Journal of & Marine Biology

Reproductive Biology of Blue runner, crysos (Mitchell, 1815) From the Coastal Waters of Rio Grande do Norte, (Southwest Atlantic )

Abstract Research Article

Reproductive biology of blue runner, Caranx crysos was investigated, based on the total body length, body weight, sex ratio, size at first sexual maturity, macroscopic Volume 5 Issue 6 - 2017 fecundity and the spawning season. The length-weight relationship for grouped sexdevelopmental was W=0.0346.LT stages 2.6717of gonads,. The sexovarian ratio histology,of the sampled gonadosomatic population index (n=116) (GSI), was 1: 1.1 without any significant difference from the expected sex ratio. First Departamento de Oceanografia e Limnologia, Centro de sexual maturation in males and females occurred at 331 mm of total body length. Biociências, Universidade Federal do Rio Grande do Norte, The macroscopic characteristics of gonad development indicated immature, Brazil maturing, mature and spent stages. Histological analyses of ovary indicated the following oocyte developmental stages: early and late primary growth stage, *Corresponding author: Sathyabama Chellappa,

Biociências, Universidade Federal do Rio Grande do Norte, mostcortical part alveolar of the stageyear, otherand early than and during late vitellogenicFebruary and growth October. stages. This GSI attained has Brazil,Departamento Email: de Oceanografia e Limnologia, Centro de peak values from April to June and in January. Mature fish occurredC. crysos during has a high reproductive output, providing population increase and exploitation of the Received: May 29, 2017 | Published: June 08, 2017 environmentala prolonged reproductive resources. period with peak periods of activity.

Keywords: Reproductive aspects, Maturity stages, Ovarian histology, Size at first maturity, Caranx crysos

Introduction Tunisia, Eastern Mediterranean [4] and from Porto Rico [10]. Sex ratio, spawning and maturity of C. crysos from the Gulf of Off the Brazilian coast, the Caranx, belonging to the family Mexico has been investigated [11]. The reproductive biology and Caranx crysos (Micthill, histological characteristics of female C. crysos from the Egyptian 1815), C. ruber (Bloch, 1793), C. hippos (Linnaeus, 1766), C. latus has been studied [12]. However, there is , is represented by five species: Agassiz, 1831 and C. lugubris Poey, 1860 [1]. Carangid species are scarcity of information on the reproductive biology of C. crysos C. crysos populations from Southwest Atlantic Ocean. Considering this and was amongst the most sampled carangid species landings during among the main fishing resources marketed in Brazil. the Research Project Revizee Score-NE, Brazil [2]. of Brazil, the present study aimed to investigate its reproductive the importance of this species in the commercial fish landings Blue runner, Caranx crysos is an important demersal species biology. This study presents information on the body size, length- weight relationship, type of growth, sex ratio, length at the onset in the fisheries and is commonly known as blue stripe jack, across the Atlantic Ocean, ranging from Brazil to Canada in the sexual maturity (L ), macroscopic developmental stages of westernEgyptians Atlantic cad, hard and tail from jack and hard to nose. Great It Britain is widely including distributed the 50 Mediterranean in the eastern Atlantic [3]. C. crysos is captured by of maturity stages and reproductive period of C. crysos, from thegonads, coastal ovarian waters histology, of Rio Grande fecundity, do GSI,Norte, monthly Brazil distribution(Southwest Atlantic Ocean).The description of the reproductive biology of C. using haul seines, lampara nets, purse seines, gill nets, and hook offshore environments, predominantly around large man made crysos is presented in to clarify characteristics related to its and line [4]. It is a schooling fish, which inhabits both inshore and offshore structures, such as petroleum platforms. Juveniles of C. reproduction. crysos end to inhabit shallower reef and lagoon waters whereas adults move to deeper waters [5]. Materials and Methods Sampling fundamental importance to understand the life history strategy Information on the reproductive biology of fish is of The state of Rio Grande do Norte is located in Northeastern [6-9]. There are reports on annual reproductive cycle, spawning C. periodicityand to take necessaryand sexual measures maturity forof C. management crysos from theand Gulf conservation of Gabes, crysos Brazil and has a coast of approximately 420 km. Specimens of were captured by experimental fishing, on a monthly basis

Submit Manuscript | http://medcraveonline.com J Aquac Mar Biol 2017, 5(6): 00136 Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 2/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

with Hematoxylin-Eosin (HE) and periodic acid Schiff (PAS). was carried out along the coast of Rio Grande do Norte, Brazil The histological description of the developmental stages and (situatedduring the between period of latitudesJuly, 2013 4°40’0’’to June, 2014.S e 6°20’0’’S,Experimental longitudes fishing 37°0’0’ and 35°0’0’ W). [18,19]. classification were performed using the existing terminology Fishing operations were carried out at depths ranging from Fecundity The oocytes from mature ovaries were dissociated using 5 to 52 m utilizing vessels of the artisanal fleet, which operate Gilson solution, and three sub-samples of 0.1 g were extracted. netswith bottomvaried from gillnets. 800 The to nets3600 were m, with made mesh of monofilament size varying nylonfrom The oocytes were counted using Bogorov counting chamber, a 45and to were 60 mmset onand the about bottom 2meters of the in sea. height. The lengthGillnets of were the fishing set in stereomicroscope and an ocular micrometer. Total fecundity the late afternoon on the bottom of the sea and were collected was estimated for the total weight of the ovaries. Fecundity = approximately two hours later. [(number of mature oocytes in the fragments of ovary) x (total weight of ovary)] / (weight of the fragment of the ovary) [20,21].

was measured to the nearest millimeter (Lt ± 1 mm) and total Gonadosomatic index (GSI) and reproductive period bodyCaptured weight fishwas weremeasured numbered, to the nearest total length gram of(Wt each ± 1 fishg). Morphometric measurements and meristic counts were carried 100[22].The gonadosomatic The breeding indexperiod (GSI) was was determined calculated by as: the GSI temporal = weight relativeof ovary frequency (g) / body distribution weight of fishof the (g) different - weight stages of gonads of gonadal (g) x out on fish to confirm the of the study species using the ice were and dissected. The location and general aspects of the maturation [23]. gonadsidentification were observed.keys [13]. AfterFish werewhich, brought the gonads to the were laboratory removed, on Statistical analyses

spaceweighed occupied (Wg ± 0.1 in g), the and coelomic sex identified. cavity Theand stage presence of reproductive of visible maturity was verified by characteristics, such as colour, shape, transformed when necessary. Pearson correlation tests were conductedDistributions to determine of raw datathe werecorrelation checked between for normality weight and possible to determine their sex by macroscopic observation. oocytes [6]. Immature individuals were not included as it was not length. The chi-square (χ² Size range and Length-weight relationship level of 5% to test any difference in the sex ratio. A Student t-test was used to verify the difference) test wasbetween applied the attotal a significancelength and ­ performed using the absolute frequencies (mean ± SD) in different The results are presented as a mean ± SD. Analysis of covariance Distribution analysis of total length and weight of each fish was classes of total length (Lt) and total weight (Wt). The total length (ANCOVAbody mass General of males Linear and females,Models procedure) at a significance was used level to of 5%.test data of males and females was grouped into class intervals of the differences between a and b values from males and females 50 mm. The length-weight relationship was determined by the growth curve. Furthermore, General Linear Models [24] was used b equation Wt = a. Lt , where Wt is the total weight (g), Lt is the total to model the expected total length (normal model and identity length (cm), a or regression [14]. The Huxley´s equation (W=a.Lb) was used to is the intercept and b is the coefficient of growth adjust length-weight model [15]. thatlink explain function). the The variability level of in significance the response was variable set at in 5% the for model the identification of statistically significant factors and coefficients Sex ratio of GLM. The Kolmogorov-Smirnov test was used to test the Sex ratio between males and females (M:F) was obtained these models to the data. The proposed model has the following through the relative frequency distribution analysis of males and structurenormality in of its the covariables: estimated Y residuals=+++β Sex GLMs, SM checking Sex* SM the where fit of females during the study period. β is an intercept term, SM is a stage of maturation.

Length at first sexual maturity Results ) where 50% of the 50 Body size (Length-weight) and size range individuals exhibited maturing gonads was estimated from the relativeBody frequency size at first distribution gonadal maturityof adult males (L and females, using A total of 116individuals of C. crysos were examined (56 their standard length classes (mean ± SD) [16]. males and 60 females). Number of males and females of C. crysos sampled each month is shown in Table 1. Macroscopic description and histology of gonads All individuals captured were above 200 mm of total length. The macroscopic developmental stages of gonads were Total body length of males varied from 283 to 435 mm and their determined by their characteristics [17,6]. Fragments of female body weight varied from 168 to 843g. The total body length of females varied from 230 to 480mm and their body weight varied solution for 12-24 h (depending on size), washed for 24 hours gonads selected for histological analysis were fixed in Bouin the total body length (f=0.019, df = 115, p > 0.05) and body weight preserved in 70% Ethyl alcohol. Fragments of ovaries were (fromt =1.159, 136 todf =1040g 115, pThere > 0.05) was of nomales significant and females. differences Figure between 1 shows in running water to remove excess fixative and were later

embedded in paraffin, sectioned at 3-5 μm thickness, and stained

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 3/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

the distribution of body length and body weight classes of males Length-Weight relationship and type of growth and females. weight relationship of males and females (F=3.889; p=0.051). TheThere length-weight was no relationship significant differencesshowed positive between correlation the length- with 2) of 0.916 for grouped sex. The length-weight relationship for grouped sex was W= 0.0346.LT2.6717 (Figurea coefficient 2). of determination (r

Figure 2: Length-Weight relationship for pooledsexes of Caranx crysos captured during July, 2013 to June, 2014from the coastal waters of Rio Grande do Norte, Brazil. Sex ratio The sex ratio of the sampled population was 1: 1.1 without any

ratio of 1M:1F(χ²= 0.21). Figure 3a shows the distribution of the frequencysignificant differenceof occurrence between males the and sexes females in relation on a tomonthly the expected basis. Figure 1: Size distribution frequency of male and female Caranx Neither of the sex predominated during the study period. Figure crysos during July, 2013 to June, 2014 (a) total length, (b) body weight. 3b shows the frequency of occurrence of males and females Data= means (columns). distributed according to total length classes. Females were more Table 1: Number of males and females of Caranx crysos sampled each in number in the total length classes. month during July, 2013 to June, 2014 from the coastal waters of Rio Grande do Norte, Brazil. The GLM model established for the total length indicated that the intercept(P=1.51 E-12) and the maturation stage(P=0.306) Total Fish sampled Month Males Females and the interaction between sex and maturation stages (P = Jan 7 5 are statistically significant (Figure 1). However, sex (P = 0.285), model adjusted fairly to the data (Figure 2), presenting normal Feb 0 1 distribution(KS=1.265;0.306) were not statistically P =0.082). significant Since the (Table applied 2). test The showed GLM Mar 6 3 Apr 9 11 the interaction of sex in relation to the maturation stages, the no significant differences in length for males and females, and May 6 12 considering the pooled sexes. Jun 11 4 curve for first reproduction of the study species was estimated Table 2: General results of the GLM analysis for the expected total length Jul 1 1 of Caranx crysos Aug 4 3 (normal modelWald and identity Chi-Square link function).df P Sep 9 11 240.09 1 1.510E-12 Oct 1 1 InterceptSex 1.14 1 0.285 Nov 0 4 Stageofmaturation 7.72 3 0.005 Dec 2 4 Sex * Stageofmaturation 1.05 5 0.306 Total 56 60

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 4/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

Macroscopic characteristics of gonads and frequency of maturity stages The macroscopic characteristics of gonads of C. crysos indicated four developmental stages for males and females:

reddishimmature, in colour,maturing, of increased mature andsize spent.with visible Immature oocytes. ovaries The spentwere of small size and filiform. Maturing and mature ovaries appeared males were not used in this study. The testes were of different ovaries were reduced size with flaccid appearance. Immature and whitish in colour. The spent testes were reduced size with sizes according to their degree of development, became thicker and testes shows how gonadal development occurred during the reproductiveflaccid appearance. cycle. The macroscopic description of the ovaries The maturity analysis for males showed that 16.7% of them

the case of females, 1.61% was immature, 14.51% were maturing, 61.29%were maturing, were mature 73.21% and were 22.58% mature were and spent.10.71% Figure were spent.5 shows In the distribution of monthly frequency of males and females in different stages of gonadal maturation. Maturing and mature

females occurred only in February. During this study there was predominancefish occurred duringof mature most males of and the females. months, whereas immature

Figure 3: (a) Relative frequency of monthly values for sex ratios of Caranx crysos, (b) Relative frequency of males and females in different classes of total length.

Length at first sexual maturity (L50) lengths of males and females of C. crysos in relation to total body There was no significant difference between the total body

50) was 331 mm of totallength body for lengththe first (Figure sexual 4). maturity. The mean size when 50% of fish were in the process of sexual maturation (L

Figure 4 relation to body size for pooledsexes of Caranx crysos(dotted line). Figure 5 The inserted: The lines cummulative represent the percentage estimated of size observed range maturewhere 50% fish inof Caranx crysos, and (b) monthly frequency of maturity stages of males and females.: (a)Temporal distribution of GSI (±SE) of males and females the fish were mature.

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 5/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

Histological analyses of ovaries Monthly distribution of maturity stages and The microscopic stages of ovaries showed oocyte development reproductive period included the early and late primary growth and cortical alveoli. constituting in two stages. The first or the pre-vitellogenic stage GSI demonstrated the functional gonadal status in relation to fish body weight, indicating the spawning period. The mean The second or vitellogenic stage included the partially yolked and occurredmonthly valuesduring of most GSI partvaried of fromthe year, 0.84 other to 3.82 than (2.33 in the± 1.23) months for advanced yolked phases. ofmales February and from and 0.02 October. to 5.89 C. (2.19crysos ± has 1.76) a prolongedfor females. reproductive Mature fish oocytesEarly thereand late was primary an increase growth: in The the oocytes number did of not nucleoli, contain which yolk. 5). wereInitially seen the near nucleus the peripheryhad few nucleoli. of the nucleusWith the (Figure development 6a). Cortical of the period with peak period of activity during June and July (Figure alveoli: Cortical alveoli begin to accumulate in the cytoplasm. Discussion The general pattern of developmental stages of the gonads Yolk granules are still absent, but small oil droplets begin to of C. crysos accumulate and disperse in the cytoplasm. Partially yolkedstage reports on the reproductive biology of C. crysos from the Eastern (vitelogenic growth): During this stage yolk deposition initiated Mediterranean conforms [4], from to Porto that ofRico teleost [10], fishfrom [25, the 26].Gulf Thereof Mexico are (vitelogenicin the cytoplasm. growth): Later The the protein yolk granules granules and increase the oocyte in number begin [11], from the Egyptian Mediterranean Sea [12], however there is to fill with protein yolk granules (Figure 6b).Late yolked stage scarcity of information on the reproductive biology of this species distributed around the nucleus (Figure 6c and 6d). from Southwest Atlantic Ocean. and fill the cytoplasm. The oil globules increase in size and were C. crysos

usually capturedreach at a 300 maximum mm of length length [27]. of 700 C. crysos mm andsampled 5.05 inkg the in centralweight, Atlanticbut is much Mediterranean more common of Gulf below of Gabes, 350 mm. the Intotal Florida length it ofis females varied from 153 to 347 mm and that of males from 146 to C. crysos were frequent in the total length classes of 320-340 and 340-360 mm 349 mm [28]. In the present study, the females of smaller than 200 mm of total length tend to inhabit shallower reefs and lagoonmales in waters. the classes There of was 340-360 no predomination and 360-380 of mm. either Individuals sex of C. crysos during this study period. More females were present in the adult population in the [29]. However, in the Gulf of Gabesthere was predominance of males [4]. Monthly and seasonal changes in the numerical proportions and the predominance of males or females can be related to the sample size frequency distribution or feeding behavior of each sex. The sex ratio of the population changes when the capture is selective for the size and C. crysos showed

relatesex of fishto non-selectivity [4]. In this study of capture males and of individuals. females of no significant difference in the bodysize and weight, which may The value of b of the length-weight ratio is within the expected range of 2.5 to 3.5 [14]. Thus, the negative allometric growth Figure 6: Photomicrographs of histological preparations from a cross-section of the gonad of female Caranx crysos, showing oocyte indicates that the body increases in length than by weight development stages. (a) Developingoocyte (Pg1) = early primary during growth [30]. For the same species studied in the central growth, (Pg2) = late primary growth, nu=nucleoli; (b) Partially

Mediterranean, the allometric coefficient was 3.03 for males yolkedstage (CA= cortal alveolar; vtg1 = early vitelogenesis; (c and d) byand factors for females such as was environmental 3.04, indicating conditions, isometric maturation growth [28].stages, In Late yolked stages(vtg2 = late vitelogenesis). N= nucleus; nu=nucleoli; d=100µ). Stained with Hematoxylin-Eosin (HE) and periodic acid sex,general, stomach parameters fullness, of healththe LW condition, relationships season, in fishpopulation are affected and Schiffyg=yolk (PAS). granules; od= oil droplets.Scale bar: (a and b = 10µ) (c and differences within species [14].

Fecundity The blue runner reaches sexual maturity at slightly different lengths throughout its distribution range, generally between 225 The fecundity of C. crysos varied from 164782 to 542278 with and 280 mm of body length. Research in northwest Florida found an average of 408606 (SD ± 172908) vitellogenic oocytes. The a length at maturity of 267 mm, a study in Louisiana showed that diameter of mature oocytes ranged from 250µ to 400 µ with a this species reaches sexual maturity at 247 to 267 mm in females mean of 350 µ (±50.2). and 225 mm in males, and in Jamaica lengths of 260 mm for males

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 6/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

and 280 mm for females were estimated [11]. Males of C. crysos 5. Andrades R, Pinheiro HT, Santos RG, Martins AS, Costa PAS (2012) Rhincodon typus in Brazilian waters: 212 mm, and females with 223 mm [4]. All males were mature at a report of association with Caranx crysos. Journal of Fish Biology in the Gulf of Gabes, Tunisia, reach their first sexual maturity at 81(6):A new 2092-2094.record of whale shark mature male and female were 283 mm and 28 mm in total length 6. Murua H, Saborido-Rey F (2003) Female reproductive strategies respectively340 mm Fork [4]. Length This andstudy females registers at 360mm the mean FL size[10]. when The smallest 50% of ) was 331 mm of Atlantic Science 33: 23-31. 50 of marine fish species of the North Atlantic. Journal of Northwest total body length. 7. Chellappa S, Lima JTAX, Araujo A, Chellappa NT (2010) Ovarian fish were in the process of sexual maturation (L Spawning of C. crysos occurs offshore year round [11], waters of Northeastern Brazil. Brazilian Journal of Biology 70 (2): 451-456.development and spawning of Serra Spanish mackerel in coastal although several peaks in spawning activity have been registered 8. Oliveira MR, Chellappa S (2014) Temporal dynamics of Reproduction in different areas. Peak spawning season in the Gulf ofC. Mexico crysos in Hemiramphus brasiliensis (Osteichthyes: Hemiramphidae). inoccurs Puerto from Rico June shows to August, a spawning with a secondaryperiod which peak extends in spawning from during October in northwest Florida [27]. The IGS data of 9. ScientificOliveira MR, World Carvalho Journal MM, 2014: Silva 837151. NB, Yamamoto ME, Chellappa S C. crysos increases slightly in late spring and present Hirundichthy saffinis March to October, with a peak in May and June [10]. In the Gulf of from the Northeastern coastal waters of Brazil. Braz J Biol 75(1): inGabes, temperature IGS of in the region [4]. The effects of geographic 198-207.(2015) Reproductive aspects of the flyingfish, variationpeaks from on Julythe reproductive to August, which variables is influenced can explain by differences the increase in 10. Figuerola-Fernández M, Pena-Alvarado N, Torrez-Ruiz W (2008) Aspects of the reproductive biology of recreationally important to phenotypic plasticity resulting from abiotic factors, such as, temperature,reproductive rainfallactivity andof fish. food These availability effects [31]. have been attributed Service pp 134. fish species in Puerto Rico. Puerto Rico: US Fish and Wildlife This study indicates that C. crysos presents prolonged 11. Goodwin JM, Finucane JH (1985) Reproductive biology of blue reproductive activity, facilitating its population increase. runner Caranx crysos from the eastern Gulf of Mexico. Northeast Gulf Science 7(2): 139-146. Knowledge of the reproduction of C. crysos in the SouthwestAtlantic 12. Assem SS (2000) The reproductive biology and histological strategies. Adequate information on its reproduction is required characteristics of pelagic Carangid female Caranx crysos, from Ocean is crucial for the development of fishery management the Egyptian Mediterranean Sea. Journal of the Egyptian-German Society of Zoology 31(C): 195-215. gives basic information on the reproductive biology of C. crysos byto investigating facilitate the the fishery size at management. maturity as well Thus, as the the presentfecundity study and 13. Carpenter KE, Niem VH (1998) The living marine resources of the reproductive cycle. Acknowledgement 2069-2790.Western Central Pacific. Volume 4: Bony fishes part 2 (Mugilidae to Carangidae). FAO Species Identification Guide for Fishery Purposes: 14. Froese R (2006) Cube law, condition factor and weight-length and Technological Development (CNPq) and the Post Graduate relationship: history, meta-analysis and recommendations. Journal FederalThe authorsAgency ofwish the toMinistry thank theof Education, National CouncilBrazil (CAPES/MEC) for Scientific 15. ofHuxley Applied JS (1924) Constant 22(4): 241-253.differential growth-ratios and their for the financial support awarded during the study period. The authors are indebted to the artisanal fishermen who helped to 16. significance. Nature 14: 896- 897. maturity using a logistic type model. Aquatic Science, 56(3): 206- Referencescapture fish during the study period. 219.Chen Y, Paloheimo JE (1994) Estimating fish length and age at 50% 1. Duarte MR, Tubino RA, Monteiro-Neto C, Tubino M (2017) Genetic 17. a Review. Australian Journal of Marine and Freshwater Research 41: the coast of Rio de Janeiro (Brazil) comprise four different species. West G (1990) Methods of assessing ovarian development in fishes: and morphometric evidence that the jacks (Carangidae) fished off 199-222. Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte 2. ão dos peixes 18. BiochemicalSystematics and Ecology 71: 78-86. growth in teleosts. American Zoologist 21(2): 325-343. Lessa R, Nóbrega MF (2000) Guia de identificaç Programa Revizee / Score Nordeste. Brazil pp. 138. 19. marinhos da região nordeste. Departamento de Pesca, UNIFPE, 3. Lowerre-Barbieri SK (2011) A standardized terminology for Brown-Peterson NJ, Wyanski DM, Saborido-Rey F, Macewicz BJ, of blue runner, Caranx crysos (Mitchill, 1815), in the Adriatic Sea. CroatianPavicic M, Journal Siljic of J, DugandzicFisheries 72: P, Skaramuca125-127. B (2014) New record 3: 52-70. describing reproductive development in fishes. Marine and Coastal 4. Sley A, Jarboui O, Ghorbel M, Bouain A (2012) Annual reproductive 20. Hunter JR, Goldberg SR (1980) Spawning incidence and batch cycle, spawning periodicity and sexual maturity of blue runner fecundity in northern anchovy, Engraulis mordax. Fishery Bulletin Caranx crysos (Pisces, Carangidae) from the Gulf of Gabes (Tunisia, US 77: 641-652. 21. Murua H, Kraus G, Saborido-Rey F, Wittzhames PR, Thorsen A, et al. 790. Eastern Mediterranean). Journal of Applied Ichthyology 28(5): 785- (2003) Procedures to estimate fecundity of marine fish species in

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the Coastal Copyright: 7/7 Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean) ©2017 Oliveira et al.

relation to their reproductive strategy. Journal of Northwest Atlantic 27. Fishery Science 33: 33-54. Ohs CL, Creswell RL,Dimaggio MA (2013) Growing marine baitfish: 22. Wootton RJ, Evans GW, Mills LA (1978) Annual cycle in female three- Publication.A guide to Florida’s common marine baitfish and their potential Gasterosteu saculeatus L.) from an upland and for aquaculture. University of Florida/IFAS. Florida Sea Grant lowland population. Journal of Fish Biology 12(4): 331-343. 28. Ghailen H, Abdallah H, Hassan A, Mourad C, Abderrahmen B (2010) spined sticklebacks ( 23. De Martini EE, FountainRK (1981) Ovarian cycling frequency Gabes (Southern Tunisia, Central Mediterranean). African Journal of Seriphus politlls: Attributes BiotechnologyLength-weight 9(37): relationships 6177-6181. for 13 fish species from the Gulf of

547-560.and batch fecundity in the queenfish. 29. Goodwin JM, Johnson AG (1986) Age, growth, and mortality of blue representative of serial spawning fishes. Fishery Bulletin US 79: runner, from the northern Gulf of Mexico. Northeast nd Caranx crysos 24. McCullagh P, Nelder JA (1989) Generalized Linear Models, (2 edn), Guv Science 8(2): 107-114. London: Chapman and Hall/CRC Press. 30. Jobling M (2002) Environmental factors and rates of development 25. biology of the saddled bream, Oblada melanura (L.1758) from the MediterraneanZaki MI, Abu-Shabana coast of Egypt. MB, Assem Oebalia: SS 21: (1995) 17-26. The reproductive and growth. In: Hart PJB, Reynolds JD (Eds.), Handbook of fish 31. biologyWen H, andLin fisheries.H (2001) Fish Effect biology. of environmental Blackwell, USA, factors pp. 413 on gonadal 26. Assem SS (2003) The reproductive biology and the histological and maturation as well as its ovulation and spawning in teleosts. Ying Yong Sheng Tai XueBao 12: 151-155. Pagellu serythrinus from the Egyptian Mediterranean water. Journal ofultrastructural the Egyptian-German characteristics Society of of the Zoology, ovary of 42: the 77-103. female pelagic fish

Citation: Oliveira MR, Nóbrega MF, Oliveira JEL, Chellappa S (2017) Reproductive Biology of Blue runner, Caranx crysos (Mitchell, 1815) From the 10.15406/jamb.2017.05.00136

Coastal Waters of Rio Grande do Norte, Brazil (Southwest Atlantic Ocean). J Aquac Mar Biol 5(6): 00136. DOI: