A DESCRIPTION OF A POSSIBLE SPAWNING AREA OF THE SWORDFISH (Xiphias gladius) IN THE TROPICAL NORTHWEST ATLANTIC.

SCRS/22/78 Col. Vol. Sci. Pap. ICCAT, 55(4): 1449-1458 (23) A DESCRIPTION OF A POSSIBLE SPAWNING AREA OF THE SWORDFISH (Xiphias gladius) IN THE TROPICAL NORTHWEST ATLANTIC. 1 Jaime Mejuto, Blanca García -Cortés SUMMARY This document aims to provide supplementary information to previous studies and to define new spawning areas of the swordfish (Xiphias gladius) in the tropical NW Atlantic, based on observations of the overall sex-ratio and by size class, in addition to the analysis of gonadal indices obtained from swordfish specimens caught between October and December, 21 by the Spanish surface longline fleet. The resulting data after sampling 1837 swordfish on board a commercial vessel would suggest that some specimens of female swordfish from the new areas under observation may be in an advanced stage of maturity-reproduction and on the verge of spawning particularly in some zones. Substantial differences were, however, found between the areas studied. Possible causes for these differences are put forth here. RÉSUMÉ Le présent document vise à compléter les études antérieures et à définir les nouvelles zones de frai de l espadon (Xiphias gladius) dans l Atlantique nord-ouest tropical, en se fondant sur les observations du sex-ratio global et par classe de taille, ainsi que sur l analyse des indices gonadiques obtenus à partir d espadons capturés entre octobre et décembre 21 par la flottille espagnole de palangre de surface. Les résultats obtenus à partir de 1.837 espadons échantillonnés à bord d un navire commercial suggèrent que certains spécimens femelles d espadon des nouvelles zones observées peuvent se trouver dans un état avancé de maturitéreproduction et sur le point de frayer, notamment dans certaines zones. D importantes différences ont néanmoins été détectées entre les zones sous étude. Les causes éventuelles de ces différences sont exposées. RESUMEN En este documento se intenta complementar estudios anteriores y definir nuevas áreas de reproducción del pez espada (Xiphias gladius) en el Atlántico NW tropical, a partir de observaciones de sex-ratio global y por clase de talla así como mediante índices gonadales, obtenidos a partir de peces espada capturados entre octubre y diciembre del 21 por la flota española de palangre de superficie. Los resultados obtenidos a partir de 1837 peces espada muestreados a bordo de un buque comercial sugieren que algunos ejemplares hembras de pez espada de las nuevas zonas observadas pueden encontrarse en un avanzado estado de maduración-reproducción y en proximidad a la puesta, especialmente en algunas áreas. No obstante fueron detectadas importantes diferencias entre las áreas estudiadas sugiriéndose posibles causas de estas diferencias. KEYWORDS Swordfish, reproduction, gonadal index, sex ratio. 1 Instituto Español de Oceanografía, P.O. Box 13, 158 A Coruña, Spain. e-mail: tunidos.coruña@co.ieo.es 1449

1. INTRODUCTION. Over the course of the commercial fishery activity carried out by the surface longliners targeting the swordfish (Xiphias gladius) in the Atlantic Ocean, scientific observers have boarded these vessels to monitor this fishery scientifically as well as to collect basic biological data. This paper is based on the information acquired thanks to the data compiled by a scientific observer working on board a commercial surface longline vessel using the Florida style gear to target the swordfish and whose fishery activity was carried out between October and December of 21 in fishing areas of the NW Atlantic not commonly exploited. This area had never before been monitored under our observer program. A number of studies have reported that the spawning areas preferred by the swordfish are predominantly the warm waters of the tropical or subtropical zones to the West of the oceans, in both the Northwest and Southwest Atlantic and in the West Indian Ocean (Mejuto et al., 1994; 1995; Mejuto & García, 1997; Arocha & Lee, 1996), as well as in the West Pacific (Matsumoto & Kazama, 1974; Nishikawa & Ueyanagi, 1974; Nishikawa et al., 1978, 1985). This could be due to the fact that the warm waters tend to be concentrated in the near surface layers of the Western zones of the gyres (see SCRS/2/15). On the basis of surface temperature data (SST), Rey (1988) suggests that the spawning of the swordfish is related to the temperature of the seawater (between 23º-26º C). However, the greater thermal homogeneity of the near surface layers in the zones located farther to the West of the tropical and subtropical equatorial band, having a deeper thermocline, may play a more important role, thus favouring female reproductive processes as well as the viability of the eggs and larvae. Therefore the SSTs should not be considered, in and of themselves, as the most appropriate indicators to define potential reproduction areas of the swordfish (Mejuto et al., 1994). The reproduction of the swordfish, the spawning season and area, in addition to fecundity estimates are important elements that must be taken into account in stock assessment. Swordfish reproduce all year round (Vialov and Ovchinnikov, 198), but maximum spawning intensity depends on the season and geographic area. This paper aims to supplement previous studies by providing biological information on geographic zones that have rarely been described to date in other studies and to classify these areas as a possible spawning zone of the swordfish. For this we have used an analysis of sex-ratio at size, gonadal indices (GIs), etc., in an attempt to provide a better definition of the possible spawning areas of this species and to determine the reproductive condition of females. 2. MATERIAL AND METHODS. The data used in this paper come from information obtained by observers working on board surface longliners under the scientific monitoring program sponsored by the I.E.O. The information analysed during the scientific observation was compiled on board a longline vessel fishing in a tropical zone of the NW Atlantic from October to December, 21. It is unusual for this fleet to carry out commercial activity in this zone and during this time of year. Data pertaining to catch, effort, size and sex were compiled during this trip. A total of 1837 fishes, both male and female, were sampled on board to obtain biological information on the zones of the tropical Northwest Atlantic (between 1º-15º N and 3º-4º W) which had not been studied before. Data on the activity of the vessel were initially recorded daily by degree of latitude and longitude, and later grouped into 5º x 5º area/month formats for analysis (Miyake and Hayasi, 1978). 145

The lower jaw fork length (LJFL) was measured to the lowest centimetre, although the specimens were later grouped into size classes at 5 cm intervals for the final analyses (Miyake and Hayasi, o.c.). During the processing of the swordfish specimens on board (removal of guts, gills, fins, head), sex was determined de visu (Artüz, 1963) and both gonads were weighed in grams using a dynamometer with an accuracy of roughly 15 grams. Sex-ratio (SR) was defined: {Females/(Females+Males)}*1, (Mejuto et al., 1995). The overall sex-ratio (SRo) was calculated for all the sizes combined and the sex-ratio at size (SRs), for each 5ºx5º square analysed by month (October, November and December) as well as for the fourth quarter of the year (Q4= October+November+December), although it is the area factor that would appear to have the greatest impact on the variability of the SRs (Mejuto et al., 1994; Mejuto et al., 1995; Turner et al., 1996). The Gonadal Index (GI) was calculated for swordfish females with a LJFL of 15 cm or greater (or of 13 cm EFL or greater), which is the minimum size at maturity observed for females in the Atlantic Ocean (Arocha and Lee, 1996). The GI values were calculated by using the formula: GI (EFL) = (Wg / EFL ^3) * 1^4 (Kume & Joseph, 1969) modified as : GI (LJFL)= (Wg / LJFL ^3) * 1^4. Where : Wg = weight of the two female gonads in grams. LJFL = lower jaw- fork length in cm. EFL = eye-fork length in cm. The EFL size value was calculated on the basis of the LJFL value as follows: EFL=-8.259+.93*LJFL (Taylor & Murphy, 1992). GI(EFL) values >= 3. would indicate, a priori, females in an active reproductive stage (Kume & Joseph, o.c.). In order to arrive at a conversion factor between the GI(EFL) and the GI(LJFL), we compared the paired values of the GIs previously obtained from 315 females sampled by scientific observers on board Spanish vessels. These female specimens were caught in different areas and exhibited varying conditions of sexual maturity. The GI(LJFL) values for each female measuring 15 cm or over were grouped into size classes at 5 cm intervals and the minimum, maximum and average GI values were calc ulated for each size class and for each 5ºx5º square/month as well as for the fourth quarter (months combined). 3. RESULTS AND DISCUSSION. A total of 1837 swordfishes ranging in size between 65-265 cm (LJFL), or 5-235 cm (EFL), were sexed during the October-December 21 period. In the zone of the NW Atlantic monitored (1º-15º N and 3º-4º W) there were 278 observations of fishes just in the month of October all found in square 14 NW, having a size range of between 8-21 cm (LJFL) or 65-185 cm (EFL). A total de 1559 observations were reported on fishes caught during the months of October, November and December in square 153 NW, with a size range of 6-265 cm (LJFL) or 5-235 cm (EFL). Figure 1 shows size distribution () by sex and sexes combined, by square and for the fourth quarter of the year. Differences were found between the size distributions of the two squares. The cumulative percentage representing 5% of the size distributions in square 14 NW is defined in smaller size classes (approx. 135 cm) than the percentage for square 153 NW (approx. 15 cm) (Figure 2). These differences would remain the same if we compare the size distributions of the two squares for the month they have in common (October), since the cumulative percentage of square 153 NW is practically the same for the three months during which observations were performed (Figure 3). Table 1 presents a summary of the information by 5º x 5º area of the fourth quarter, the number of fishes sampled by squares and their overall sex ratio values (SRo). Values of SRo = 24.1 % for square 14 NW and of SRo= 11.87 % for square 153 NW would already point to differences in distribution by sex between the two areas as regards the population captured using this fishing gear. 1451

These differences become even more accentuated if we calculate a SRo restricted to only individuals with a LJFL >= 15 cm resulting in values of SRo= 33.93 % in area 14 NW and of SRo= 11.45 % in area 153 NW. In addition to the 1% difference between the SRos calculated for square 14 NW based on the sizes under consideration, the greater percentage of males in this square would appear to be concentrated especially in the sizes measuring less than 15 cm LJFL. While the SRo should be interpreted with utmost caution as it is affected by the size range considered, this variable would suggest that there are differences in sex-ratios, particularly in the area located farther to the north. Table 2 gives the SRo values and the number of specimens sampled by month in square 153 NW. In general the SRo values indicated a predominance of males regardless of the month or size range analysed. The SRs values by size class () obtained by square are shown in Table 3. The SRs values pertaining to the fourth quarter of the year indicate that there are changes between the two zones (Figure 4). In area 14 NW, the percentage of females was less than 5% for sizes under 175 cm LJFL. In area 153 NW, however, females were only dominant in sizes greater than 22 cm LJFL, and they practically disappeared or were present in small percentages in some of the size groups. This SRs pattern observed in area 153 NW might be interpreted as being similar to the SRs pattern which has been defined as characteristic of the reproduction zones in other oceans (Mejuto et al., 1995; Arocha and Lee, 1996). The transformation of the LJFL into the EFL in 315 females caught by commercial vessels in different areas made it possible to obtain paired GIs (LJFL and EFL) to calculate a conversion factor by means of a simple linear regression: GI(EFL) = 1.4291 * GI (LJFL). If we consider that a value of GI (EFL) >= 3. would indicate the possibility of there being females in an active stage of reproduction (Kume and Joseph, o.c.), the equivalent value of GI(LJFL)>=2.9 would indicate a similar reproductive condition. On the basis of the GI (LJFL) values found after analysing 122 females >=15 cm LJFL caught in these zones of the NW Atlantic, we calculated the minimum, maximum and average GIs by square for the last quarter and by months (Table 4). Only data from 38 females ranging between 15-21 cm LJFL were available for area 14 NW in the fourth quarter. The resulting values of ave.gi= 1.5 and max.gi= 2.33 would not generally imply an advanced stage of reproduction in these females as a whole, although there were random observations of females with a high GI, which would suggest that there is sporadic spawning (Figure 5). However, in area 153 NW, in the fourth quarter, there were observations of 11 females ranging between 15-265 cm LJFL. The resulting values of ave.gi= 5.33 and max.gi= 17.77 would suggest the these females as a whole were in an advanced stage of reproduction. Therefore, within this area/quarter, favourable conditions would be expected, giving rise, in general, to the successful evolution of the processes of maturation and spawning (Figure 5). The sampling size was not large enough to provide conclusive evidence, particularly in area 14 NW. Nevertheless, the SRs pattern seen in area 153 NW appears to be similar to the pattern which is typical of a reproductive zone (a biological spawning region) and this area also presents very high overall average GI values. Moreover, data on catch per unit of effort (CPUE) by sex obtained in the two areas would suggest that males clearly prevail over females. In area 14 NW the predominance of males over females (males/females) is 3.12 and 2.7 for the CPUEs in number and weight, respectively. In area 153 NW this prevalence of males is even greater, showing values of 7.43 and 5.85 for the CPUEs in number and weight, respectively. 1452

Although the location of new spawning grounds is often linked to the research means available and an increase in geographic coverage, it has generally been reported that the reproduction zones of the swordfish are in keeping with the hypothesis that they are conditioned by the sea surface temperature SST (between 23º and 26º C) (Rey, 1988). Yet, the greater homogeneity of the near surface layers of the areas located farthest to the West of the gyres in the tropical equatorial band, could play a key role in triggering the reproductive processes in females. For this reason, the spawning areas of this species may be especially linked to the distribution of the isotherms of the near surface layers as a whole, particularly at depths of 5-2 metres. A look at the maps of temperature distribution (Anonymous, 1977; SCRS/2/98) at different depths (5, 1, 2, 3 metres) shows that the zone under study may exhibit major temperature differences between areas in the near surface layers. Although on the surface layer, there would appear to be a certain continuity of the SST between the reproduction areas defined for the Northern and Southern stocks, the maps of the isotherms in the near surface layers, on the whole, would point to the existence of clear thermal discontinuities between these areas. After examining the areas under study, it is possible to generalise that there is a difference of roughly 4º C in temperature between the two squares, with the higher temperature being consistently found in the square located farther to the North (153 NW), which would account for our findings here. Therefore, depending on the thermal conditions in the zone, these areas could be traditional spawning grounds for this species or, they may occur as an anomaly due to the expansionconcentration of the traditional spawning areas of the swordfish which have been reported in the North Atlantic to date. In exceptional cases there may even be some sporadic connection or continuity between the reproduction areas of the North and South Atlantic, although this would be rather unlikely in view of the data on the temperature of the near surface layers, especially around 1-2 metres depth. ACKNOWLEDGEMENTS. The authors would like to express their most heartfelt gratitude to the skippers and crews of the ships who have aided us in our endeavour, allowing scientific observers on board the longliners, with special thanks to the scientific observer of this trip, Alberto Iglesias Alvaro-Gracia. This research was carried out with funds from project SWOATL of the Spanish Institute of Oceanography. LITERATURE CITED. ARTÜZ, M. I. 1963. Contribution to the knowledge of the biology of the swordfish (Xiphias gladius L.) in the Sea of Marmara. Proc. Gen. Fish. Coun. Medit. 7: 459-471 (Tech. Pap. 47). TAYLOR, R.G., M.D. Murphy. 1992. Reproductive biology of the swordfish Xiphias gladius, in the Straits of Florida and adjacent waters. Fish. Bull. 9:89-816. ANÓNIMO, 1999. Report of the Swordfish Assessment Workshop. Detailed report. ICCAT 2. AROCHA, F., D.W. Lee. 1996. Maturity at size, reproductive seasonality, spawning frequency, fecundity and sex ratio in swordfish from the Northwest Atlantic. ICCAT Col. Vol. Sci. Pap. Vol XLV(2):35-357. KUME, S., J. Joseph. 1969. Size composition and sexual maturity of billfishes caught by the Japanese longline fishery in the eastern Pacific Ocean east of 13º W. Far Seas Fish. Res. Lab. Bull. 2:115-162. 1453

MATSUMOTO, W.M., T.M. Kazama.1974. Occurrence of young billfishes in the Central Pacific Ocean. In R.S. Shomura and F. Williams, (eds). Proceedings of the International Billfish Symposium, Kailua-Kona, Hawaii, August 9-12, 1972. Part 2. Review and Contributed Papers, p.238-251. US. Dep. Commer., NOAA Tech. Rep. NMFS-SSRF-675. MEJUTO, J., J.M. de la Serna, B. García, M. Quintans, E. Alot. 1994. Sex ratio at size of the swordfish (Xiphias gladius L.) in the Atlantic and Mediterranean Sea: Similarity between different spatial-temporal strata. ICCAT Col. Vol. Sci. Pap. Vol. XLII(1):322-327. MEJUTO, J., J.M. de la Serna, B. García. 1995. An overview of the sex-ratio at size of the swordfish (Xiphias gladius L.) around the world: Similarity between different strata. ICCAT Col. Vol. Sci. Pap. Vol. XVIX(3):197-25. MEJUTO J., B. García. 1997. A preliminary analysis of gonadal indices of the swordfish (Xiphias gladius L) in the Atlantic Ocean. ICCAT. Col. Vol. Sci. Pap. Vol. XLVI(3):336-343. (SCRS 96/142). MEJUTO, J. 1999. A possible relationship between the N.A.O. index and the swordfish (Xiphias gladius) recruitment index in the North Atlantic: hypothesis of reproduction and possible effects on recruitment levels. ICCAT Col. Vol. Sci. Pap. Vol. XLIX (4):339. SCRS 99/111. MIYAKE, M., S. Hayasi. 1978. Manual de operaciones para estadísticas y muestreo de los túnidos y especies afines en el océano Atlántico. (2ª edición) ICCAT (Madrid.España). NISHIKAWA, Y., S. Ueyanagi. 1974. The distribution of the larvae of swordfish, Xiphias gladius, in the Indian and Pacific Oceans, p. 261-264. U.S. Dep. Commer., NOAA Tech. Rep., NMFS. SSRF-675. NISHIKAWA, Y., S. Kikkawa, M. Honma and S. Ueyanagi. 1978. Distribution atlas of larval tunas, billfishes, and related species-results of larval surveys by R/V Shunyo Maru and Shoyo Maru (1956-1975). Far Seas Res. Lab., S Series 9, 99p. NISHIKAWA, Y., M. Honma, S. Ueyanagi, S. Kikkawa. 1985. Average distribution of larvae of oceanic species of scombroid fishes, 1956-1981. Far Seas Fish. Res. Lab., S Series 12, 99p. REY J.C. 1988. Comentarios sobre las areas de reproducción del pez espada (Xiphias gladius) en el Atlántico y Mediterráneo. Col. Vol. Sci. Pap. Vol. XXVII: 18-193. TAYLOR, R.G., M.D. Murphy. 1992. Reproductive biology of the swordfish Xiphias gladius, in the Straits of Florida and adjacent waters. Fish. Bull. 9:89-816. VIALOV, Y.A, V.V. Ovchinnikov, 198. Main results of the tuna, swordfish and sailfish studies in the Atlantic research institute for the fisheries and oceanography (ATLANINIKO) for 2 years period (1957-1977). ICCAT. Col. Vol. Sci. Pap. Vol. IX. 1454

Table 1. Number of females, males, total (females+males) and overall sex ratio in percentage (SRo) by square of the North West Atlantic, for all size classes of swordfish sampled and for size classes >= 15 cm (LJFL). Area 14 NW 153 NW 14 NW 153 NW LJFL 5-35 cm 5-35 cm >= 15 cm >= 15 cm No. Females 67 185 38 11 No. Males 211 1374 74 781 Total Nº 278 1559 112 882 SRo 24,1 11,87 33,93 11,45 Table 2. Number of females, males, total (females+males) and overall sex ratio in percentage (SRo) for square 153 of the North West Atlantic and by month, for all size classes of swordfish sampled, for size classes <15 cm (LJFL) and for size classes >= 15 cm (LJFL). AREA= 153 NW OCTUBRE 15-35 cm < 15cm >= 15cm No. Females 27 11 16 No. Males 337 158 179 Total No. 364 169 195 SRo 7,42 6,51 8,21 NOVIEMBRE 15-35 cm < 15cm >= 15cm No. Females 97 44 53 No. Males 83 354 449 Total No. 9 398 52 SRo 1,78 11,6 1,56 DICIEMBRE 15-35 cm < 15cm >= 15cm No. Females 61 29 32 No. Males 234 81 153 Total No. 295 11 185 SRo 2,68 26,36 17,3 1455

Table 3. Overall sex ratio in percentage (SRo) and sex ratio at size (SRs) for both squares of the North West Atlantic Ocean and quarter (Q4). QUARTER 4 4 QUARTER 4 4 AREA 14 NW 153 NW AREA 14 NW 153 NW SRo 24,1 11,87 SRo 24,1 11,87 SRs SRs SRs SRs T5 T165 37,5 3,67 T55 T17 36,84 7,48 T6 T175 54,55 19,44 T65, T18 71,43 1, T7, T185 1, 18,75 T75, T19 1, 19,5 T8,, T195, 41,18 T85, T2 33,33 T9 5, 1, T25 1, 5, T95,, T21 1, 2, T1 7,69 4,35 T215 T15 6,67 5,88 T22 66,67 T11 16,67 11,11 T225 1, T115 25, 23,53 T23 T12, 12,5 T235 T125 9,9 6,98 T24 1, T13 13,33 9,21 T245 T135 17,39 11,11 T25 1, T14 47,37 16,28 T255 1, T145 33,33 16,2 T26 1, T15 8,7 9,55 T265 1, T155 13,33 7,94 T27 T16 28,57 6,88 T28 Table 4. Number of females of swordfish sampled, minimum, maximum and average gonadal index obtained for females >=15 cm (LJFL) in Q4 and by month for both squares of the North West Atlantic. AREA: 14 NW AREA: 153 NW OCTOBER OCTOBER NOVEMBER DECEMBER < 15 cm >=15 cm < 15 cm >=15 cm < 15 cm >=15 cm < 15 cm >=15 cm nº sam 29 38 11 16 44 53 29 32 mín GI,16,9,15,44,15,43,15,59 máx GI 3,38 2,33,28 12,99,7 17,77,62 11,85 ave GI,41 1,5,21 4,84,26 4,94,3 4,27 1456

25 2 SIZE DISTRIBUTION OF SWO. NORTH ATLANTIC. 14 NW F+M Males Females # Fish 15 1 5 T5 T7 T9 T11 T13 T15 T17 T19 T21 T23 T25 T27 T29 T31 # Fish 2 18 16 14 12 1 8 6 4 2 T5 SIZE DISTRIBUTION OF SWO. NORTH ATLANTIC. 153 NW T7 T9 T11 T13 T15 T17 T19 T21 T23 T25 T27 T29 T31 F+M Males Females Figure 1. Size distribution by sex and sex combined obtained for swordfish by squares 14 NW and 153 NW of the Atlantic Ocean in quarter 4 (Q4). : NORTH ATLANTIC. Cum. % % 1 9 8 7 6 5 4 3 2 1 14 NW 153 NW Figure 2. Cumulative percentage of size distribution of swordfish sampled by square in quarter 4 (Q4). T5 T7 T9 T11 T13 T15 T17 T19 T21 T23 T25 T27 T29 T31 153 NW. Cum. % by Month. Figure 3. Cumulative percentage of size distribution of swordfish sampled by month for square 153 NW. % 1 9 8 7 6 5 4 3 2 1 OCTOBER NOVEMBER DECEMBER T5 T7 T9 T11 T13 T15 T17 T19 T21 T23 T25 T27 T29 T31 1457

SEX-RATIO SWO. NORTH ATLANTIC. QUARTER 4. Figure 4. Sex ratio at size (SRs) of the swordfish obtained by square defined in the North West Atlantic areas, in quarter 4 (Q4). % Females 1 9 8 7 6 5 4 3 2 1 14 NW 153 NW T5 T65 T8 T95 T11 T125 T14 T155 T17 T185 T2 T215 T23 T245 T26 T275 T29 T35 T32 12 SWO Gonadal Index. 14 NW Gonadal Index 1 8 6 4 2 min GI max GI ave GI T1 T12 T14 T16 T18 T2 T22 T24 T26 T28 T3 T32 T34 2 SWO Gonadal Index. 153 NW Gonadal index 18 16 14 12 1 8 6 min GI max GI ave GI 4 2 T1 T12 T14 T16 T18 T2 T22 T24 T26 T28 T3 T32 T34 Figure 5. Gonadal indices (maximum, minimum and average) of female swordfish for each square monitored. 1458