SCRS/2011/021 Collect. Vol. Sci. Pap. ICCAT, 68(4): 1387-1396 (2012)

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SEX RATIO AT SIZE OF BLUE MARLIN (MAKAIRA NIGRICANS) FROM THE VENEZUELAN FISHERY OFF THE CARIBBEAN SEA

AND ADJACENT WATERS

Freddy Arocha1*, Luis Marcano2 and José Silva1

SUMMARY

Information on sex ratio at size of blue marlin (Makaira nigricans) from the Venezuelan pelagic longline fishery and the artisanal drift gillnet fishery is presented for the period 1991-2009. The document analyzes the spatial and temporal distribution of 1935 fish from the pelagic longline fishery and 19037 fish from the artisanal drift gillnet fishery. Results indicate sex ratio vary between fisheries; in the pelagic longline fishery sex ratio favored males throughout the season; but as not much in the artisanal drift gillnet fishery. Sex ratio at size was strongly favored towards males in specimens <200 cm LJFL in both fisheries and throughout the season. Spatial distribution of males and females is presented.

RÉSUMÉ

Des informations sur le ratio des sexes par taille du makaire bleu (Makaira nigricans) provenant des palangriers pélagiques et des pêcheries artisanales de filet maillant du Venezuela sont présentées pour la période comprise entre 1991 et 2009. Le document analyse la distribution spatio-temporelle de 1.935 spécimens capturés par les palangriers pélagiques et 19.037 spécimens capturés par les pêcheries artisanales de filet maillant. Les résultats indiquent que le ratio des sexes varie d’une pêcherie à l’autre ; le ratio des sexes présentait davantage de mâles pendant toute la saison dans la pêcherie palangrière pélagique mais dans une moindre mesure dans la pêcherie artisanale de filet maillant. Le ratio des sexes par taille présentait davantage de mâles de manière prononcée pour les spécimens de <200 cm LJFL pour les deux pêcheries et pendant toute la saison. La distribution spatiale des mâles et des femelles est présentée.

RESUMEN

Se presenta información sobre la ratio de sexos por talla de la aguja azul (Makaira nigricans) de la pesquería de palangre pelágico y de la pesquería artesanal de redes de enmalle de deriva de Venezuela para el periodo 1991-2009. El documento analiza la distribución espacial y temporal de 1935 peces procedentes de la pesquería de palangre pelágico y de 19037 peces procedentes de la pesquería artesanal de redes de enmalle de deriva. Los resultados indican que la ratio de sexos varía entre las pesquerías, en la pesquería de palangre pelágico la ratio de sexos favorecía a los machos durante toda la temporada, pero no tanto en la pesquería artesanal de redes de enmalle de deriva. La ratio de sexos era muy favorable para los machos en ejemplares <200 cm LJFL en ambas pesquerías y durante toda la temporada. Se presenta la distribución espacial de machos y hembras.

KEYWORDS

Blue marlin, sex ratio at size, Caribbean Sea, Venezuela

1Instituto Oceanográfico de Venezuela, Universidad de Oriente, Apartado de Correos No. 204, Cumaná 6101, Venezuela. *Corresponding author: farocha@sucre.udo.edu.ve / farochap@gmail.com 2 Instituto Nacional de Investigaciones Agrícolas, Cumaná 6101 – Venezuela.

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1. Introduction As in all billfish, it is a known fact that blue marlin display sexual dimorphism in size; i.e., female fish dominate against male in the catch, particularly as the size becomes larger. However, the size of fish from which they start to deviate from 1:1 is unclear as with most billfish species, due to the limited information available on sex ratio at size and the absence of appropriate samples of small size fish (<130 cm LJFL). Whether this dimorphism is due to differences in growth rate, natural mortality or vulnerability is not yet known. Circumstantial evidence suggest that the observed difference in sex ratio at size is probably due to sexually dimorphic growth patterns with females growing faster and achieving larger sizes than males (Mather et al., 1972; Chiang et al., 2004) or the possibility of different natural mortality rates, as suggested for swordfish in the North Atlantic Ocean by Restrepo et al. (1991). In the recent statistical models used to assess tuna species in the eastern Pacific Ocean (Anon. 2002a and Anon. 2002b), sexual dimorphism is used to explain the different natural mortality rate by sex (Miyabe, 2003). Similar statistical model are being developed for Atlantic bigeye tuna (Miyabe, 2003), and sex-specific VPA assessment was used for Atlantic swordfish (Anon., 1999, 2000). Therefore, sex ratio at size data which well represents the overall stock is important. ICCAT’s Enhanced Billfish Research Program in Venezuela started compiling size data by sex since 1991, and those data for blue marlin caught by the Venezuelan fishery are analyzed in this document. 2. Materials and methods Blue marlin size by sex was obtained from two fisheries: the Venezuelan pelagic longline fishery that targets primarily tropical tunas, based out of Cumaná and Puerto La Cruz in northeastern Venezuela, and the artisanal drift gillnet fishery based at Playa Verde (east of La Guaira) in the central coast of Venezuela which targets billfish. Size by sex data was recorded by scientific observers while aboard Venezuelan fishing vessels operating in the western central Atlantic between 5°N and 25°N (west of 40°W), and by trained port samplers at the community of Playa Verde from artisanal catches around La Guaira Bank. Sex determination was based on macroscopic characteristics; although the accuracy of sex data for the smaller size fish (<130 cm LJFL) may be biased due to the subtle differences between sexual organs. A total of 20972 blue marlins were measured and examined for sex determination between 1991 and 2009. The sex ratio data was calculated as the number of females divided by the sum of male and female, and categorized by 5 cm (LJFL) length class. Due to the unbalanced number of samples in all years, the annual changes of seasonal pattern seemed unlikely. Instead, sex ratio data were summed over all years and shown as quarterly sum based on the proportion of females partitioned into four quarters for all years combined. A locally weighted regression (Venable and Ripley, 1999) was fitted to the proportion of female data to observe trend patterns; 95% confidence intervals about proportions were calculated following Brown et al. (2001). 3. Results and discussion The trend in annual and monthly size of blue marlin by sex is presented for each fishery (Figure 1). The annual trend in size of most of the fish caught by the artisanal drift gillnet fishery has remained stable around 175 cm LJFL in males and 200 cm LJFL in females (Figure 1A). However, the number of large males present in the early years of the fishery has decreased in recent years; in contrast there has been an increase of small males in the catches of recent years. Similarly, the monthly trend in size caught by the artisanal fishery has remained stable like the annual trend. It was noticeable, although small in numbers, that large males (>300 cm LJFL) were present during most of the year. The female trend in size did not show any particular pattern in either time step. The size trend in the fish caught by the pelagic longline fishery showed some variability in the annual time step as well as in the monthly trend (Figure 1B). The majority of the males caught annually were around 175 cm LJFL, with large males (>250 cm LJFL) been most frequent during the first 10 years of the fishery. While the annual trend in females varied over the years, mostly around 175-200 cm LJFL; like in the males, several large females were also found at the beginning of the time period. The seasonal trend in size from the pelagic longline fishery showed some variation in the females where size increased during the summer months (July-September), and large females (small in numbers) were present through November. This seems to coincide with large males appearing during the same months, although the trend in male size was similar to that of the females (175-200 cm LJFL) for all months.

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Overall sex ratio for blue marlin caught by the two Venezuelan fisheries was 0.440, indicating some dominance of male fish over female. However, this overall proportion was dominated by the weight of the artisanal fishery, in which the next to most common species of the billfish catch is blue marlin (Marcano et al., 2010). In the artisanal fishery the overall sex ratio was 0.453, although the sex ratio favored the females during the 3rd quarter of the year, while during the rest of the time the sex ratio favored the males (Table 1). In contrast, in the pelagic longline fishery, the overall sex ratio was 0.343, indicating a strong dominance of males which remained stable throughout the year. Seasonal (quarterly) sex ratio by size for both fisheries combined is given in Figure 2. Throughout most of the season the trend in the overall sex ratio at size is ‘S’ shaped; i.e., the bottom portion is formed mostly by male fish of <200 cm LJFL, and the upper portion is mostly formed by female fish of >250 cm LJFL. While sex ratio at sizes between 200 and 250 cm LJFL show a steep increase with size. Only during the 4th quarter a reduction in the dominance of males was observed for sizes <160 cm LJFL, but the number of fish was small as indicated by the broad confidence intervals. On the opposite end, there appear to be some large males that tend to force down the locally weighted regression trend, but this is mostly caused by the very low numbers observed which were usually <5. Although it is possible to have large size males, the majority of large size fish (>300 cm LJFL) are females. Seasonal (quarterly) sex ratio by size and by fishery is shown in Figure 3. Seasonal sex ratio at size from the artisanal fishery mimics the overall sex ratio due to the unbalanced sample size between fisheries caused by the nature of the artisanal fishery (i.e., targets billfish in a ‘billfish hot spot’, and uses net gear). In contrast, seasonal sex ratio at size from the pelagic longline fishery displayed a notably different trend from that of the artisanal fishery. The trend in the pelagic longline fishery varied seasonally, but for fish size between 170 and 210 cm LJFL sex ratio strongly favored males throughout the seasons. As size increased, the trend also increased favoring female fish. Unlike in the artisanal fishery, only few large males were observed. However, at sizes <170 cm LJFL the trend in sex ratio increased towards the 1:1 ratio as the sizes decreased, noticeably during the 2nd , 3rd , and 4th quarter, but during the 1st quarter the trend was inverted favoring males for sizes 140-160 cm LJFL. This seasonal sex ratio pattern seem to follow the general expected pattern (i.e., female fish dominate against male in the catch), as observed in white marlin (Arocha & Barrios, 2009). However, some differences in the sex ratio trend were observed between fisheries which may be due to the selectivity of the gear, and the spatial distribution of the fish caught by the longline gear. The quarterly spatial distribution of sex ratio is shown in Figure 4. It should be noted that squares with 0 shading sex ratio means that only males are present in that square. During the first quarter, the sex ratio is characterized by an important presence of males in the central Caribbean Sea and the area west of Venezuela (in the Atlantic side), female dominant sex ratio appear scattered during this time period. In the second quarter, there is an increase in female dominant sex ratio in the Caribbean Sea, but the sex ratio north-northeast of the Hispaniola and Puerto Rico is dominated by males. The sex ratio in the Venezuelan western side appear to be equally shared by areas favoring male and female sex ratios, but in the third quarter the pattern shifts towards an area where the sex ratio is mostly dominated by females. While the sex ratio in the Caribbean continues to be favoring females, but northeast of the Antillean arc males dominate the sex ratio. In the fourth quarter, most of the fishery is centered in the Caribbean Sea and in the Atlantic side of Venezuela, and the sex ratio is somewhat similar as in the previous quarter, with less dominance of females in the Atlantic side. It becomes clear that there is temporal and spatial differentiation in the sex ratio, as well as in the sex ratio at size, and between fisheries. Some differences may not be explained due to the unbalanced number of samples in all years, but other variation can be explained by inferring from the available life history information from the area and the movement patterns observed from fish tagged with conventional tags. Blue marlin movements from conventional tagging has been significant between the US mid-Atlantic coast, and the Gulf of Mexico to Venezuelan waters (Ortiz et al., 2003), and it has been hypothesized that the concentration of blue marlin in the Caribbean correspond to spawned fish moving towards feeding areas to restore energy loss due to spawning (Arocha and Marcano, 2008). Blue marlin spawning grounds in the North Atlantic are not well defined, however, inferring from spawning fish caught and larvae samples, spawning areas are to be located in the tropical western areas of the Atlantic, most likely between 17°N and 32°N west of 60°W, during warm months with SST of 27-30°C (Arocha and Ortiz, 2006).

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Therefore, most of the blue marlin caught by the Venezuelan fisheries are males of different stages of maturity that inhabit warm waters year round with an ample supply of food resources due to the prevailing oceanographic conditions in the southeastern Caribbean Sea (i.e., upwelling during the first part of year and Orinoco river influence in the second part of the year (Cherubin and Richardson, 2007; Aparicio, 2003), resulting in a continuous process of enrichment that will attract prey species year round (Varela et al., 2003; Mendoza, 1993). Mature males will probably move north towards spawning grounds during the warmer months, to an area known for spawning fish – off north of Puerto Rico (Erdman, 1968). Hence the male dominant sex ratio during the 2nd and 3rd quarters in the Atlantic area north – northeast of the Hispaniola, Puerto Rico and Antillean arc, and the strong dominance of males in the sex ratio for sizes 185-205 cm LJFL during the 2nd quarter in fish caught by the longline fishery. The spatial distribution of the sex ratio in favour of females (>0.51) appears to increase during the 2nd quarter from the northern Atlantic area outside the Caribbean into the Caribbean and towards the area of the Atlantic off eastern Venezuela during the 3rd quarter, most likely are mature specimens (>200 cm LJFL) that seem to increase in numbers during the third quarter, as indicated by the catches from the longline fishery. Spawning is presumed to take place off north of Puerto Rico during the 2nd and 3rd quarter, thus the fish caught in the Caribbean and off eastern Venezuela are likely spawned fish that come into the enriched tropical waters to feed. An additional line of evidence is a fish (most likely a mature young female ~200 cm LJFL) that may have spawned in September off north of Puerto Rico, was tagged with a PSAT tag (E. Prince, personal comm.) displaying a trajectory that took the fish from the spawning area into the Caribbean Sea and then onto the enriched waters off the continental shelf influenced by the Amazon river plume. Although the information from the PSAT tagged fish does not indicate sex, and no other information other than the trajectory over 124 days at large. It does contribute to the hypothesis that young mature females (200-275 cm LJFL) after spawning off Puerto Rico come into the Caribbean and the warm Atlantic waters influenced by the large rivers (Orinoco and Amazon; Corredor et al., 2004; Muller-Karger et al., 2001) to feed, likely to replenish energy after a protracted spawning season. Additionally, variations in the sex ratio-at-size has also been used to discern spatial patterns in spawning (Mejuto et al., 1994), which can lead to develop models to separate the catch-at-size by sex that would allow potentially unbiased length/age structured assessments models. However, the information needed for a similar exercise would require a similar amount of information from other fleets so a full analysis can be performed. Finally, it should be noted that sex ratio information can be added to estimates of reproductive potential to calculate female spawning biomass, which can produce some difference in the perception of stock status relative to a selected Biological Reference Points, as has been pointed out for some fish stocks (Morgan, 2008). The recent literature has shown that taking into account the variation in reproductive biology can have a major impact on advice for fisheries management. Thus, to further research on the methods used to estimate reproductive characteristics such as maturation, sex ratio, and fecundity, for a species with dimorphic growth and a variable proportion of females-at-size, it would be necessary to broaden the geographical scale to better define the timing and the locations of bleu marlin spawning in the Atlantic Ocean. The results can produce robust estimations of reproductive metrics necessary to incorporate them for better scientific advice. 4. References Anon. 1999, Report of the ICCAT Meeting for the Development of Standardized Methods for Estimating

Swordfish Catch at Age by Sex (Hamilton, Bermuda, 21-27 January, 1998). Collect. Vol. Sci. Pap. ICCAT, 49: 211-321.

Anon. 2000, Detailed Report on Swordfish: Report of the ICCAT Swordfish Stock Assessment Session (Madrid,

Spain, September 27-October 4, 1999). Collect. Vol. Sci. Pap. ICCAT, 51: 1001-1208. Anon. 2002a, Status of yellowfin tuna in the eastern Pacific Ocean in 2001 and outlook for 2002. Background

paper A2 presented at the 69th Annual Meeting of the IATTC. June 2002. 66pp. Anon. 2002b, Status of bigeye tuna in the eastern Pacific Ocean in 2001 and outlook for 2002. Background paper

A4 presented at the 69th Annual Meeting of the IATTC. June 2002. 84pp.

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Aparicio, R. 2003, Revisión de las características oceanográficas de la plataforma nororiental de Venezuela. En: Fréon, P. & J. Mendoza (Eds.). The sardine Sardinella aurita its exploitation and environment in eastern Venezuela. Editions IRD, Paris. 550 p.

Arocha, F., and Barrios, A. 2009, Sex ratios, spawning seasonality, sexual maturity, fecundity of white marlin

(Tetrapturus albidus) from the western central Atlantic. Fish. Res., 95:98-111. Arocha, F., and Marcano, L. 2008, Life history characteristics of blue marlin, white marlin, and sailfish from the

eastern Caribbean Sea and adjacent waters. Pages: 1481-1491 in J. Nielsen, J. Dodson, K. Friedland, T. Hamon, N. Hughes, J. Musick, and E. Verspoor, eds. Proceedings of the Fourth World Fisheries Congress: Reconciling Fisheries with Conservation. American Fisheries Society, Symposium 49, Bethesda, Maryland.

Arocha, F., and Ortiz, M. 2006, Blue marlin. In: ICCAT Manual, Chapter 2.1.7. ICCAT, Madrid, Spain.

http://www.iccat.int/Documents/SCRS/Manual/CH2/2_1_6_BUM_ENG.pdf Brown, L.D., Cai, T.T. and DasGupta, A. 2001, Interval estimation for a binomial proportion. Stat. Sci., 16:101-

133. Corredor, J., Morell, J., Lopez, J. Capela, J. and Armstrong, R. 2004, Cyclonic eddy entrains Orinoco river

plume in eastern Caribbean. EOS, 85:197-208. Cherubin, L. and Richardson, P. 2007, Caribbean current variability and the influence of the Amazon and

Orinoco freshwater plumes. Deep-Sea Res. part I, 54:1451-1473. Chiang, W., Sun, C., Yeh, S. and Su, W. 2004, Age and growth of sailfish (Istiophorus platypterus) in the waters

off eastern Taiwan. Fish. Bull., 102:251-263. Marcano, L., Arocha, F., Alió, J., Marcano, J., Gutierrez, X. and Vizcaino, G. 2010, Actividades desarrolladas en

el Programa de Investigación Intensiva sobre Marlines en Venezuela. Col. Vol. Sci. Pap. ICCAT, 65:1824-1832.

Mather, F.J., Jones, A. and Beardsley, G.L. 1972, Migration and distribution of white marlin and blue marlin in

the Atlantic Ocean. Fish. Bull. 70, 283–298. Mejuto, J., de La Serna, J.M., García, B., Quintans, M. and Alot, E. 1994, Sex ratio at size of the swordfish

(Xiphias gladius L.) in the Atlantic and Mediterranean Sea: similarity between different spatial-temporal strata. Collect. Vol. Sci. Pap. ICCAT, 42, 322–327.

Mendoza, J. 1993, A preliminary biomass budget for the northeastern Venezuela shelf ecosystem. En:

Christensen,V, and Pauly, D. (Eds), Trophic models of Aquactic Ecosystem. ICLARM Conference Proceedings 26, pp. 285-297,390.

Miyabe, N. 2003, Recent sex ratio data of the bigeye tuna caught by the Japanese longline fishery in the Atlantic.

Collect. Vol. Sci. Pap. ICCAT, 55(5): 2028-2039. Morgan, M.J., 2008, Integrating reproductive biology into scientific advise for fisheries management. J. Northw.

Atl. Fish. Sci., 41:37-51. Muller-Karger, F. Varela, R., Thunell, R., Scranton, M., Bohrer, R., Taylor, G., Capelo, J., Astor, Y., Tappa, E.,

Ho, T. and Walsh, J. 2001, Annual cycle of primary production in the Cariaco Basin; response to upwelling and implications for vertical export. J. Geosphys. Res., 106:4527-4542.

Ortiz, M., Prince, E.D., Serafy, J.E., Holts, D.B., Dary, K.B., Pepperell, J.G., Lowry, M.B. and Holdsworth, J.C.

2003, Global overview of the major constitutent-based billfish tagging programs and their results since 1954. Mar. Freshwater Res., 54:489-507.

Restrepo, V. 1991, Some possible bias in swordfish VPAs due to sexually dimorphic growth. Collect. Vol. Sci.

Pap. ICCAT, 35: 338-345.

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Varela, R., Carvajal, F. y Müller-Karger, F. 2003, El fitoplancton en la plataforma nororiental de Venezuela. En: Fréon, P. & J. Mendoza (Eds.). The sardine Sardinella aurita its exploitation and environment in eastern Venezuela. Editions IRD, Paris. 550 p.

Venable, W., and Ripley, B. 1999, Modern applied statistics with S-plus. Springer. 501 pp. Table 1. Seasonal blue marlin sex ratio at size (proportion of females) by fishery (artisanal and pelagic longline-VPLOP), obtained from ICCAT’s Enhanced Billfish Research Program in Venezuela between 1991 and 2009.

Artisanal VPLOP Combined

1st quarter 0.401 0.308 0.394 2nd quarter 0.440 0.309 0.429 3rd quarter 0.619 0.393 0.577 4th quarter 0.444 0.350 0.426 Total

0.453 0.343 0.440

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Figure 1. Box-plots of annual and monthly blue marlin size by sex obtained from ICCAT’s Enhanced Billfish Research Program in Venezuela between 1991 and 2009 (A, artisanal drift-gillnet; B, pelagic longline).

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Figure 2. Overall blue marlin seasonal sex ratio by size, obtained from ICCAT’s Enhanced Billfish Research Program in Venezuela between 1991 and 2009.

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Figure 3. Seasonal blue marlin sex ratio by size by fishery (artisanal left, VPLOP right), obtained from ICCAT’s Enhanced Billfish Research Program in Venezuela between 1991 and 2009.

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Figure 4. Seasonal (by quarters) and spatial distribution of blue marlin sex ratio (as proportion of females) displayed in 1 degree grids, obtained from Venezuelan Pelagic Observer Program (VLPOP) between 1991 and 2009.

 

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