Migration of Kawakawa Euthynnus Affinis in the Waters Near Taiwan

Home , Euthynnus affinis

Blackwell Science, LtdOxford, UK FISFisheries Science0919-92682004 Blackwell Science Asia Pty Ltd 705October 2004 867 Migration of Euthynnus afﬁnis near Taiwan W-D Chiou and L-K Lee 10.1111/j.1444-2906.2004.00867.x Original Article746757BEES SGML

FISHERIES SCIENCE 2004; 70: 746–757

Migration of kawakawa Euthynnus afﬁnis in the waters near Taiwan

Wann-Duen CHIOU* AND Liang-Kang LEE

Department of Fisheries, National Kaohsiung Marine University, Kaohsiung 811, Taiwan

ABSTRACT: Kawakawa Euthynnus affinis is the most abundant species among the small tuna in the coastal waters of Taiwan. The migration pattern of kawakawa to Taiwan was determined in the present study based on the species’ feeding habits and reproductive biology and on temporal variation of catch for kawakawa and its prey fishes. Schools of this species successively migrate to Taiwan from September to May, and then move away in June. They travel to the waters off Taiwan with the warm Kuroshio current, migrate toward coastal waters for feeding and move away for spawning. It is suggested in the present study that the kawakawa spawning ground is in the waters of the northern Philippines. The migration of kawakawa exhibits size-segregating behavior. Schools of immature young fish first arrive in the coastal waters around Taiwan, followed by the adults.

KEY WORDS: Euthynnus afﬁnis, feeding ground, migration, Taiwan.

INTRODUCTION migration in the Gulf of Oman and in Hong Kong,1,3 but the migration in the western Pacific Ocean has Kawakawa Euthynnus affinis is an epipelagic not yet been clarified. Although the food and feed- migratory tuna species that is widely distributed in ing habits,4 and the catch fluctuation in relation to the tropical and subtropical waters of the Indo– oceanographic and meteorological conditions of Pacific region. In the north-western Pacific Ocean, kawakawa have been documented,5 the reasons this species is distributed along the coastal area of why this species migrate to the coastal waters of the Asian continent from Malaysia north-eastward Taiwan have not been studied. Hence, the present through mainland China and Taiwan to southern study aimed to describe the seasonal pattern of Japan.1 Kawakawa is the dominant species among this species’ migration to the coastal waters of the small tuna caught in the coastal waters of Taiwan, and also to discuss the migration mecha- Taiwan, which include Katsuwonus pelamis, Auxis nism based on the species’ feeding habits and rochei and A. thazard. In recent years, the annual reproductive biology and on the temporal varia- production of kawakawa in the coastal waters of tion of catch for the prey fishes and kawakawa. Taiwan has been approximately 900 t – approximately 43.3% of all small tuna. This species occurs primarily on the north-eastern, eastern and south- MATERIALS AND METHODS ern coasts of Taiwan and Penghu.2 Kawakawa are caught mainly by set net operating in coastal In order to elucidate the seasonal pattern of waters; however, small numbers of kawakawa are kawakawa migration to Taiwanese waters, com- also captured by gill net, long line and small purse mercial catch statistics were collected and ana- seine in eastern and south-western Taiwan. lyzed. These records included daily catch statistics The migration of kawakawa to the coast of of kawakawa from five set net sites along the coast Taiwan shows a seasonal pattern, which is well of Taiwan dating from 1980 to 2001, and those from reflected by the catches made by commercial fish- the offshore area of Taitung from 1994 to 2001. eries. Commercial catches of kawakawa are made Among these sites, the Pengshing and Mangfong mainly in spring and much less in summer. How- set net sites are located on the south-west coast ever, current knowledge of kawakawa migration is of Taiwan, and the Shinshyefa, Shinyahjou and limited. There are brief descriptions of kawakawa Sanyuhyih set net sites are located on the east coast of Taiwan (Fig. 1). The catch statistics of kawakawa *Corresponding author: Tel: 886-7-361-7141. from the Mangfong, Shinshyefa and Sanyuhyih set Fax: 886-7-364-4190. Email: [email protected] net sites were commercially categorized into three Received 11 June 2003. Accepted 19 April 2004. sizes according to fork length: small (<30 cm),

Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 747

Fig. 1 Map of Taiwan area showing the survey localities of kawakawa Euthynnus afﬁnis catch data.

medium (30–50 cm) and large (>50 cm). Those Fishermen’s Association were more detailed, they from the Pengshing and Shinyahjou set net sites were adopted to determine the months of the were categorized into two sizes: small (<50 cm) and kawakawa’s occurrence in offshore Taiwan. large (>50 cm). Normally, set net fishermen stop Fish samples were also collected for basic bio- any fishing activities in the typhoon season (July– logical study in an attempt to gain further insight September) to avoid damaging fishing gear. into the migration of kawakawa. In total, 966 However, the newly designed net at the Mangfong specimens, ranging from 253 to 681 mm fork net site enables the fishermen to operate all year length, were collected from 1995 to 2001. Some round. Kawakawa are mainly caught by drift gill net were obtained from Hwalien, eastern Taiwan, and and long line in eastern Taiwan and by small purse the rest were from Jwukeng and Linyuan, south- seine in south-western Taiwan all year round. western Taiwan. Fresh specimens were weighed to Because the catch records from the Taitung the nearest 1 g; fork length was measured to the

748 FISHERIES SCIENCE W-D Chiou and L-K Lee

nearest 1 mm; and the gonads and stomach con- merase chain reaction (PCR) amplifications were tents were weighed to the nearest 0.01 g. The carried out, adopting the protocols of Innis et al.13 gonads and stomach contents were removed and A total of 35 cycles of 1.0 min at 94°C for denatur- preserved in 10% formalin for further treatment in ing, 1.0 min at 50°C for annealing and 1.5 min at the laboratory. The spawning season of kawakawa 72∞C for extension were carried out with a thermal was determined mainly by the gonadosomatic cycler (GeneAmp PCR System 9600, Perkin Elmer, index (GSI) in both sexes, and also by histological Norwalk, CT, USA). Two primers were used for the examination. The GSI was calculated as follows: PCR process; primer SP (5¢-TACCCCAAACTC- CCAAAGCTA-3 , modified from Rosel and Block),14 GSI (gonad weight/body weight) 103 (1) ¢ = ¥ which targets the light strand of the tRNAPro gene, Each food item in the stomach was identified to the and primer S12S (5¢-CAGAAGGCTAGGAC- lowest possible taxon and weighed to the nearest CAAACCT-3¢ modified from Kocher et al.),15 which 0.01 g, and the number of items was counted. The targets the heavy strand of the 12S-rRNA gene. species composition of food items was expressed Sequencing was performed with an ABI 377 auto- using the index of relative importance (IRI).6 This mated DNA sequencer (ABI, Foster City, CA, USA). index allowed the prey items to be ranked, and the For computing the genetic distances between relative importance of each food item was then pairs of populations, the pairwise FST values were compared among different localities.7 It was estimated using the method described by Tajima calculated by the following equation: and Nei,16 and the analysis of molecular variance (AMOVA) were analyzed for population subdivi- IRI (N% W%) F% (2) = + ¥ sion.17 The AMOVA analysis calculates genetic vari- where N% is the number of each food item as a ance components and hierarchical F-statistic percentage of the total number of all food items analogs (f-statistics), and tests the significance of identified; W% is the wet weight of each food item these observed variances using permutation as a percentage of the total wet weight of all food methods. In these f-statistics, fst is viewed as the items identified; and F% is the frequency of occur- correlation of random haplotypes within popula- rence of each food item as a percentage of the total tions, relative to that of random pairs of haplotypes number of stomachs containing any food. drawn from the whole species; fct as the correlation The control region is the most variable portion of random haplotypes within a group of popula- of the mitochondrial DNA;8–10 therefore, a tions, relative to that of random pairs of haplotypes sequence analysis of this region is usually con- drawn from the whole species, and fsc as the ducted to analyze the stock structure.11 Fifty fish correlation of the molecular diversity of random samples were collected to identify the kawakawa haplotypes within populations, relative to that of stock. Among these samples, 42 individuals col- random pairs of haplotypes drawn from the region. lected from the coastal waters of south-western Both analyses were carried out using the program and north-eastern Taiwan in 2002 were assigned Arlequin.18 In the AMOVA analysis, individuals are to four spatio-temporal populations, and eight assigned to five populations based on geographic individuals collected from Laoag in the northern and temporal sampling, and these populations are Philippines in January 2003 were assigned to nested into groups. another population (Table 1). Approximately 2 cm3 of muscle tissue under the dorsal fin base was RESULTS removed from each individual and preserved in ethanol (95%) for further DNA experimentation in Temporal changes of catch the future. DNA was extracted from 50 individuals, fol- Monthly catches of kawakawa from various sites lowing the procedure of Hillis and Moritz with (Fig. 2) showed that they were rarely caught during minor modifications.12 Double-stranded poly- July and August; the catch increased from Septem-

Table 1 Data collected for stock identiﬁcation of kawakawa Euthynnus afﬁnis Samples Position Sample size Date IL1 Coastal waters of I-lan, north-eastern Taiwan 8 May 2002 IL2 Coastal waters of I-lan, north-eastern Taiwan 13 October 2002 LY1Coastal waters of Linyuan, south-western Taiwan 12 April 2002 LY2Coastal waters of Linyuan, south-western Taiwan 9 November 2002 NP Coastal waters of Laoag, northern Philippines 8 January 2003

Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 749

Fig. 2 Monthly average catch of kawakawa Euthynnus afﬁnis by set net in the survey localities around Taiwan and by long line and drift gill in the offshore waters off eastern Taiwan.

ber to reach a peak in March or April; and from March, increased rapidly from April and reached a then the catch greatly decreased until June. peak in July; then they declined in August and However, two peaks in the monthly catches for this dropped to a minimum thereafter (Fig. 4). Similar species were found in offshore waters (Fig. 2). The patterns were also found for male kawakawa. Ova- first peak occurred in December and January and ries were already well developed, with a migratory the second peak occurred in April. As the nucleus stage19 when the GSI value reached 4. Mangfong set net and offshore fisheries are known Based on these results, it is suggested that the to operate throughout the year, it is suggested that spawning season of kawakawa is from April to the disappearance of kawakawa in July and August August, but the main spawning season is in July. results from kawakawa migrating away from Taiwan. The monthly catch size composition of this species further indicated that the catch was Composition of diet in different localities mainly composed of small-sized fish from October to December (Fig. 3). Few small-sized kawakawa The diet composition and the IRI value of were caught from January to April, and small-sized kawakawa in different waters around Taiwan, kawakawa were not observed between May and shown in Table 2, indicate that kawakawa is a typ- August in Taiwan. Medium-sized kawakawa were ical piscivore (i.e. consumes mainly fish). The most caught all year round, and large-sized fish dominant prey items of kawakawa in Linyuan appeared in large numbers only between February waters were Benthosema pterotum and Encrasicho- and June (Figs 2,3). lina heteroloba, in Jwukeng waters were Engraulis japonicus, Stolephorus spp. and B. pterotum, in Monthly changes in gonadosomatic index Hwalien waters were undetermined fish and B. pterotum, and in Taitung were E. japonicus and The GSI values for female kawakawa were low from A. rochei.4 Although the relative importance of September to February; they started to increase in composition of food items varied with localities,

750 FISHERIES SCIENCE W-D Chiou and L-K Lee

100 I-lan, 1990-2000 Large-sizedfish Medium-sizedfish 80 Small-size fish

20 AVERAGE PERCENTAGE(%) 0 JFMAMJJASOND 100 Taitung, 1999-2002 Large-sizedfish 80 Medium-sizedfish Small-size fish 60

AVERAGE PERCENTAGE (%) 0 JFMAMJJASOND 100 Jwukeng, 1992-1997 Large-sizedfish 80 Medium-sizedfish Small-size fish 60

AVERAGE PERCENTAGE (%) 0 Fig. 3 Monthly change in the ﬁsh size composition of kawakawa JFMAMJJASOND Euthynnus afﬁnis by set net around MONTH Taiwan.

larval anchovies and lanternfish were basically the of Penghu, and have been highly exploited since main food items for kawakawa in the waters of 1977.20 There are two major fishing grounds in Tai- Taiwan. wan, one in the north-eastern I-lan Bay area and the other in the south-western Fanliao area.21 The annual catch of larval anchovies ranged between Monthly abundance and distribution of prey 1600 and 3050 t from 1991 to 2000, with an aver- fish larvae age annual catch of 1987 t; however, the annual catch was 14 000 t in 1976 when they were not Because larval anchovies and lanternfish were the highly exploited.13 The monthly mean catches of main food items for kawakawa, the catch data for such prey fishes in different fishing grounds are these prey fishes were also collected. Anchovies shown in Fig. 5a. An abundance of larval ancho- are one of the important catches for Taiwanese vies was found each year, with two peaks. The first larval fisheries. Larval anchovies can be found peak was observed in April and May and the other along most of the coast of Taiwan and the waters in September.

Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 751

Male Famale Jwukeng, Oct. 1994-Aug. 1995 7 = 10 n F 130 8 = 6 n M 107 10 9 5 11 11 10 4 3 G.S.I 3 5 3 2 14 = 3n F 17 48 7 1 = 14 M 18n 20 8 8 0 JFMAMJJASOND

8 Hwalien, Oct. 1996-Jul. 1997 31 n = 166 7 16 F n = 104 6 M 23 5 16 17 55 11 4 18 G.S.I 3 15 2 = 10 F 16n 12 = 16 1 M 14n 0 JFMAMJJASOND

21 Linyuan, Feb. 2000-Feb. 2001 8 31 17 n = 183 7 12 F = M 168n 6 23 5 0 22 18 4 G.S.I 3 32 25 12 25 2 8 = F 14n 20 = 16 27 1 M 0n Fig. 4 Monthly change of gonado- 17 11 somatic index for female kawakawa 0 Euthynnus afﬁnis. Vertical bars indi- JFMAMJJASOND cate ±1 standard deviation; numbers indicate sample size. MONTH

Lanternfish are also found in the waters around Mitochondrial DNA sequence analysis Taiwan. There are 40 species recorded in the waters around Taiwan and the Tungsha Islands. A total of 42 variable nucleotide positions (of Benthosema pterotum is the most important com- 849 base pairs in the control region) were identi- mercial fish among lanternfish in Taiwan, and is fied among the 50 kawakawa sequences. All popu- abundant in the coastal waters of north-eastern lation pairwise FST among the five populations and south-western Taiwan.19 The annual catch is were <0.02 and no significant difference was more than 2800 t in south-western Taiwan. The observed (P = 0.05). For molecular ANOVA, all pos- monthly catch of lanternfish in south-western sible grouping types were analyzed, and no sig- Taiwan is shown in Fig. 5b. nificant difference was found among groups Basically, the above fishes were more abundant (P > 0.05; the partial results are shown in Table 3). around the coast of Taiwan from February to May, Thus, no genetic heterogeneity was observed and were scarce from June to August. among samples.

752 FISHERIES SCIENCE W-D Chiou and L-K Lee NT

4 N % Taitung 41.3 15.5 57 29 10.0 3.8 14 F % 138 %, no. each food item as %, no. N ‡ IRI –– –– W % Hwalien % N , index of relative importance; , index of relative % –– –– IRI F 11.11 3.17 10.27 149.40 – – – 27 265 ‡ IRI % –– –– –– W Linyuan % N % –– –– –– 4.96 0.65 13.64 70.90 – – – – – – – 3.72 22.35 4.39 99.43 – – – – – – – 7.85 1.13 20.86 172.66 – – – – – – – F 19.83 19.59 6.81 523.58 – – – – – – – 418 242 %, wet weight of each food item as a percentage of the total wet weight all food items identiﬁed; %, wet weight of each food item as a percentage –, no W ‡ IRI in different localities around Taiwan† localities around in different

% –– –– –– –– –– –– –– , no. organisms; , no. W Jwukeng % N uthynnus affinis E % –– –– –– ––– – – – – – – – – – – – – – – – – – – – – – 3.70 – 0.79 – 8.24 – – 33.47 – – – – – – – 9.4 5.8 3.5 2.2 13 8 –– – ––– – – 9.09 0.98 23.58 223.33 – – – – – – – –– –– – – – – – – – – – – – – – – – – – – – – 3.70 – 0.79 4.85 – – 20.91 – – – – – – – – 11.6 4.4 43.4 16 16.4 60 –– –– 5.81 2.51 2.66 30.08 1.24 0.30 0.59 1.10 18.52 13.49 12.76 486.19 – – – 3.49 0.70 1.23 6.72 – – – – – – – – – – – F 86 12.79 43.7915.12 8.05 10.46 12.01 663.15 16.53 339.70 37.40 – 6.69 728.87 – 18.52 67.46 – 13.50 1499.23 – – – – – – – – – – – 12.79 3.77 2.82 84.21 – – – – – – – – – – – 33.72 22.32 25.74 1620.40 – – – – – – – – 42.8 16 59 298 spp. spp. spp. ain food items of kawakawa spp. M 5 not listed. angidae < egmaceros lanceolatus egmaceros ecapterus maruadsi irundichthys oxycephalus ndetermined fishes 72.09 9.76 42.56 3772.41 36.36 15.66 20.67 1321.19 48.15 13.49 50.13 3063.25 11.6 4.4 16 enthosema pterotum pecimens from Jwukeng, Linyuan and Hwalien were collected from 1994–1995, 1996–1997 and 2001–2002, respectively. pecimens from Jwukeng, Linyuan and Hwalien were uxis rochei ncrasicholina heteroloba ncrasicholina ngraulis japonicus ngraulis richiurus lepturus . fish examined . fish with food S IRI ustacea T A H D Auxis spp. Baustidae Car Loligo chinensis Octopus E Decapterus Stolephorus Leiognathidae Leiognathus lineolatus Br Scomber australasicus Mesogastropoda Euphausidae B U E † ‡ of the total number stomachs containing any food; of each food item as a percentage of occurrence F %, frequency able 2 a percentage of the total no. all food items identified; NT of the total no. a percentage data collected. No Mollusca T Cr No Pisces Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 753

(a) I-lan, 1990-1999 Fangliao, 1991-2000

(b) Tungkang and Linyuan 2001-2002

Fig. 5 Monthly average catch of varied species made by Taiwan fisheries, which are also found in the stomach contents of kawakawa Euthynnus affinis. (a) larval anchovies; (b) lanternfish.

DISCUSSION Second, kawakawa is regarded as a neritic species; they usually live in the shallow coastal waters The monthly catch statistics of kawakawa indicate and are rarely captured beyond the edge of the that this species regularly appears in large num- continental shelf.1,25 East off Taiwan, the ocean is bers around the coastal waters of Taiwan from Sep- deep – the 200-m contour line is very near to the tember to May, and disappears in July and August. coast.26 Thus, it is unlikely that the Taiwanese Furthermore, in the present study, young fish with kawakawa stock travel between Taiwan and its a fork length of <25 cm were never caught all year eastern deep ocean. round.23 This suggests that the kawakawa spawn Third, based on the results of sequence analysis somewhere outside of Taiwanese waters, and their of the control region of kawakawa by molecular young migrate to Taiwanese waters only when they ANOVA, there was no significant difference between grow to a fork length of >25 cm. The disappearance kawakawa samples collected from Taiwan and of fish during the summer months also implies that those from the northern Philippines in the present they are ready to spawn and migrate back to their study. This suggests that the Taiwanese kawakawa spawning grounds. It is therefore suggested in the and the northern Philippine kawakawa are the present study that the Taiwanese kawakawa stock same stock. The migratory patterns of fish often might be mainly from the waters of the Philippines exhibit a strong similarity to the trajectories of for the following reasons. First, whole-year opera- ocean currents.27,28 Kawakawa have the character- tion of mackerel purse seine fishery and torch light istic of traveling between feeding grounds and net fishery occurs in the area between Pengchia Yu spawning grounds. Kawakawa stock of Kwangtung, and Taioyu Tai in the waters off north-eastern China, are dispersed over the south of Hong Kong Taiwan. However, kawakawa was rarely caught at during most of the year, but move close inshore on both fisheries.24 This could reflect the fact that the the east side of Hong Kong from June to August to Taiwanese kawakawa stock do not travel between spawn.3 The main axis of the Kuroshio current runs Taiwan and its northern waters in large numbers. north-east from the Luzon Strait of the Philippines 754 FISHERIES SCIENCE W-D Chiou and L-K Lee

Table 3 The partial results of molecular ANOVA of kawakawa Euthynnus afﬁnis collected from the coastal waters off Taiwan and the northern Philippines Groupings (samples) Variance component Variance (%) Φ-statistics P† Group 1 (NP, IL1, IL2, LY1, LY2) AP −0.88 −0.00876‡ 0.6999 WP 100.88 Group 1 (NP) AG −0.63 −0.00627§ 0.6012 Group 2 (IL1, IL2) AP/WG −0.32 −0.00314¶ 0.4839 Group 3 (IL1) WP 100.94 −0.00943‡ 0.7273 Group 4 (LY2) Group 1 (NP) AG 2.62 0.02621§ 0.3412 Group 2 (IL1, LY1) AP/WG −3.24 −0.03327¶ 0.4985 Group 3 (IL2) WP 100.62 −0.00620‡ 0.6589 Group 4 (LY2) Group 1 (NP) AG 1.03 0.01030§ 0.3988 Group 2 (IL1, LY2) AP/WG −1.83 −0.01850¶ 0.4067 Group 3 (IL2) WP 100.8 −0.00801‡ 0.6804 Group 4 (LY1) Group 1 (NP) AG −6.33 −0.06334§ 0.8905 Group 2 (IL2, LY1) AP/WG 4.45 0.04185¶ 0.7586 Group 3 (IL1) WP 101.88 −0.01884‡ 0.6794 Group 4 (LY2) Group 1 (NP) AG −1.22 −0.01221§ 0.6980 Group 2 (IL2, LY2) AP/WG 0.20 0.00197¶ 0.7077 Group 3 (IL1) WP 101.02 −0.01022‡ 0.7302 Group 4 (LY1) Group 1 (NP) AG 0.63 0.00630§ 0.5142 Group 2 (LY1, LY2) AP/WG −1.44 −0.01446¶ 0.5024 Group 3 (IL1) WP 100.81 −0.00807‡ 0.7067 Group 4 (IL2) Group 1 (NP) AG 0.01 0.00014§ 0.5367 Group 2 (IL1, IL2) AP/WG −0.89 −0.00887¶ 0.4829 Group 3 (LY1, LY2) WP 100.87 −0.00873‡ 0.6862

†Largest value; ‡ST; §CT; ¶SC. AG, among group; AP, among population; WG, within group; WP, within population. AG, *.057*.057; AP, *.057*.057; IL, I-lan, north-eastern Taiwan; LY, Linyuan, south-western Taiwan; NP, Laoag, northern Philippines; WG, *.057*.057; WP, *.057*.057.

along the eastern coast of Taiwan to the Ryuku 30 27 50 40 38 Islands of Japan. A branch of it flows into the Tai- 31 21 47 21 20 26 wan Strait to encounter the current from the north 73 27 13 29 52 in the middle of the strait in winter. Hence, it is 18 8 68 22 reasonable that the kawakawa from Taiwan regu- 29 33 larly travel between Taiwan and the Philippines 15 in large numbers using the Kuroshio current. 14 28 Feeding might be a very important factor in the 44 18 45 migration of kawakawa to the coast of Taiwan for a few months of the year. The diet composition in different areas shown in Table 2 indicates that kawakawa consume mainly local teeming prey Fig. 6 Monthly change of empty stomach ratio (ESR) of fishes. The pattern of monthly change in the kawakawa Euthynnus affinis in Hwalien, Jwukeng and kawakawa catch coincides with those of its main Linyuan, Taiwan. ESR = (the number of specimens prey fishes. The highest catch of kawakawa is in with empty stomachs/the total number of specimens) 100%; numbers indicate sample size. March or April, and prey fishes are most abundant ¥ from February to May in Taiwan. The empty stomach ratio in the present study was very high in the because larval anchovies and lanternfish are abun- Hwalien and Jwukeng coastal waters because of a dant in south-western Taiwan (Fig. 5). This evi- lack of prey foods (Fig. 6). The empty stomach ratio dence implies that kawakawa migrate toward the is apparently low in Linyuan coastal waters (Fig. 6) coastal waters of Taiwan to feed. In addition, Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 755

although the total biomass of prey fishes of spring to early autumn, replaces the Kuroshio kawakawa in the waters of Taiwan can not be esti- water. During this period, kawakawa can be found mated exactly yet, the biomass of larval anchovies on all the western coasts of Taiwan.2,29 and lanternfish should be more than 5000 t/year According to investigation of the monthly catch only in the coastal waters of south-western Taiwan (Fig. 2) and size composition (Fig. 3) in the present according to the estimation of the yearly catch of study and in some previous reports on oceanic con- the two main prey fishes and the yearly fishing rate ditions,5,26,29 the spatio-temporal distribution and of 0.691 of larval anchovies.30 There is no doubt that movement of kawakawa around Taiwan can be the coastal waters around Taiwan are a good feed- illustrated. In autumn, kawakawa gradually migrate ing ground for kawakawa because of the abundant toward the coastal waters of Taiwan. The coastal food organisms around Taiwan. waters of Taiwan are gradually occupied by a colder Another important factor affecting the distribu- water mass from November when the north-east- tion and migration of kawakawa is ambient tem- ern monsoon prevails. The surface temperature of perature. In Hong Kong, kawakawa are seldom inshore water decreases to its lowest in January and caught inshore during the coldest months.3 In February. This colder coastal water forms a temper- south-western Taiwan, the catch of this species is ature barrier and forces kawakawa to congregate in usually poor in winter. However, when a branch the warmer offshore waters where the Kuroshio of the warm Kuroshio current intrudes into the current runs through. So, the first peak in kawakawa coastal waters, kawakawa migrate toward the catch appears in December and January in the off- coastal waters with the warm current and then a shore waters. The biomass of this species is low, and good catch of this species in set nets is reached.5 schools are mainly small and mid-sized fish from Although kawakawa are captured throughout the September to December. In this period, a good year off western Thailand, the highest catches are catch of this species is reached (daily made during the months when the sea surface catch > 1000 kg), usually resulting from the intru- temperature rises.1 Evidently, kawakawa is a typical sion of a warm water tongue.5 These catches mainly warm-water species that does not have a prefer- comprise small fish, which are categorized as ence for low temperature habitats. Hence, water immature fish.32 The schools of immature young temperature plays an important role in the distri- fish arrive first in the coastal waters around Taiwan, bution and migration of kawakawa. The results of and then the adults. This phenomenon further indi- a previous study by Chiou and Cheng revealed that cates that the migration of kawakawa demonstrates kawakawa prefer staying offshore and do not size-segregating behavior. Similar size segregation migrate toward the coastal waters in south-western is found in mackerel and herring.33 By March, the Taiwan when the difference in water temperature colder water mass diminishes gradually and disap- at 15 m depth between inshore and offshore is pears completely from the coast of Taiwan during greater than 0.6∞C.5 the following months. When the temperature of From these results, it is suggested that coastal waters rises from March onward, large- kawakawa migrate to the waters of Taiwan with the sized kawakawa mainly migrate from deeper off- warm water current and then migrate toward the shore to coastal waters. The coastal waters are com- coastal waters for feeding. The main flow of the pletely occupied by the warm water mass from May warm Kuroshio current runs northward closely and the occurrence of cold water and warm water along the eastern coast of Taiwan all year round. tongues were not more developed again. The Hence, it is the primary fishing ground for kawakawa do not appear in dense schools, and are kawakawa in eastern Taiwan,2 and the highest only scattered along the coast of Taiwan from May. catches occur in I-lan Bay, north-eastern Taiwan Hence, the main fishing period is between March (Fig. 2), because larval anchovies are abundant and April in the coastal waters of Taiwan. there and the warm Kuroshio current intrudes into The monthly catch analysis of kawakawa in the the bay.21,31 A branch of the Kuroshio passes by the present study indicates that this species appears in southern end of Taiwan and flows into Taiwan the coastal waters of Taiwan from September to Strait to encounter the current from the north in May, and it then moves away from Taiwan in June. the middle of the strait in winter; it is then forced In the 1970s in Taiwan, kawakawa were primarily by the north-eastern monsoon to flow westward captured by purse seine operating in the offshore near the Penghu Islands.29 The kawakawa might waters of eastern and north-eastern Taiwan. The also migrate to these areas by taking advantage of catch from July to September was also scarce.2 In the Kuroshio branch. This could also explain the the present study, the spawning season of fact that the south-western coasts of Taiwan and kawakawa in Taiwan was from April to August and the Penghu waters are important fishing grounds peaked in July. The possibility of kawakawa spawn- of this species.2 South China Sea water, which flows ing in Taiwanese waters was noted. The appearance all the way through the Taiwan Strait from late of kawakawa larvae around Taiwanese waters has 756 FISHERIES SCIENCE W-D Chiou and L-K Lee

been reported by Chiu and Chen,34 as well as by RS, Majkowski J, Langi S (eds). Interactions of Pacific Tuna Nishikawa et al.35 However, it should be noted that Fisheries, Vol. 2: Papers on Biology and Fisheries, Processing few samples were collected during their studies. of the First FAO Expert Consultation on Interactions of Therefore, it is suggested that the disappearance of Pacific Tuna Fisheries, 3–11 December 1991, Noumea, New kawakawa during the summer months can be Caledonia. FAO, Rome. 1994; 388–408. 2. Yang RT. Skipjack tuna fisheries in the waters around ascribed to spawning migration and, although Taiwan. J. Fish. Soc. Taiwan 1975; 4: 93–110 (in Chinese). some mature fish might spawn around Taiwan, the 3. Williamson GR. Little tuna Euthynnus affinis in the Hong main spawning grounds for this species are evi- Kong area. Bull. Jpn Soc. Sci. Fish. 1970; 36: 9–18. dently not in the waters around Taiwan. 4. Chen YU, Tsay CT. Food and feeding habits of oceanic As mentioned, kawakawa might regularly travel bonito, Euthynnus affinis yaito (Kishinouye) in eastern between Taiwan and the Philippines. Fishermen waters of Taiwan. Bull. Taiwan Fish. Res. Inst. 1986; 42: 51– in Taiwan do not catch large numbers of larval 56 (in Chinese). and juvenile kawakawa (fork length < 25 cm) all 5. Chiou WD, Cheng LZ. Catch fluctuation of the oceanic year round, and spawning and/or spent female bonito (Euthynnus affinis) in relation to oceanographic kawakawa are found in June and July in the and meteorological conditions in Jwu-Keng coast of southwestern Taiwan. J. Fish. Soc. Taiwan 1995; 22: 213– Philippines.1 This implies that the Taiwanese 225. kawakawa stock’s spawning ground is in the 6. Pinkas L, Oliphant MS, Iverson ILK. Food habits of albacore, waters of the northern Philippines; then juvenile bluefin tuna, and bonito in California waters. Sacramento: kawakawa can use the Kuroshio current for a California Department of Fish and Game. Fish. Bull. 1971; free ride back the Taiwanese feeding grounds. 152: 1–139. The smallest kawakawa caught by set net in the 7. Cailliet GM, Milton SL, Ebeling AW. Fishes: A Field and present study was approximately 25 cm fork Laboratory Manual on Their Structure, Identification, and length, and fish smaller than that are not caught Natural History. Wadsworth Publishing, CA. 1986. by other fishing methods in Taiwan. These facts 8. Moritz C, Dowling TE, Brown WM. Evolution of animal further imply that kawakawa larvae might remain mitochondrial DNA: relevance for population biology and in the spawning and/or hatching grounds of the systematics. Annu. Rev. Ecol. Syst. 1987; 18: 269–292. 9. Brown WG, Gadaleta G, Pete G, Saccone C, Sbisa E. Struc- Philippines for a few months. After this, they tural conservation and variation in the D-loop containing migrate to the Taiwanese feeding grounds with region of vertebrate mitochondrial DNA. J. Mol. Biol. 1986; the Kuroshio current until reaching fork lengths 192: 503–511. of approximately 25 cm. A similar migration pat- 10. Southern S, Peter JS, Andrew ED. Molecular characteriza- tern has been found for skipjack tuna – when the tion of cloned mitochondrial genome. J. Mol. Evol. 1988; 28: young fish become adolescent fish, they migrate 32–42. to the feeding grounds using the oceanic cur- 11. Ikeda M, Taniguchi N. Genetic variation and divergence in rent.25 Most juvenile kawakawa migrating north- populations of ayu Plecoglossus altivelis, including endan- ward with the Kuroshio current will stay in the gered subspecies, inferred from PCR-RFLP analysis of the coastal waters of Taiwan because of the abundant mitochondrial DNA D-loop region. Fish. Sci. 2002; 68: 18– 26. food organisms. Juvenile kawakawa ranging in 12. Hillis DM, Moritz C. Molecular Systematics. Sinauer Associ- length from 18.3 to 33.2 cm can be caught from ates, Sunderland. 1990. 36 August to October off Aburatsu, southern Japan. 13. Innis MA, Gelfand DH, Sninsky JJ, White TJ. PCR Protocols: Some kawakawa might therefore limit northward A Guide to Methods and Applications. Academic Press, New migration to the south of Japan following the York. 1989. Kuroshio current. 14. Rosel PE, Block BA. Mitochondrial control region variability and global population structure in the swordfish, Xiphias gladius. Mar. Biol. 1996; 125: 11–22. ACKNOWLEDGMENTS 15. Kocher TD, Thomas WK, Mayer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC. Dynamics of mitochondrial DNA This study was funded by the Council of Agricul- evolution in animals: amplification and sequencing with ture, Executive Yuan, Taiwan. We are most grateful conserved prime. Proc. Natl Acad. Sci. USA. 1989; 86: 6196– to Dr Lei-Zong Cheng (Fortune Institute of 6200. Technology) and Dr Chiee-Young Chen (National 16. Tajima F, Nei M. Estimation of evolutionary distance Kaohsiung Marine University) for their valuable between nucleotide sequences. Mol. Biol. Evol. 1984; 1: 269– suggestions. 285. 17. Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplo- REFERENCES types: application to human mitochondrial DNA restriction data. Genetics 1992; 131: 479–491. 1. Yesaki M. A review of the biology and fisheries for kawakawa 18. Schneider S, Roessli D, Excoffier L. Arlequin Ver 2000: A (Euthynnus affinis) in the Indo–Pacific region. In: Shomura Software for Population Genetics Data Analysis. Genetics Migration of Euthynnus affinis near Taiwan FISHERIES SCIENCE 757

and Biometry Laboratory, University of Geneva, Geneva. 27. Sumich JL. An Introduction to the Biology of Marine Life – 2000. The Nekton. Wm. C. Brown Publishers, Dubuque, USA. 1992. 19. Lin KL, Chen CT. Seasonal changes in the Indian driftfish, 28. Harden Jones FR. Fish Migration. Edward Arnold, London. Ariomma indica (Day) from northeastern waters of Taiwan. 1968. J. Fish. Soc. Taiwan 1991; 18: 195–203. 29. Fan KL. A study of water masses in Taiwan Strait. Acta 20. Chen TS. A study on anchovy resource of Taiwan. Exp. Rep. Oceanogr. Taiwanica 1982; 13: 140–153. Taiwan Fish. Res. Inst. 1984; 25 (in Chinese). 30. Chen TS, Kuo CL. Estimation of original population 21. Chiu TS, Young SS, Chen CS. Monthly variation of larval size and rate of fishing of engraulid larvae using the anchovy fishery in I-lan Bay, NE Taiwan, with an evaluation Delury’s method. J. Taiwan Fish. Res. 1994; 2: 15–30 (in for optimal fishing season. J. Fish. Soc. Taiwan 1997; 24: Chinese). 273–282. 31. Hsia KY, Lee KT, Lee MA. Fishing ground formation of larval 22. Wang TM, John Chen CT. A review of lanternfishes (fam- anchovy in relation to oceanographic and meteorological ilies: Myctophidae and Neoscopelidae) and their distri- conditions in the I-lan Bay of northeastern Taiwan. J. Fish. butions around Taiwan and the Tungsha islands with Soc. Taiwan 1998; 25: 239–249. notes on seventeen new records. Zool. Stud. 2001; 40: 32. Chiou WD, Cheng LZ, Chen KW. Reproduction and food 103–126. habits of kawakawa Euthymus affinis in Taiwan. J. Fish. Soc. 23. Anonymous. Fisheries Yearbook Taiwan Area. Taiwan Taiwan 2004; 31: 23–38. Fisheries Bureau, Department of Agriculture and Forestry, 33. Pitcher TJ, Magurran AE, Edwards JI. Schooling mackerel Provincial Government of Taiwan. 1997–2001. and herring choose neighbours of similar size. Mar. Biol. 24. Hsu CH, Lee KT, Lee MA, Liao CH, Lu HJ. Effects of sea- 1985; 86: 319–322. sonal environmental changes on the mackerel purse seine 34. Chiu TS, Chen CS. Distribution of scombrid larvae (Pisces: fishery in the waters off northeast Taiwan monitored by Scombridae) in the waters around Taiwan. J. Fish. Soc. satellite remote sensing. Proceedings of the Joint Taiwan– Taiwan 1995; 22: 303–312. Australia Aquaculture Fish Resources Management Forum, 35. Nishikawa Y, Honma M, Ueyanagi S, Kikawa S. Average Dis- 2–8 November 1998, Keelung, Taiwan, ROC. 2000; 4: 257– tribution of Larvae of Oceanic Species of Scombroid Fishes, 261. 1956–1981, Far Seas Fisheries Research Laboratory S Series 25. Anderson RC, Waheed Z, Scholz O. Kawakawa (Euthynnus 12. Shimizu, Japan. 1985. affinis). Maldives Mar. Res. Bull. 1998; 3: 127–144. 36. Yabe H, Anraku N, Mori T. Scombroid young found in the 26. Chu TY. Environmental study of the surrounding waters of coastal seas of Aburatsu, Kyushu, in summer. Contr. Nankai Taiwan. Acta Oceanogr. Taiwanica 1971; 1: 15–32. Reg. Fish. Res. Lab. 1953; 11: 1–10.