Occurrence, Diet and Growth of Juvenile Blacktip Sharks ... - BioOne

Caribbean Journal of Science, Vol. 44, No. 3, 291-302, 2008 Copyright 2008 College of Arts and Sciences University of Puerto Rico, Mayagu¨ez

Occurrence, Diet and Growth of Juvenile Blacktip Sharks, Carcharhinus limbatus, from Los Roques Archipelago National Park, Venezuela RAFAEL TAVARES 1

Instituto Nacional de Investigaciones Agrícolas (INIA), Ministerio de Ciencia y Tecnología (MCT). La Asunción 6311, Isla de Margarita, Estado Nueva Esparta, Venezuela. Telephone: +58 295 2422220. Fax: +58 295 2420252. E-mail: [email protected] 2 Centro para la Investigación de Tiburones (CIT). Av. Don Bosco, Qta ABC, No. 10, La Florida, Caracas 1050, Venezuela.

ABSTRACT.—Distribution, occurrence, diet and growth of juvenile blacktip sharks, Carcharhinus limbatus, were examined based on specimens caught between 1995 and 2002 by the artisanal shark fishery from Los Roques Archipelago. Fishery monitoring revealed that C. limbatus was the species most frequently caught, accounting for 48.5% of the shark catch. Capture of neonate and juvenile sharks was concentrated in the central lagoon of the archipelago, indicating that this area corresponds to a nursery area for the species. Birth season was approximately from mid June to the end of August. Average length at birth was 63.5 cm TL, based on neonates with an open umbilical scar. The smallest mature male and female sharks measured 152 and 161 cm TL, respectively. Diet was composed of teleost fishes, with the most important prey being Eucinostomus argenteus (13.3 %IRI), Opisthonema oglinum (6.9 %IRI) and Gerres cinereus (5.5 %IRI). Monthly length frequencies revealed that juveniles remain within the nursery area for 14-16 months after birth, reaching a length of about 130 cm TL during this period. The growth of the juvenile population is characterized by a linear function, with sharks almost doubling their birth length during the first year of life. This growth was more rapid than the estimated rates reported from the Gulf of Mexico, western Florida and South Africa. The results suggest that growth rate is negatively correlated with latitude or positively correlated with temperature. The rapid growth shown by these juveniles will have positive implications for the recovery of the adult populations of this species. KEYWORDS.—Carcharhinus limbatus, diet, growth, nursery area, sharks, Los Roques

INTRODUCTION The blacktip shark, Carcharhinus limbatus, is a widespread species found on or adjacent to the continental and insular shelves of tropical and subtropical regions. In the western Atlantic, it is distributed from Massachusetts to southeastern Brazil, including the Gulf of Mexico and Caribbean Sea (Compagno 1984). Carcharhinus limbatus is one of the most important shark species caught by commercial longline and gillnet fisheries in the southeastern United States of America and Gulf of Mexico (Castro 1996; Castillo-Géniz et al. 1998). Likewise, on the northeastern coast of South America, between French Guyana and Brazil, this species is commonly caught in the commercial shark fishery conducted 291

by the Venezuelan gillnet fleet (Tavares 2005a). In the Caribbean region, it was reported as abundant around Venezuelan islands, where it was frequently captured by artisanal fisheries targeting sharks (Cervigón 1966). Currently, the blacktip shark is rarely observed among the sharks caught by diverse commercial fisheries operating in Venezuelan waters (Tavares 2005b; Tavares and Arocha 2007). Despite the commercial importance of this shark species in the western Atlantic, biological and fisheries information is scarce or nonexistent. The migratory behavior of C. limbatus is a factor that has impeded the study of its biology and ecological. Tag-recapture information has revealed a migratory route from the eastern coast of the USA to the Gulf of Mexico, and there is probably also a

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connection between these two regions and the Caribbean Sea (Castro 1996; Kohler et al. 1998). Studies on the biology traits of Carcharhinus limbatus, such as distribution, diet, reproduction and growth have been carried out in several regions of the Atlantic Ocean in order to generate the information required for stock assessment and for the design of management strategies. The diet composition and hence the feeding habits have been studied in the Los Roques Archipelago by Tavares and Provenzano (2000), and in the Gulf of Mexico by Barry (2002) and Bethea et al. (2004). The reproductive biology was described by Castro (1996) in the southeastern USA and by Capapé et al. (2004) on the western and northern coasts of Africa. Growth biology was examined by Branstetter (1987) in the Gulf of Mexico, Killam and Parsons (1989) on the west coast of Florida and Wintner and Cliff (1996) on the east coast of South Africa. More recently, life history traits were analyzed in order to determine the likelihood of separate stocks between two geographic areas, the eastern Gulf of Mexico and South Atlantic Bight (Carlson et al. 2006). Contributing to the reduction in global shark abundances is the high proportion of juvenile sharks caught by commercial fisheries and the degradation of nursery areas (Camhi et al. 1998). Shark nursery areas are geographically discrete zones where the gravid females give birth to their pups, and where the young spend their first weeks, months or years (Castro 1993). Nurseries are usually located in highly productive shallow water areas as coastal marshes, estuaries and lagoons which offer abundant food to the young, as well as protection against predators. The identification and delimitation of the areas inhabited by juvenile sharks are prerequisites for the design of conservation strategies, particularly for species heavily exploited by commercial fisheries (Rechisky and Wetherbee 2003). In recent years, biotelemetry has been used in extensive studies of the juvenile populations of Carcharhinus limbatus within their nursery areas (Heupel and Hueter 2002; Heupel and Simpfendorfer 2002, 2005). These studies have generated significant in-

formation regarding movement patterns, aggregation behavior and habitat use. Other studies have sought to characterize the genetic structure of juvenile populations of the blacktip shark in nursery areas distributed along the southeastern coast of the USA and the Gulf of Mexico (Keeney et al. 2003). MATERIALS AND METHODS The Los Roques Archipelago National Park is located in the Caribbean Sea, 160 km directly north of the central coast of Venezuela (11º43’-11º58’ N, 66º35’-6º57’ W) (Fig. 1). The archipelago occupies a total area of 2,251 km2 and comprises more than 40 small and low islands that are distributed around a main central lagoon. This semi-closed central lagoon covers an area of about 210 km2 with a maximum depth of 8 m, and it contains a large number of sand and coral banks. The water temperature ranges between 25 and 30 ºC, with the minimum values occurring in JanuaryFebruary and maximum values in JuneOctober. Los Roques Archipelago sustains an important marine biodiversity, with its ichthyological fauna comprising about 370 species, including 21 shark species (Ramírez and Cervigón 2004; Tavares 2005b). The data used in this paper were obtained from the local commercial fishery targeting sharks and during the following periods: April 1995-April 1996, September 1998-August 1999, January-November 2001 and March-August 2002. The Los Roques shark fishery employs artisanal bottom longlines of monofilament with 100 to 400 hooks (J-type, size # 3-5). A common characteristic of these longlines is the use of a section of stainless steel between the line and hook to avoid the escape of the sharks. The fishing vessels are mainly small wooden and fiberglass boats with outboard motors, ranging between 6 and 8 m long. Data collected during 2001 are the most complete, because they were obtained during intensive fishing monitoring as part of the shark program. Two relative abundance measures were used, the number of

BLACKTIP SHARKS AT LOS ROQUES, VENEZUELA

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FIG. 1. Map of the study area, Los Roques Archipelago, showing the catch distribution of Carcharhinus limbatus during the whole study period, 1995-2002. Map colors: black = islands or keys, dark grey = eastern coral reef barriers, light grey = shallow-water zones maximum depth 8 m. Symbols: CL central lagoon, + neonates and juveniles, □ adult males, 䡵 adult females, 䊊 fishing sets with positive catches for other shark species during the fishing monitoring in 2001.

individuals/100 hooks and the number of individuals/fishing set. In both cases, the relative abundance was calculated for each fishing operation and then averages were estimated by length classes of sharks. A tagging experiment of juvenile Carcharhinus limbatus was also conducted within the central lagoon of the archipelago with the assistance of the local fishermen to facilitate shark catches during 2001. Fishing sites were located around several coral banks located in the western end of the cen-

tral lagoon which is a common fishing area for C. limbatus. Fishing operations were always conducted during daylight hours, between 6:00 and 9:00 AM, and between 4:00 and 6:00 PM. On the basis of initial fishing results, it was determined that the optimal set time to avoid the death of the blacktip sharks was one hour. Two common shark tags were used (M dart-tag and plastic dart-tag), attached near the base of the first dorsal fin. To avoid injury and additional stress on captured sharks, the dart head of

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the tag was inserted between the skin and the muscle through an incision made by surgical scalpel. The data recorded for each specimen comprised sex, size (cm), weight (kg), and catch location (by GPS). The size measures used were the total length (TL) and fork length (FL) according to Compagno (1984). Neonates were identified by the presence of an open or partially closed umbilical scar. This ontogenetic stage lasts four to six weeks, until the umbilical scar is completely healed (Castro 1993). For discussion purposes, neonates were included in a juvenile group as a single stage prior to sexual maturation. Sexual maturity was assessed by the general development and characteristics of the reproductive organs in both sexes (Castro 1996). All biological measurements of the sharks were recorded by the same researcher. Regression techniques were applied between the most important biometric variables (FL vs. TL and TL vs. W), in order to obtain conversion equations. Differences between line regressions by sex were tested by analysis of covariance, ANCOVA (Zar 1996). During the period January-November 2001 period, stomachs were collected for analysis of diet composition. The prey items contained in the stomachs were identified to the lowest taxonomic level possible. The diet was analyzed quantitatively by applying the importance percentage indices by number (%N), by occurrence (%O) and by weight (%W). The index of relative importance (%IRI), which incorporates the previous three indices and facilitates comparisons among the contributions of different prey, was estimated (Cortés 1997). Growth analysis of Carcharhinus limbatus was based on the juvenile population and employed methods that required length and age information. Juvenile length structure (years combined) is graphically presented through histograms of monthly length frequencies. On the basis of these length frequency distributions, the relative ages (in months) were then assigned to the distinct groups. Since blacktip sharks are born mainly during July, this month was taken to be the arbitrary initial birth date (age-0). Therefore, neonate sharks observed

during June were excluded from the analysis. Juvenile growth rates by sample period and by sex were examined by regression analysis between the assigned ages and observed lengths. The resultant growth curves were statistically compared by an F-test (Zar 1996). A method based on tag-recapture information (Francis 1988) was also employed to examine the growth rates of the juvenile population. Because the data obtained from the tag-recapture procedure were insufficient for fitting the growth models with this method, analogous information was used based on the average length for the different age groups. For this approach, average lengths for the age groups (0-14 months) were estimated by applying a bootstrap resampling (n = 2000) routine of nonparametric statistics (Manly 1997). The variables required in this growth analysis are length at release (LM), length at recapture (LR) and period at liberty (T). It was assumed that these variables provide analogous information related to the difference between the monthly average length of the age groups and the time period between these groups (where T ⱖ 2 months). For example, the monthly average lengths for the age groups of 0 and 2 months comprise the lengths at release (LM) and at recapture (LR), where T is 2 months. Similarly, the monthly average lengths of the age groups of 0 and 3 months are taken to represent the lengths at release and at recapture of the next observation, where T is 3 months. All possible combinations among the average lengths of the age groups generated a total of 91 data, which are equivalent to the observations. This method (Francis 1988) incorporates a regression analysis by a maximum likelihood routine to fitting growth models, and involves estimates of growth parameters and measurement error. The expected individual growth increment (⌬Li), considering the length at release (Li), and the time at liberty (⌬Ti), is calculated by the following equation:

⌬Li =

冋

␤g␣ − ␣g␤ − Li g␣ − g␤

册冋冉

1− 1+

g␣ − g␤ ␣−␤

冊册 ⌬Ti


where g␣ and g␤ are the growth rates at two selected lengths (␣ = 65 cm TL and ␤ = 120 cm TL). The log likelihood function is: ␭

兺 log关共1 − p兲␭ + p Ⲑ R兴 i

i

␭i =

exp共−0.5共⌬Li − ␮i − m兲2 Ⲑ 共␴2i + s2兲兲关2␲共␴2i + s2兲兴0.5

where, v is the coefficient of variation of growth variability, m is the mean of the measurement error, s is the standard deviation of the measurement error, p is the contamination probability, R is the range of observed growth increments, µi is the expected value of growth increments, and ␴i is the standard deviation of the growth variability. The growth parameters were estimated by maximizing the likelihood value (␭) for each model using the solver function in MS Excel (Microsoft® Office Excel 2003). The likelihood ratio test (LRT), based on the statistical differences between the likelihood values, was applied to determine which model gave a significantly better fit (Francis 1988). All comparisons of the lengths and growth rates made in the present study were based on total length (cm TL). RESULTS During monitoring of local fishing in 2001, a total of 11 species of sharks (n = 637) were recorded. The most common in the catch composition were Carcharhinus limbatus (48.5%) and Carcharhinus perezi (38.2%). Other species commonly observed in the fishery were Ginglymostoma cirratum, Carcharhinus falciformis and Negaprion brevirostris which, together, represented 9.4% of the total catch. The distribution of fishing sets with positive catches for C. limbatus vs. other shark species caught during 2001 is shown in Fig. 1. During that year the total effort deployed was 158 fishing sets (26,896 hooks), of which 65 (10,360 hooks) were conducted within the central lagoon and the remainders were in areas around the eastern insular shelf of the archipelago. The

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relative abundance estimates by length classes of C. limbatus and other shark species showed that linehooks used by local fishermen selected a wide range of lengths, from small to large individuals (Fig. 2). Nevertheless, in the case of C. limbatus, 96.2% of those caught were neonates and juveniles captured within a specific area of the archipelago. A total of 861 specimens of Carcharhinus limbatus were examined during the complete study period, of which 849 were juveniles and 12 were adults. The relationship between the selected biometric variables and conversion equations are presented in Fig. 3. There were no significant differences between sexes for FL vs. TL or TL vs. W (ANCOVA, p > 0.05). All juveniles sampled were caught within the central lagoon of the archipelago and no captures of other species were observed during fishing operations carried out in this area during the study period. For the juvenile population, no significant differences in sex ratios were found for any of the sample periods (␹2-test, p > 0.05). In 1995, blacktip sharks were not examined for umbilical scar condition. Among the juveniles examined in subsequent surveys, 71 (53-71 cm TL) had an open or partially closely umbilical scar, suggesting that they were newborn individuals. In 1999, neonates were captured between 28 June and 16 August. In 2001, they were captured from 9 July to 1 September, and one shark with a recently closed umbilical scar was registered on 23 June. Sharks examined in

FIG. 2. Relative abundance estimates by length classes of Carcharhinus limbatus vs. other shark species caught during the year 2001 from the Los Roques Archipelago.

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F IG . 3. Biometric relationships and conversion equations between the variables selected (FL vs. TL, TL vs. Weight) for Carcharhinus limbatus from the Los Roques Archipelago.

the year 2002 were captured in August and had a recently closed umbilical scar, so these specimens were not considered to be neonates. On the basis of this temporal catch distribution of the neonates, it was deduced that the birth season of C. limbatus is approximately from mid June to late August, with most pups being born during July. The birth size estimated from the average lengths of the neonates was 63.5 ± 4.1 cm TL. All adult blacktip sharks were recorded during the year 2001 and these comprised seven males (152-188 cm TL) and five females (161-218 cm TL). Two females showed no sign of ovulation or recent mating, and the other 3 females were pregnant and carried embryos at advanced stages of development. These three pregnant females were caught in the months preceding the putative birth season; one female (173 cm TL) carrying 3 embryos was caught on

18 March, a second female (180 cm TL) carrying 5 embryos (38.0-38.6 cm TL) was caught on 20 March, and the third female (193 cm TL) carrying 4 embryos (43.4-45.0 cm TL) was caught on 4 April. Except for the pregnant female caught on 4 April, which was found at the southwestern edge of the central lagoon, all the adult sharks were observed in the northwest area of the archipelago (Fig. 1). The two smallest adult males examined (152 cm TL) were caught on 4 April and 9 August, and their clasper calcification and length, as well as their testis development, suggested that these specimens had only recently reached sexual maturity. Similarly, the smallest adult female (161 cm TL) examined on 19 March was classified as recently mature, on the basis of the development of the ovary, uterus and oviductal gland. Of 184 specimens (62-218 cm TL) examined for diet analyses in 2001, 71.73 % had empty stomachs. The prey items found were all teleost fishes, comprising 16 identified taxa together with unidentified teleost material (Table 1). The most important prey were the species Eucinostomus argenteus (13.32 %IRI), Opisthonema oglinum (6.88 TABLE 1. Diet composition of Carcharhinus limbatus in the Los Roques Archipelago, expressed as percentage by numbers (%N), frequency of occurrence (%O) and percent weight (%W). Also shown is the index of relative importance (%IRI), which incorporates the three previous indices. Prey items

%N

%O

%W

%IRI

Teleosts Eucinostomus argenteus 18.75 13.46 7.80 13.32 Opisthonema oglinum 9.38 9.62 9.81 6.88 Gerres cinereus 6.25 5.77 19.36 5.51 Haemulon spp. 9.38 7.69 4.30 3.92 Albula vulpes 6.25 7.69 5.70 3.43 Calamus bajonado 1.56 1.92 8.72 0.74 Archosargus rhomboidalis 3.13 3.85 1.96 0.73 Acanthurus chirurgus 1.56 1.92 8.51 0.72 Pomacentrus spp. 3.13 3.85 1.12 0.61 Lutjanus synagris 1.56 1.92 4.96 0.47 Sparisoma viride 1.56 1.92 2.41 0.28 Lutjanus spp. 1.56 1.92 0.94 0.18 Caranx hippos 1.56 1.92 0.84 0.17 Sparisoma rubripinne 1.56 1.92 0.73 0.16 Chaetodon striatus 1.56 1.92 0.65 0.16 Ablennes hians 1.56 1.92 0.51 0.15 Teleosts non-identified 29.69 32.69 21.67 62.58


%IRI) and Gerres cinereus. (5.51 %IRI). Other prey with relatively important values were Haemulon spp. (3.92 %IRI) and Albula vulpes (3.43 %IRI). The teleosts that remained unidentified because of their advanced stage of digestion represented the highest proportion of the diet (62.58 %IRI). The monthly length frequencies of juvenile Carcharhinus limbatus showed a bimodal distribution during June-November, leading to the recognition of two cohorts (Fig. 4). Cohort-1 comprises the new sharks of that year and cohort-2 constitutes the sharks that were born in the previous year. The sharks of cohort-2 were not observed after November because they had left the nursery area. Hence, after birth, juveniles remain within the central lagoon for about 14-16 months. Therefore, the ages of the groups were assigned as follows: cohorts 1 and 2 during July were aged 0 and 12 months, respectively; during August they were aged 1 and 13 months, respectively; and so on. Regression analysis of age against length revealed that juvenile growth was described by a linear model (Fig. 5). Differences between sample periods and between sexes were not significant (F-test, p > 0.05). Growth rate obtained by combining years and sexes was 4.12 cm/ month. Average lengths estimated by a bootstrap routine for the distinct age groups observed in the juvenile population are also shown in Fig. 4. In relation to the Francis (1988) approach, the results from the likelihood ratio test (LRT) indicated that the appropriate model contained the parameters g␣, g␤, v and s (Table 2). Growth rates estimated for individuals of 65 and 120 cm TL were 5.00 and 3.10 cm/month, respectively. Hence, this approach detected a slight decrease in growth rate along the length range examined. Between 26 January and 25 July 2001, a total of 31 juvenile blacktip sharks were tagged, comprising 16 males (64.5-95.6 cm TL), 14 females (62.5-95.0 cm TL) and one specimen of unidentified sex (81.0 cm TL). During the same year, seven recaptures (82.0-108.0 cm TL) were recorded through the monitoring of the shark fishing. The intervals in time and distance between

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tagged and recapture sites were 40-139 days and 0.7-3.0 km, respectively. Since each recapture was comparatively near the tagging site, juvenile individuals of this species appear not to travel far within the nursery. Individual growth rates obtained from tag-recapture data varied from 4.57 to 5.13 cm/month, with an average of 4.82 cm/month. DISCUSSION The monitoring of the local shark fishery deployed in the Los Roques Archipelago during 2001 indicated that Carcharhinus limbatus was the species most frequently caught, and its occurrence in the study area is limited to juveniles captured in a specific area of the archipelago. Considering the abundance of juvenile blacktip sharks in the archipelago, it might be expected that a significant number of adults would be caught by this local fishery, as occurs for example with the species C. perezi. However, a low number of C. limbatus adults was caught in the study area and this did not appear to be related to fishing effort or gear selectivity. The monitoring of other fishery activities targeting sharks off several Venezuelan oceanic islands has shown that adult C. limbatus were infrequently caught on the insular shelf of the Los Roques Archipelago (Tavares 2005b). Taking into account these findings and the migratory behavior of this species, it is probable that adult individuals are not common inhabitants of the study area. Furthermore, the fact that three of the five adult females were at similar stages of pregnancy during the months preceding the parturition season suggests that these females had arrived at the archipelago in order to give birth. The absence of captures of other shark species (juveniles or adults) within the central lagoon indicated that this shallowwater zone is a specific nursery area for Carcharhinus limbatus. This strategy associated with habitat use by juvenile sharks might reduce predation and competition, and might also ensure food availability during these early life stages. Other studies conducted with C. limbatus on the south-

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FIG. 4. Monthly length frequencies and relative abundance estimates by length classes of juvenile Carcharhinus limbatus within the nursery of the Los Roques Archipelago (years combined). Average lengths (AL, in cm LT) estimated by a bootstrap re-sampling (n = 2000) method are presented for each age group.


FIG. 5. Relationship between age and length for males (n = 459) and females (n = 390) of juvenile Carcharhinus limbatus sampled between 1995 and 2002 from the Los Roques Archipelago. Plotted line is linear regression fitted to data.

eastern coast of the USA and Gulf of Mexico have reported multispecific shark nurseries (Castro 1993; Heupel and Hueter 2002; Hueter et al. 2006). Juvenile populations of C. limbatus on the Gulf coast of Florida showed the highest rates of natural mortality (61-91%) caused mainly by predation, and an absence of correlation between neonate distribution and prey density suggested that predator avoidance would be an important factor in the selection of nurseries (Heupel and Hueter 2002; Heupel and Simpfendorfer 2002). In the

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case of the Los Roques Archipelago, it is probable that the juvenile population of C. limbatus experiences a low level of predation and competition within the nursery, since few if any adult individuals or other shark species are caught there. The birth season of Carcharhinus limbatus in the study area is approximately from mid June to late August, with a peak in the numbers of neonates seen in July. Similarly, new-born blacktip sharks were observed mainly during July in the tropical region off the western African coast (Capapé et al. 2004). However, off the southeastern coast of the USA and Gulf of Mexico, births occurred during May and June (Branstetter 1987; Castro 1996; Castillo-Géniz et al. 1998). This temporal variation in birth season among geographic zones could be principally conditioned by water temperature. In sub-tropical and temperate regions influenced by temporal climatic changes, the birth of sharks during spring months will allow the young to remain within the nurseries for a period of several months characterized by warm water. Castro (1993) stated that in temperate zones, winter temperatures force the young sharks out from the nurseries into deeper waters or to other areas. The birth size observed for C. limbatus in the Los Roques Archipelago is similar to

TABLE 2. Log-likelihood values (␭) resulting from the distinct growth models fitted to juvenile Carcharhinus limbatus from the Los Roques Archipelago and using the Francis (1988) method. Model 6 was selected through the likelihood ratio test (LRT). Model #

Parameters

LRT ␭

1

g65, s

−307.70

2

g65, s, v

−317.30

3

g65, s, v, m

−301.29

4

g65, s, v, m, p

−307.04

5

g65, g125, s

−263.61

6

g65, g125, s, v

−253.74

7

g65, g125, s, v, m

−253.64

8

g65, g125, s, v, m, p

−254.30

Models

⌬␭

␹2

p

1 vs. 2

9.59

19.19

0.000

2 vs. 3

16.01

32.01

0.000

3 vs. 4

5.75

11.51

0.000

4 vs. 5

43.43

86.87

0.000

5 vs. 6

9.87

19.74

0.000

6 vs. 7

0.10

0.20

0.652

7 vs. 8

0.67

1.33

0.247

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those recorded from other areas of the Atlantic Ocean (Castro 1996; Castillo-Géniz et al. 1998; Capapé et al. 2004). The sizes of the smallest adults recorded in the study area (152-161 cm TL) are comparable with the lengths at maturity reported for the northwestern Atlantic (130-150 cm TL; Branstetter 1987; Castro 1996; Castillo-Géniz et al. 1998; Carlson et al. 2006), but differ from those reported from African coasts (170-185 cm TL; Capapé et al. 2004). The diet of sharks of the genus Carcharhinus is typically dominated by teleost fishes (Wetherbee and Cortés 2004). Previous studies of C. limbatus have shown that clupeids such as herring and menhaden are among the most important prey groups: O. oglinum in the Los Roques Archipelago (Tavares and Provenzano 2000), Brevoortia tyrannus in the southeastern USA (Castro 1996) and Brevoortia patronus in the northeastern Gulf of Mexico (Barry 2002; Bethea et al. 2004). In the present study area, two main groups dominated the diet of the juvenile C. limbatus: the Gerreidae through consumption of E. argenteus and G. cinereus, and Clupeidae through consumption of O. oglinum. The high percentage of empty stomachs observed, combined with the frequent occurrence of prey items in advanced stages of digestion, was probably a consequence of the fishing method used. According to Wetherbee and Cortés (2004), the sharks attracted with bait (e.g. linehooks) were primarily those that had relatively empty stomachs. The use of gill nets would be the fishing method most appropriate for diet analysis in sharks. The growth biology of sharks is usually examined through non-linear models such as the von Bertalanffy relationship and its derivative functions. These procedures commonly require information on lengths and ages that includes individuals with asymptotic lengths, as well the use of ageing techniques based on analyses of calcified structures. Therefore, analysis of the growth of juvenile shark populations might require the use of other approaches. In the present study, it was possible to assign ages to the distinct size groups, owing to the clear pattern in the juvenile length structure and its evolution in relation to time.

Results showed that growth of juvenile Carcharhinus limbatus was best described by a linear model. Other studies conducted with Carcharhinus obscurus in southwestern Australia (Simpfendorfer 2000) and N. brevirostris in the Bahamas (Barker et al. 2005) also showed that juvenile growth during the first years of life was characterized by a linear function. Although regression analysis showed a constant growth rate, the use of the Francis (1988) method detected a slight decrease in growth rate between lengths of 65 and 120 cm TL, indicating that this approach can be a useful tool to detect smallest differences within the length range examined. A decrease in growth rate with ontogenetic development is biologically the more likely. Growth rate estimates for juveniles were supported by data from recaptured tagged individuals, although these recaptures were limited. Taking into account the growth rates obtained from all methods employed, young blacktip sharks appear to grow at about 5 cm/month during the first months of life, a rate that decreases to about 3 cm/month after the first year of life. This is more rapid juvenile growth than the rates reported for other geographic areas. In the Gulf of Mexico, juvenile blacktip sharks had a growth rate of about 20 cm/year (1.7 cm/ month) for the first 2 years of life, and of about 10 cm/year (0.8 cm/month) through adolescence (Branstetter 1987; Killam and Parsons 1989). In waters off South Africa, the rate was about 32 cm/year (2.7 cm/ month) during the first year of life and about 16 cm/years (1.3 cm/month) from then until attainment of sexual maturity (Wintner and Cliff 1995). Considering that Carcharhinus limbatus reaches ∼130 cm TL during a period of 1416 months, and the smallest mature individuals with unknown ages measured 152161 cm TL, it is reasonable to assume that this species in the study area would attain sexual maturity in about 2 years. The growth rate estimate (3.1 cm/month) from individuals of 120 cm LT supports this hypothesis. These findings contrast significantly with the age at maturity recorded for this species. Previous aging studies have determined that C. limbatus, reaches sexual


maturity on the southeastern coast of the USA and Gulf of Mexico after 4-7 years (Branstetter 1987; Killam and Parsons 1989; Carlson et al. 2006), and in South Africa after 6-7 years (Wintner and Cliff 1995). In fisheries science, geographic variation in biological parameters of the species can indicate separate stocks, and this feature is essential for resource assessment. Nevertheless, what happens with migratory species of sharks? It is reasonable to assume that at least the growth rate in these species varying according to geographic region or changes in latitude. Hence, variability in growth estimates for these migratory species (principally in juvenile populations) between regions would not necessarily indicate distinct stocks. The present study has demonstrated that significant differences exist in growth rate and age at maturity for blacktip sharks between tropical and subtropical-temperate regions in the northwestern Atlantic. The results suggest that growth rate of Carcharhinus limbatus is negatively correlated with latitude (or positively correlated with temperature). Conversely, a study conducted by LombardiCarlson et al. (2003) reported a positive relationship between growth and latitude for bonnethead shark, Sphyrna tiburo, along the eastern coast of the Gulf of Mexico. Those authors concluded that faster growth rates in individuals at high latitudes would be a mechanism to compensate the shorter growth season by growing faster during a shorter time period. In the case of C. limbatus, Carlson et al. (2006) detected no difference in life history traits of this species from the western coast of Florida and south Atlantic Bight. In any case, it is necessary to consider that a significant separation in latitude (of 15-25 degrees) exists between the Los Roques Archipelago and the Gulf of Mexico and southeastern coast of USA. To conclude, the results obtained in the present study reveal that the Los Roques Archipelago is an important habitat for juvenile Carcharhinus limbatus where parturition occurs and young sharks spend the initial phase of their life cycle. Furthermore, the rapid growth and sexual maturation exhibited by this species would have a positive implication for the recovery of the

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adult population in the area. In general, sharks are primarily characterized by slow growth; consequently, the populations have a lowest rate to increase in size when confronted with high levels of fishing pressure. Considering the fast growth and the highly migratory behavior of blacktip sharks, it can be concluded that the Los Roques Archipelago may function as an efficient producer of recruits for the adult populations of blacktips distributed throughout the Caribbean Sea and probably other areas of the western Atlantic. An immediate conservation measure that should be considered is the protection of the nursery area and the juveniles by establishing size limits and a closed season for C. limbatus in the Los Roques Archipelago. Acknowledgments.—This study was partially supported by the Oficina Nacional de Diversidad Biológica (Ministerio del Ambiente) through projects No. 2000-279 and 2001-0074. Research permits were given by the Instituto Nacional de Parques and the Instituto Nacional de la Pesca y Acuicultura. The shark tags used were provided through the collaboration of the Cooperative Shark Tagging Program/National Marine Fisheries Service of the USA. Thanks to the benefactor members of the Fundacion Cientifica Los Roques, which contributed with the flights to transport personnel and equipment during the research. Special thanks to L. Castillo-Géniz, A. Aranguren and A. Grant, who made invaluable revisions and suggestions to improve the manuscript. This research was possible thanks to the full cooperation of the fisher community of Cayo Fernando, Los Roques. LITERATURE CITED Barry, K. P. 2002. Feeding habits of blacktip sharks, Carcharhinus limbatus, and Atlantic sharpnose sharks, Rhizoprionodon terraenovae, in Louisiana coastal waters. Master Thesis. Louisiana State University. 72 p. Barker, M. J., S. H. Gruber, S. P. Newman and V. Schluessel. 2005. Spatial and ontogenetic variation in growth of nursery-bound juvenile lemon sharks, Negaprion brevirostris: a comparison of two ageassessing techniques. Environ. Biol. Fish. 72:343-355. Bethea, D. M., J. E. Buckel and J. K. Carlson. 2004.

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