Environ Biol Fish (2010) 88:253–260 DOI 10.1007/s10641-010-9636-7
Reproductive biology of Bigeye Tuna, Thunnus obesus, (Scombridae) in the eastern and central tropical Pacific Ocean Guoping Zhu & Xiaojie Dai & Liuxiong Xu & Yingqi Zhou
Received: 18 June 2009 / Accepted: 8 February 2010 / Published online: 9 March 2010 # Springer Science+Business Media B.V. 2010
Abstract Understanding the reproductive potential of any species is of great importance for resource assessment and management. We studied the reproductive biology of Bigeye Tuna, Thunnus obesus, based on 1283 samples taken from the Chinese longline vessels in the eastern and central Tropical Pacific Ocean during February through November 2006. The female-male ratio was 1.0 : 1.5 and males were predominant in all length classes except for the length class of 166–170 cm (fork length). Males dominated in sizes larger than 171 cm, all specimens of 192 cm or larger were males. The main spawning period of Bigeye Tuna was between March and November. Gonadosomatic rates of males were larger than those of females. Statistically, female and male Bigeye Tuna had no significant reproductive seasonality. The observed minimum length at sexual maturity for female Bigeye Tuna was 94 cm. Length G. Zhu : X. Dai : L. Xu : Y. Zhou The Key Laboratory of Shanghai Education Commission for Oceanic Fisheries Resources Exploitation, College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China G. Zhu (*) : X. Dai : L. Xu : Y. Zhou The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China e-mail:
[email protected]
at 50% sexual maturity of female Bigeye Tuna was estimated at 107.8 cm, and maturation rate was 0.106 cm−1. The results derived in this study provide the information critical to our understanding of key life history parameters of Bigeye Tuna in tropic Pacific Ocean. Keywords Reproduction . Bigeye tuna . Sex ratio . Maturity . Spawning . Sex development . Pacific Ocean
Introduction Bigeye Tuna (Thunnus obesus Lowe, 1839) is a commercially important species inhabiting the warm waters of the Atlantic, Indian, and Pacific Oceans (Collette and Nauen 1983; Collette et al. 2001). They are found across the entire Pacific between northern Japan and the North Island of New Zealand in the west and from 40°N to 30°S in the east (Calkins 1980; Matsumoto 1998). Adult Bigeye Tuna are caught mainly by longlines, but substantial numbers of juveniles are taken by purse seines (Sun et al. 2001). Understanding and quantifying the reproductive potential of any species is of great importance for resource assessment and management (Schaefer 1998). Information on maturity gives important knowledge about reproduction for initial management and enables separation of estimates of abun-
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dance into values representing the immature and mature populations (Kolding and Giordano 2002; Schaefer et al. 2005). There are still large uncertainties about the population biology of Bigeye Tuna (Schaefer 2001; Schaefer et al. 2005), which is being overfished with no conservation measures in place to ensure its sustainability (ISSF 2009). This raised some concerns about the potential impact on the resource given recent increases in juvenile Bigeye Tuna catches (Schaefer et al. 2005). Only limited studies have been done on the reproductive biology for Bigeye Tuna in the Pacific Ocean recently. Yuen (1955) studied the maturity and fecundity of Bigeye Tuna for the central equatorial, western equatorial and Hawaiian areas of the Pacific. Kikawa (1953, 1957, 1961, 1966) studied the length at maturity, spawning period and spawning area for Pacific Bigeye Tuna. Kume (1969a, b) also conducted research on the spawning season, sex ratio, and spawning area for the Pacific Bigeye Tuna. Kume and Joseph (1966) studied the sex ratio and maturity at length for the eastern Pacific Bigeye Tuna. Nikaido et al. (1991) studied the spawning time and frequency of Bigeye Tuna captured in the waters off Java (12°–14°S, 109°–115°E) and offshore of southwestern Hawaii (11°–13°N, 163°–176° W), respectively. Schaefer et al. (2005) studied the reproductive biology of Bigeye Tuna in the eastern and central Pacific Ocean (15°N–15°S, 80°W–175° W) with their data collected from the purse seine fishery in the Eastern Pacific Ocean (EPO) (n=1986) and a Japanese longline research vessel in the EPO and central Pacific Ocean (n=124). Sun et al. (2006) studied the reproductive biology of Bigeye Tuna in the Western and Central Pacific Ocean. Except for the paper presented by Schaefer et al. (2005), the reproductive biology for the eastern and central Tropical Pacific (ECTP) Bigeye Tuna has not been studied since 1970s. The objective of this paper is to evaluate the reproductive biology of Bigeye Tuna using the samples collected by the Chinese tuna longline vessels operated in the ECTPO. We estimate: (1) sex ratios; (2) length at sexual maturity; (3) spawning season; (4) sexual development; and (5) spawning seasonality, which are critical parameters in determining the population dynamics of Bigeye Tuna.
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Materials and methods Field sampling Gonads were collected from Bigeye Tuna of different sizes randomly sampled by the Chinese Scientific Observers aboard longline vessels in the ECTPO during February through November 2006 (Fig. 1). A total of 1283 gonads were sampled. We have randomly sampled 10 individuals in each set and all individuals caught if the number was less than 10. Fork length (FL) was measured with calipers to the nearest centimeter and body weight was measured with electronic balance to the nearest 1 kg. The gonads were removed and weighed to the nearest gram with an electronic balance. For all sets in which gonad samples were collected, capture locations, dates, and times were recorded. Data analysis Sex ratios Sex ratio was calculated as the proportion of males by month and by size class (5 cm). Chi-square tests were used to test for any significant difference in sex ratio among months and among sizes. To examine the possibility of an interaction between body size and month, we examined the sex ratio data using a generalized linear model (GLM), the response (sex
155°W 150°W 145°W 140°W 135°W 130°W 5°N
5°N
0°S
0°S
5°S
5°S
10°S
10°S 0
250
500km
155°W 150°W 145°W 140°W 135°W 130°W Fig. 1 Sampling stations of this study
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ratio, using a probit link function) was modeled as a function of month, body size and the interaction effect between body size and month. We used Akaike’s information criterion (AIC) (Akaike 1973) for the selection of significant terms in the models to determine which variables best predict sex ratio. The S-PLUS (Mathsoft 2000) software package, Version 6.0, was used to fit the GLM model and to obtain the AIC values. Sex development based on visual observations The ovary (testis) of Bigeye Tuna is considered asynchronous because oocytes (sperm) in various developmental stages are present in the ovary (testis) simultaneously (Wallace and Selman 1981). For each ovary (testis), the oocytes (sperm) in the most-developed mode were classified as: (1) I— Undeveloped stage; (2) II—Early developing stage; (3) III—Later developing stage; (4) IV—Mature stage; (5) V—Spawned stage; and (6) VI—Spent stage (Sun et al. 2006).
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Spawning season Reproductive seasonality was determined by monthly inspection of the development stages and by monthly Gonadosomatic Rate (GSR) for each sex. Gonadosomatic rate: The GSR was calculated as (Nootmorn 2004): GSR ¼
W 104 FL3
where W = gonad weight (g); FL = fork length (cm). We used the t-test to analyze the difference of GSR by month and by size with 5 cm fork length interval between female and male Bigeye Tuna. Temporal trends in GSR were investigated using periodic regression (Batschelet 1981). To test the null hypothesis that there was no cyclic trend in GSR throughout the year, GSR was linearly regressed against the transformed month of the year data as follows: lnðGSRi þ 1Þ ¼ b0 þ b1 SINMOYi þ b2 COSMOYi þ "i
Length at sexual maturity The logistic model, PL ¼ 1þed1ðLL50 Þ (Lysack 1980), was used to describe the relationship between the proportion of mature fish (PL) (Stages IV–VI) in each length interval and fork length based on 391 specimens for females. The length at maturity was then obtained by substituting PL =0.5 in the above equation, where PL is the proportion of the mature fish at length L, L50 (length at sexual maturity) and δ (the rate at which maturity is attained) are the parameters to be estimated. For most fish populations in nature, all individuals tend to attain maturity after a specific length (Chen and Paloheimo 1994). The logistic parameters were estimated by nonlinear minimization of a negative binomial loglikelihood of the form (Maartens and Booth 2005; Rutaisire and Booth 2005) ln L ¼
X L
PL yL ln þ nL lnð1 PL Þ 1 PL
where yL is the observed numbers of fish mature in a total of nL fish sampled in length class L.
where the independent variables represent angular transformations in radians of the month (MOY)i when the GSR data were collected, such that MOYi SINMOYi ¼ sin 2p ; COSMOYi 12 MOYi ¼ cos 2p 12
Results Sex ratio Fork lengths ranged from 75 to 198 cm for 656 (60.5%) male specimens and 85–182 cm for 429 (39.5%) female specimens. Monthly sex ratios were larger than the expected 0.5 (Fig. 2). Chi-square analysis of the sex ratio by month showed significant deviation from the expected 0.5 in 5 of 10 months with males dominating, and when the data are pooled, the overall ratio differs significantly from the expected 0.5 (p<0.0001, χ2 = 49.08), the number of males was larger that that females.
Sex ratio
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Environ Biol Fish (2010) 88:253–260 1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0
Feb Mar Apr May Jun
Jul Aug Sep Oct Nov
Month
Fig. 2 Monthly variations in sex ratio of Bigeye Tuna in the eastern and central tropic Pacific Ocean
(Fig. 4). However, without the data from December to January, we cannot infer if the main spawning period continues to December, ever to January. Maturity stages I and II were only applicable to Bigeye Tuna with fork lengths below 110 cm, and Maturity stage III only occurred in Bigeye Tuna with fork lengths below 150 cm. When fork lengths were larger than 105 cm, the proportion of mature specimens increased significantly and reached over 50% (Fig. 5). The spent stage occurred mainly for fish from 126 cm to 175 cm.
When the fish were divided into groups at 5 cm length intervals, males were predominant at the overall length classes except for the length class 166–170 cm (Fig. 3). Males became significant predominant at 176 cm and larger, all specimens were males at 192 cm and larger. Chi-square tests of males and females grouped into 5 cm length classes for the pooled data indicated significantly greater numbers of males in 6 of 23 fork length classes. The analysis of GLM model showed there was an interaction effect between body size and month.
Length at 50% sexual maturity (L50)
Sex development
Gonadsomatic rate
Monthly ovarian development
Our analyses showed that monthly GSRs of female and male had a significant difference in the ECTPO (t = 5.822, p = 0.021 < 0.05). Variations in GSR among months for female Bigeye Tuna were much higher than those for male Bigeye Tuna (Fig. 7). There was a significant difference (t=8.741, p< 0.001) in GSR between female and male Bigeye Tuna at 5 cm interval. The GSRs of males were larger than those of females (Fig. 8).
PL ¼
Proportion of sex maturity
Sex ratio
Six maturity stages were identified for Bigeye Tuna. There were only 2 mature stages (stage II and III) in February (n=5). The proportion of Bigeye Tuna that attained mature stage (stage IV–V) was high and over 50% during March through November. The proportion of specimens in various ovarian maturity stages showed that the main spawning period of the ECTP Bigeye Tuna occurred between March and November
The observed minimum length at sexual maturity for female bigeye was around 94 cm. Length at 50% sexual maturity for female bigeye was estimated at 107.8 cm, whereas the maturation rate parameter was 0.106 cm−1 (Fig. 6). The estimated maturation model was:
1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 85
95 105 115 125 135 145 155 165 175 185 195 Fork length classes (cm)
Fig. 3 Sex ratio of Bigeye Tuna in the eastern and central tropic Pacific Ocean with pooled data by 5 cm interval
100 90 80 70 60 50 40 30 20 10 0
1 1þ
e0:106ðL107:8Þ
VI V IV III II I
Feb Mar Apr May Jun Jul Aug Sep Oct Nov Month
Fig. 4 Monthly maturity stages of female Bigeye Tuna in the eastern and central tropic Pacific Ocean
100 90 80 70 60 50 40 30 20 10 0
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VI V IV III
GSR
Proportion of sex maturity
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II I
9 8 7 6 5 4 3 2 1 0
Female
Feb Mar Apr May Jun Jul Month
86 96 106 116 126 136 146 156 166 176 186 Fork length (cm)
Male
Aug Sep Oct
Nov
Fig. 5 Maturity stages of female Bigeye Tuna in the eastern and central tropic Pacific Ocean by 5 cm interval
Fig. 7 Monthly Gonadosomatic rates of female and male Bigeye Tuna (Vertical bars indicated standard deviation)
Female and male Bigeye Tuna showed no significant reproductive seasonality (Fig. 9). The GSR models were estimated as:
gears. Schaefer et al. (2005) further showed that some sexual differences in behavior, including vertical distributions, in bigeye aggregations associated with floating objects, causing differential vulnerability to capture by purse-seine vessels. However, previous studies of Bigeye Tuna (Kume and Joseph 1966; Nikaido et al. 1991; Matsumoto and Miyabe 2002; Schaefer et al. 2005; Sun et al. 2006) reported a preponderance of males in overall sex ratios and in the larger length intervals. Schaefer et al. (2005) reported, for Bigeye Tuna caught by purse seiner operating the eastern and central Pacific Ocean, the overall sex ratio deviated significantly from the expected 1:1 ratio with greater numbers of males. Sun et al. (2006) showed, for longliner-caught Bigeye Tuna in the tropical western Pacific Ocean, that monthly sex ratios showed no significant deviation from the expected 1 : 1 ratio, but differed significantly from the expected 1 : 1 ratio for the pooled data, with males being more prevalent than females. Similar results were found in our study, monthly sex ratios were larger than the expected 0.5, males were predominant at the overall length classes except for
Female : lnðGSRi þ 1Þ ¼ 1 0:1114SINMOYi þ 0:1206COSMOYi
Male : lnðGSRi þ 1Þ ¼ 0:8573 þ 0:0563SINMOYi 0:0072COSMOYi
Discussions Sex ratio Schaefer (1987) suggested that differentials in sex ratio with size classes might reflect differences between males and females with respect to growth, mortality, or availability to fisheries or sampling 0.9 0.8 0.7 0.6 0.5 0.4
GSR
Proportion of mature fish
1.0
0.3 0.2 0.1 0.0
0
50
100
150
200
Fork length classes (cm)
Fig. 6 Proportion of sexually mature female Bigeye Tuna. Length at 50% sexual maturity was estimated using a logistic model
9 8 7 6 5 4 3 2 1 0
Female
Male
90 100 110 120 130 140 150 160 170 180 190 200 Fork length (cm)
Fig. 8 Gonadosomatic rate of female and male Bigeye Tuna at 5 cm interval. (Vertical bars indicated standard deviation)
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14
Female l
12
GSR
10 8 6 4 2
GSR
0 5 Male 4 4 3 3 2 2 1 1 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month
Fig. 9 Distribution of monthly Gonadosomatic rate of female (upper) and male (lower) Bigeye Tuna and their variations of reproductive seasonality
the length class 166–170 cm. Males became significantly predominant at 171 cm and larger, all specimens were males at 192 cm and larger. Although our data show a consistent preponderance of males in overall sex ratios and in the larger length intervals, we need to collect more data to identify causes resulting in size-specific sex ratios in Bigeye Tuna. Length at 50% sexual maturity The length at which various proportions of a population of Bigeye Tuna reach maturity is an important life history parameter that has been inadequately evaluated in previous studies of sexual maturity. Previous studies have commonly reported the apparent length at first maturity, which is misleading regarding the reproductive potential of a population and inappropriate for inclusion in stock assessments (Schaefer 2001). The current study has derived a functional relationship between the estimated proportion mature and length of bigeye. While the minimum observed length at sexual maturity for female bigeye in this study was 94 cm, the predicted length at sexual maturity is 107.8 cm. Regardless of the methodology utilized, most previous studies reported the minimum length at sexual maturity for female bigeye to be around
100 cm, which is similar to the finding in the present study. Kikawa (1953, 1957, 1961, 1962) reported that very few female bigeye sampled in the Pacific Ocean were mature at less than 100 cm, based on evaluations of gonad indices. Yuen (1955) recorded a weight of 14–20 kg as the range necessary to attain sexual maturity and reported a similar minimum length at maturity, based on gonad indices, for female bigeye sampled from the central and western equatorial Pacific. Kume (1969a) recorded the minimum size for spawning as 92 cm in fork length, while Kume and Joseph (1966) estimated that Bigeye Tuna in the eastern Pacific reached maturity at 100–130 cm on the basis of gonad indices and that the minimum length at maturity for female bigeye sampled from the EPO was about 100 cm. McPherson (1988) and Nikaido et al. (1991) noted that some fish as small as 100 cm long could be mature. McPherson (1991) reported the minimum size at first maturity in the Coral Sea, based on comparisons of macroscopic and histological classifications, to be 100 and 125 cm in areas fished by handline and by longlines, respectively. The minimum length at maturity based on histological evaluations of ovarian tissues from female bigeye sampled in the western Pacific Ocean was reported to be 100 cm (Sun et al. 1999). Sun et al. (2006) studied the minimum maturity length of Bigeye Tuna in the Western and Central Pacific Ocean was 99.7 cm based on the histological examination and outside view of gonads. In contrast to other previous studies on maturity of bigeye, the smallest mature female reported from the northwestern Coral Sea in a relatively recent study was 80 cm and length at 50% maturity was estimated to be 102.4 cm in females (Farley et al. 2003, 2006). The classification of mature or immaturity stages was, however, based on macroscopic appearance of the ovaries, which potentially resulted in an underestimation of the length at 50% maturity. It should be noted that life history characteristics of bigeye, including length at maturity, may demonstrate some geographic variation across the Pacific, considering the limited amount of mixing observed from tagging studies to date (Hampton and Williams 2005; Schaefer et al. 2005). Spawning season The monthly maturity stages and the gonadsomatic rate suggest that Bigeye Tuna spawn in March to
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November. We cannot infer that Bigeye Tuna spawn in February because of few data in February (n=5) and no data from December to January. Kikawa (1961) studied the seasonality of maturation in Bigeye Tuna from 1951 through 1960 at 130°E to 110°W and 12°N to 10°S and found the main spawning season was from April to September throughout the entire equatorial Pacific, except for the eastern area south of equator, where spawning took place most intensively from January to March. Kikawa (1966) reported that western Pacific Bigeye Tuna spawn throughout the year, with peaks in June and September. Schaefer et al. (2005) concluded that spawning of Bigeye Tuna in the ECPO was widespread and occurred during most months of the year. Sun et al. (2006) noted that the western Pacific Bigeye Tuna spawned around the year, and the main spawning period happened between February and September. These results are similar to our study.
Conclusion The reproductive biology, including sex ratio, sex development, and length at 50% sexual maturity, and gonadsomatic rate are presented based on the fishery data collected in the eastern and central tropical Pacific Ocean. Males dominated in our samples and sex ratios deviated significantly from the expected 0.5. The main spawning period of the ECTP Bigeye Tuna occurred between March and November. Female and male Bigeye Tuna showed no significant reproductive seasonality. The observed minimum length at sexual maturity for female bigeye was around 94 cm. Length at 50% sexual maturity for female bigeye was estimated at 107.8 cm, which was significant lower than the value (135 cm) provided by Schaefer et al. (2005) in the eastern and central Pacific Ocean, although the present study concluded some similar results to others authors on Bigeye Tuna in the Pacific Ocean, even in the other oceans.
Acknowledgements The authors are grateful to the Chinese scientific fishery observer Wei Liu aboard China longline vessels for collecting samples. We acknowledge Professor Yong Chen of the School of Marine Sciences, University of Maine for his constructive comments on the manuscript. The present study is sponsored by the following funding, including Shanghai (China) Leading Academic Project grant No. S30702,
259 Special Science and Technology Research Funds for Shanghai Universities and Colleges to Select and Foster Excellent Young Teachers grant No. SSC-07011, Innovation Program of Shanghai Municipal Education Commission grant No. 09YZ275, The Research Fund for the Doctoral Program of Higher Education (RFDP) No. 20093104120005, and Initial Doctoral Funding of Shanghai Ocean University grant No. B-8202-07-0279.
References Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petran BN, Csaaki F (eds) International Symposium on Information Theory, 2nd edn. Acadeemiai Kiadi, Budapest, Hungary, pp 267–281 Batschelet E (1981) Circular statistics in biology. Academic, London, p 371 Calkins TP (1980) Synopsis of biological data on the Bigeye Tuna, Thunnus obesus (Lowe, 1839), in the Pacifi c Ocean. In: Bayliff WH (ed) Synopses of biological data on eight species of scombrids, p. 219–259. Inter-Am. Trop. Tuna Comm. Spec. Rep. 2 Chen Y, Paloheimo JE (1994) Estimating fish length and age at 50% maturity using a logistic type model. Aquat Sci 56:206–219 Collette BB, Nauen CE (1983) FAO species catalogue. Vol. 2. Scombrids of the world. An annotated and illustrated catalogue of tunas, mackerels, bonitos and related species known to date. FAO Fish. Synop. 125, Vol. 2: 137 pp Collette BB, Reeb C, Block BA (2001) Systematics of the tunas and mackerels (Scombridae). In: Block BA, Stevens ED (eds) Tuna: physiology, ecology and evolution, fish physiology, vol. 19. Academic, San Diego, pp 1–33 Farley J, Clear N, Leroy B, Davis T, McPherson G (2003) Age and growth of Bigeye Tuna (Thunnus obesus) from the eastern and western AFZ. CSIRO Marine Research, Fisheries Research and Development Corporation, and Queensland Government, Department of Primary Industry, Report No. 2000/100: iv. 93 pp Farley JH, Clear NP, Leroy B, Davis TLO, McPherson G (2006) Age, growth and preliminary estimates of maturity of Bigeye Tuna, Thunnus obesus, in the Australian region. Mar Freshwater Res 57:713–724 Hampton J, Williams P (2005) A description of tag-recapture data for Bigeye Tuna (Thunnus obesus) in the western and central Pacific Ocean. Coll Vol Sci Pap ICCAT 57:85–93 ISSF (2009) Tuna Sustainability Matrix. http://www.issfoundation.org/tsm Accessed 31 May 2009 Kikawa S (1953) Observations on the spawning of the bigeyed tuna (Parathunnus mebachi Kishinouye) near the sourthern Marshall Islands. Contr Nankai Reg Fish Res Lab 1:10 Kikawa S (1957) The concentrated spawning area of Bigeye Tuna in the western Pacific. Nankai Reg Fish Res Lab 5:145–157 Kikawa S (1961) The group maturity of Bigeye Tuna Parathunnus mebachi (Kishinouye) in the spawning areas of the Pacific. Rept Nankai Reg Fish Res Lab 13:35–46
260 Kikawa S (1962) Studies on the spawning activity of Pacific tunas, Parathunnus mebachi and Neothunnus macropterus, by the gonad index examination. Rept Nankai Reg Fish Res Lab, Occas Rep 1:43–56 Kikawa S (1966) The distribution of maturing bigeye and yellowfin and an evaluation of their spawning potential in different areas in the tuna longline grounds in the Pacific. Rept Nankai Reg Fish Res Lab 23:131–208 Kolding J, Giordano UW (2002) Lecture notes. Report of the AdriaMed Training Course on Fish Population Dynamics and Stock Assessment. FAO-MiPAF Scientific Cooperation to Support Responsible Fisheries in the Adriatic Sea. GCP/RER/ 010/ITA/TD-08. AdriaMed Technical Documents 8. 143 pp Kume S (1969a) Ecological studies on Bigeye Tuna—V. A critical review on distribution, size composition and stock structure of Bigeye Tuna in the North Pacific Ocean (north of 16°N). Bull Far Seas Fish Res Lab 1:57–75 Kume S (1969b) Ecological studies on Bigeye Tuna—VI. A review on distribution and size composition of Bigeye Tuna in the equatorial and south Pacific Ocean. Bull Far Seas Fish Res Lab 1:77–98 Kume S, Joseph J (1966) Size composition, growth and sexual maturity of Bigeye Tuna, Thunnus obesus (Lowe), from the Japanese longline fishery in the eastern Pacific Ocean. Inter-Amer Trop Tuna Comm Bull 11:45–99 Lysack W (1980) 1979 Lake Winnipeg fish stock assessment program. Manitoba Dept Nat Res Rep 80–30:1–118 Maartens L, Booth AJ (2005) Aspects of the reproductive biology of monkfish, Lophius vomerinus, off Namibia. Afr J Mar Sci 27:325–329 Mathsoft (2000) S-Plus 6.0 for UNIX, Guide to Statistics. MathSoft Inc., Seattle, WA Matsumoto T (1998) Preliminary analyses of age and growth of Bigeye Tuna 509 (Thunnus obesus) in the western Pacific Ocean based on otolith increments. In: Deriso RS, Bayliff WH, Webb NJ (eds) Proceedings of the first world meeting on Bigeye Tuna. Inter-Am Trop Tuna Comm Spec Rep 9, pp. 238–242 Matsumoto T, Miyabe N (2002) Preliminary report on the maturity and spawning of Bigeye Tuna Thunnus obesus in the central Atlantic Ocean. Coll Vol Sci Pap 54:246–260 McPherson GR (1988) Verification of the postovulatory follicle method for establishing the spawning frequency of
Environ Biol Fish (2010) 88:253–260 yellowfin, bigeye and skipjack tuna in the Coral Sea. Queensland Dep. Primary Industries, Northern Fisheries Res. Center, Cairns, Australia, Tech. Rep. FRB 88/9, 42 p McPherson GR (1991) Reproductive biology of yellowfin tuna in the eastern Australain fishing zone, with special reference to the North-western Coral Sea. Aust J Mar Freshw Res 42:465–477 Nikaido H, Miyabe N, Ueyanagi S (1991) Spawning time and frequency of Bigeye Tuna, Thunnus obesus. Bull Nat Res Inst Far Seas Fish 28:47–73 Nootmorn P (2004) Repoductive biology of Bigeye Tuna in the Eastern Indian Ocean. IOTC Proceedings 7:1–5 Rutaisire J, Booth AJ (2005) Reproductive biology of ningu Labeo victorianus (Pisces: Cyprinidae) in the Kagera and Sio Rivers, Uganda. Environ Biol Fish 73:153–162 Schaefer KM (1987) Reproductive biology of black skipjack, Euthynnus lineatus, an eastern Pacific tuna. Inter-Amer Trop Tuna Comm Bull 19:169–260 Schaefer KM (1998) Reproductive biology of yellowfin tuna, Thunnus albacares, in the eastern Pacific tuna. Inter-Amer Trop Tuna Comm Bull 21:205–272 Schaefer KM (2001) Reproductive biology of tunas. In: Block BA, Stevens ED (eds) Tuna: physiology, ecology and evolution. Fish physiology, vol 19. Academic, San Diego, pp 225–270 Schaefer KM, Fuller DW, Miyabe N (2005) Reproductive biology of Bigeye Tuna (Thunnus obesus) in the eastern and central Pacific Ocean. Inter-Amer Trop Tuna Comm Bull 23:1–31 Sun CL, Chu SL, Yeh SZ (1999) Note on the reproduction of Bigeye Tuna in the western Pacific. SCTB12/WP/BET-4. 6 pp. Twelfth Meeting of the Standing Committee on Tuna and Billfish. Tahiti, French Polynesia, June 14–23, 1999 Sun CL, Huang CL, Yeh SZ (2001) Age and growth of the Bigeye Tuna Thunnus obesus in the western Pacific Ocean. Fish Bull 99:502–509 Sun CL, Chu SL, Yeh SZ (2006) The reproductive biology of female Bigeye Tuna (Thunnus obesus) in the Western Pacific Ocean. WCPFC-SC2-BISWG-WP-1. 22 pp Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Amer Zool 21:325–345 Yuen HSH (1955) Maturity and fecundity of Bigeye Tuna in the Pacific. US Fish Wildl Serv, Spec Sci Rept Fish 150:30