, was estimated as the negative of the ratio of the coefficients ([CL.sub.50] = -a/b) by substituting P = 0.5 into the equation.
Length-frequency distributions by sex were constructed using 2-mm intervals of CL. Growth was described using the modified von Bertalanffy growth function (VBGF) (Pauly & Gaschu 1979, Pauly & David 1981).
[L.sub.t] = [L.sub.[infinity]] x [1 - exp(-k(t - [t.sub.0]) - (CK/2[pi]) x sin(2[pi] x (t - [t.sub.s])))] (3)
where [L.sub.[infinity]] is the theoretical maximum individual size that the species would reach if it lived indefinitely, K is the intrinsic growth rate, [t.sub.0] is the age at length 0, C is the amplitude of seasonal growth oscillation, [t.sub.s] is the age at the beginning of growth oscillation, and WP (= [t.sub.s] + 0.5) is the time of year when growth is slowest.
WP ranges between 0 and 1. Values close to 0 or 1 indicate a deceleration down in growth during the winter months; values close to 0.5 indicate that the deceleration in growth takes place during the summer. Calso ranges between 0 and 1. For values of C close to 0, the equation reduces exactly to the von Bertalanffy equation without seasonality; for values close to 1, the amplitude of the seasonality factor is maximal.
[t.sub.max] (the corresponding age of [L.sub.max] or maximum longevity) can be the obtained from the VBGF, and calculated for females and males:
[t.sub.max] = (2.996/k) + [t.sub.0]
Because the parameters [L.sub.[infinity]] and k are correlated inversely, the growth performance index ([phi]) was calculated to enable comparison of growth rates between male and female S. melantho (Pauly & Munro 1984):
[phi] = 2log[L.sub.[infinity]] + log k
Taking into account the inverse correlation between the two parameters of [L.sub.[infinity]] and k, the growth performance index is more robust than either [L.sub.[infinity]] or k individually. Thus, it fulfills the requirement for a simple single parameter for comparison of growth.
All specimens of S. melantho were sexed, and proportions of females and males in the samples taken monthly are shown in Figure 2. Of the 1,801 specimens, 49.5% were identified as females and 50.5% as males. A chi-square showed that the number between females and males was not different throughout the sampling period ([chi square] = 13.85, P > 0.2), although the sex ratio varied month to month.
The sex ratio of S. melantho varied with CL classes; females attain a greater size than males. The percentage of females was highest for more than 25 mm in CL whereas in males it was highest between 15 mm in CL and 25 mm in CL. A chi-square test showed the number of females and males was no different when CL was smaller than 15 mm; however, it was significantly different when CL was larger than 15 mm (Table 1).
Gonad Maturation and GSI
Ovary condition was divided into 3 stages, and females with immature ovaries occurred throughout the year--mainly from December to the next June (Fig. 3). Ovarian development began in July, and females with maturing or ripe ovaries were noted from August to November (Fig. 3).
[FIGURE 2 OMITTED]
All 888 females with different ovarian states were examined to estimate GSI. The ovary became larger and GSI increased with ovarian maturity. GSI began to increase in July, and reached its maximum in October, then began to decrease in December and remained low until the next June (Figs. 3 and 4). Mature females with a GSI greater than 4 appeared from August to November, which indicates that the spawning season of S. melantho continues from July to December and the peak is during August to November. ANOVA showed that there was a significant difference in mean GSI between months (F = 28.53, P < 0.001). Turkey-HSD multiple comparisons revealed that the mean GSI of the breeding season (August to November) was significantly different with that of other months (Table 1).
Size at Onset of Sexual Maturity)
The 931 female S. melantho used in the analysis ranged from a CL of 13.9-41.1 mm. The minimum CL of mature females was found to be 22.1 mm. The relationship between CL and the proportion of sexually mature females by 2-mm-CL size class was calculated by fitting a logistic function to the size-specific maturity data:
P = 1/(1 + exp(7.84 - 0.24CL)) ([r.sup.2] = 0.89, P < 0.001)
From this, the estimated size for 50% sexual maturity for females was 28.7 mm in CL (Fig. 5).
[FIGURE 3 OMITTED]
[FIGURE 4 OMITTED]
CL-BW and CL-TL Relationships
Using the pooled data sets, a single regression equation, covering the entire sampling period, was produced for each sex separately. All 3 regressions (females, males, and combined sexes) of BW on CL showed that the BW was a significantly positive allometric function of CL (Table 2). Females exhibited higher weight values than males during all study periods. ANCOVA showed a significant difference in the regression slopes between sexes (F = 95.61, P < 0.0001).
For conversion of CL into TL, the TL-CL relationship was as follows:
Female: TL = 2.9278CL + 17.373 (n = 708, [R.sup.2] = 0.89, P < 0.0001)
Male: TL = 2.542CL + 28.215 (n = 741, [R.sup.2] = 0.87, P < 0.0001)
Differences in the regression slopes between sexes were not significant (ANCOVA: F = 3.743, P > 0.05).
Between June 2009 and May 2010, 2,009 specimens (1,029 females and 980 males) were collected. The CL of S. melantho ranged from 9.1-41.0 mm for females and 10.5-31.2 mm for males. The monthly length-frequency distributions are illustrated separately for each sex in Figure 6. Statistically significant differences (ANOVA) between the mean CL of both sexes per month were found (females: F = 103.3, P < 0.001; males: F = 47.1, P < 0.001).
[FIGURE 5 OMITTED]
In females, the sample in June 2009 was essentially unimodal, with a peak at a CL of about 20-24 mm. The mode lasted to December with increasing CL, then young recruits first appeared in January 2010 with a modal mean CL of 14-18 mm. Males displayed a similar modal progression.
The VBGF parameters, estimated by ELEFAN for each sex, are summarized in Table 3. The analysis of modal progression for each sex separately showed that females had lower K values but reached larger sizes at age than males. This was indicated by the growth performance indices ([phi]'): 3.28 for females and 3.115 for males. The growth curve showed a seasonal oscillation in growth (C) of 58% for females and 45% for males. The maximum life span ([t.sub.max]) of S. melantho was estimated to be 2.43 y for females and 2.20 y for males.
[FIGURE 6 OMITTED]
Few biological studies on deep-water shrimp such as Solenocera are reported in comparison with inshore shrimps. This is obviously attributed to the difficulty in collecting samples covering a large size range in deep waters for a long period of time. In the current study, a large number of specimens off the coast of the East China Sea over a period of 1 y were collected, and the biological study of S. melantho, including the sex ratio, spawning season, size at sexual maturity, CL-weight relationship, and growth, was conducted.
In the current study, the sex ratio of S. melantho was not substantially different from 1:1, with a little larger value in the main spawning season (August to November) than that in other months. This is consistent with previous studies of penaeid shrimp (Ohtomi & Irieda 1997, Cha et al. 2001, Cha et al. 2004a, Cha et al. 2004b, Oh et al. 2005, Dineshbabu & Manissery 2008), and is considered to be a benefit for the species' life history strategies by raising reproduction. Although the sex ratio for the total population of S. melantho was close to 1, it showed varied markedly with CL class, which has been reported in Solenoceridae (Baelde 1992, Ohtomi & Irieda 1997, Oh et al. 2005, Dineshbabu & Manissery 2008). Possible factors affecting the sex ratio included longevity, differential migration, differential mortality, differential growth rate between females and males, and sex reversal pattern (Wenner 1972, Baelde 1992). However, sex change was not observed in the current study.
The study of the breeding season in penaeid shrimps can facilitate our understanding of the adaptive strategies and reproductive potential of a species related to its environment (Dall et al. 1990, Gillett 2008). And different reproductive strategies, including a continuous breeding season throughout the year for tropical species and a seasonal breeding period for subtropical species, have been reported in solenocerid shrimp (Gueguen 1998, Ohtomi et al. 1998, Ohtomi & Matsuoka 1998, Oh et al. 2005, Dineshbabu & Manissery 2008). The breeding season of S. melantho was reported by several researchers in different areas. Ohtomi et al. (1998) found that the species inhabiting Kagoshima Bay, Japan, had a breeding season from June to December, with a peak during October to November. Oh et al. (2005) estimated the breeding season of the same species in Geomun Island, Korea, from August to early November, with a peak in October to early November. The current study clearly showed that S. melantho had a single breeding season from August to November, as reflected by the ovaries of mature females and monthly GSI values. All of the previously mentioned studies on S. melantho indicated that, regardless of where it was found, it exhibited 1 spawning peak per year, and the peak spawning season tended to be longer in lower latitudes (Table 4). The bottom temperature in this study fluctuated from 12.8-21.9[degrees]C, and the mean value is a little higher than that in Kagoshima Bay and Geomun Island. This difference may lead to the variance in length of spawning season, as discussed in previous studies (Dall et al. 1990, Hossanin & Ohtomi 2008). However, more data are needed to understand more completely the influence of factors controlling the variance in spawning of S. melantho.
Size at sexual maturity is very important in fisheries regulations, determining the size limits with the aim to protect immature individuals from exploitation and to ensure an adequate number of reproductively active animals to support the total reproductive output, or egg production, of the populations (Lizarraga-Cubedo, 2008). This study determined that the size at sexual maturity in female S. melantho was a CL of 28.7 mm (estimated as 101.4 mm in TL). The value was much larger than that reported in previous studies (Ohtomi et al. 1998, Oh et al. 2005) (Table 4). In penaeid shrimp, 2 methods--including histological characteristics and ovary maturation--are used to estimate the size at sexual maturity (Ohtomi et al. 1998, Cha et al. 2001, Oh et al. 2005, Dineshbabu & Manissery 2008). Ohtomi et al. (1998) considered the CL of the smallest mature female with stage-III ovaries among the specimens as the size at sexual maturity. The difference in criteria may result in the difference in determining the size at sexual maturity. Geographical variations may be another influence determining the size at sexual maturity, which is well documented for other decapods, including Jasus edwardsii (Annala et al. 2010, Gardner et al. 2006), Marsupenaeus japonicas (Ohtomi et al. 2003), and Penaeus indicus (Jayawardane et al. 2002). The variations could be the result of differences in population abundance and structure because of variations in the characteristics of catchability of fishing gears used on different grounds, or differences in growth rates between areas.
In the current study, negative allometry was observed in the CL-BW relationship in both males and females, with a faster growth rate in females than males. This result agrees with many previous studies (Oh & Hartnoll 2004, Josileen 2011, Ozcan & Katagan 2011). Penaeid shrimp typically show an allometric coefficient (b) close to 3. The value in this study was a little less than that in S. melantho (Ohtomi & Irieda 1997), and larger than that in Solenocera membranacea (Ozcan & Katagan 2011). However, our result was within the limits of 2.5-3.5 reported by Froese (2006).
This study suggests that the first recruitment of S. melantho in the East China Sea occurs once a year in winter (January), and similar patterns were reported in earlier studies of the same species in Kagoshima Bay populations (Ohtomi & Irieda 1997). The von Bertalanffy growth models fit to the data of S. melantho, as indicated from the high score function ([R.sub.n]). The estimated values of K (1.14 for females and 1.26 for males) and [L.sub.[infinity]] are different from that of a population in Kagoshima Bay (Ohtomi & Irieda 1997) and Geomun Island (Oh et al. 2005) (Table 3). However, the maximum age is similar between different populations of the same species. The K values decreased within the range (0.39-1.6) reported by Pauly and Munro (1984) for a number of penaeid shrimp. The variations in growth parameter were suggested to be attributed to sea water temperature and fishing pressure (Taylor 1958, Oh et al. 1999). The growth of performance index ([phi]') is preferred for growth comparison between species and sexes of a species rather than comparisons of K and [L.sub.[infinity]] because of the inherently negative correlation between these 2 parameters (Pauly & Munro 1984). Our [phi]' values, which changed a little in different areas, were closely consistent with those in different populations (Table 3). The comparison of [phi]' between sexes indicates that the growth rate is larger and reached a larger size for females than for males, with relatively low growth in both sexes during the spawning season. The coincidence of slow growth and maturation with spawning periods in females indicates that metabolic costs are associated with reproductive activities, when shrimp cease molting during the spawning period. Similar patterns of growth are found in previous studies in penaeid shrimp (Baelde 1994, Ohtomi & Irieda 1997, Ohtomi & Matsuoka 1998, Cha et al. 2001, Lopez-Martinez et al. 2005, Oh et al. 2005, Hossain & Ohtomi 2008); however, this pattern did not appear to be generalized in decapod crustaceans (Hartnoll 1982).
We thank Professor Li Ping Yan for helpful advice and suggestions in field sampling. This work was supported by special research funds for the national nonprofit institutes (East China Sea Fisheries Research Institute; no. 2007M17), the Chinese Ministry of Agriculture Assessment of Marine Fisheries Resources Program, and the Ministry of Science and Technology Public Project (2008-2010).
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HUI YU LI, * JIA HUA CHENG AND SHENG FA LI
Key and Open Laboratory of East China Sea & Oceanic Fishery Resources Exploitation and Utilization, Ministo, of Agriculture, East China Sea Fisheries Research Institute, CAFS, Shanghai 200090, China
* Corresponding author. E-mail: firstname.lastname@example.org
TABLE 1. Sex ratio of S. melantho in different carapace length (CL) classes. CL Classes (mm) Female (%) Male (%) Total (%) P <11 0.07 0.08 0.07 >0.05 11-15 3.40 2.59 3.02 >0.05 15/1/20 22.00 37.19 29.12 <0.001 20/1/25 36.29 55.03 45.08 <0.001 25/1/30 28.66 4.95 17.55 <0.05 30/1/35 7.63 0.16 4.13 <0.05 >35 1.94 0 1.03 1.00 TABLE 2. Regression analysis of body weight (BW) on carapace length (CL) in Solenocera melantho. n Equations Female 933 BW = 0.0012[CL.sup.2.7418] Male 907 BW = 0.0028[CL.sup.2.4816] Pooled 1,840 BW = 0.0017[CL.sup.2.6327] [+ or -] Slope [r.sup.2] P Female [+ or -]0.002 0.96 <0.0001 Male [+ or -]0.002 0.89 <0.0001 Pooled [+ or -]0.002 0.92 <0.0001 TABLE 3. Parameter estimation of ELEFAN analysis of length--frequency data for females and males. Parameters Females Males Pooled [L.sub.[infinity]] 46.75 33.6 39.00 K 1.14 1.26 0.93 C 0.58 0.45 0.47 WP 1.00 0.90 0.98 [phi]' 3.28 3.15 3.16 [t.sub.max] 2.43 2.20 Ohtomi and Oh et al. Irieda (1997) (2005) Parameters Female Male Female Male [L.sub.[infinity]] 45.76 33.09 51.731 27.499 K 0.777 0.857 1.109 1.848 C -- -- 0.343 0.145 WP -- -- 0.716 1.000 [phi]' -- -- 3.291 3.145 [t.sub.max] 37 mo >2 [L.sub.[infinity]], asymptotic length (in millimeters); K, growth coefficient (per year); C, amplitude of growth oscillation; WP, winter point; [phi], growth performance index; [t.sub.max], maximum life span (y). TABLE 4. Summary of the spawning season and the size of S. melantho at onset of sexual maturity (SOM) in various areas. Peak in Spawning Areas Latitude Season Kagoshima Bay, Japan 32-33[degrees]00' N October-November Geomun Island, Korea 34[degrees]00' N October November East China Sea, China 31[degrees]00' N August-November Areas SOM (CL, mm) Source Kagoshima Bay, Japan 25.3 Ohtomi and Irieda (1994) Geomun Island, Korea 20.65 Oh et al. (2005) East China Sea, China 28.7 Current study CL, carapace length.
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