Abstract: Background and Objective: Sardinella sp. has gained much attention lately because of its biomass increase, which might be the result of climatic changes occurring across the Atlantic sea. Little information is known about reproduction of these species particularly in the Moroccan Atlantic area. The objective of the this study was to explore some aspects of the reproductive biology of Sardinella in the South of Atlantic Moroccan coast. Materials and Methods: Monthly samples were collected during the period between February, 2015 and January, 2016 in the area between Cape Boujdor and Cape Blanc. The data collected concerned the measure of the total length, the weight, the gonad weight as well as the sex and maturity stages. The χ2 test was used to compare the differences between both sexes and the ANOVA test was adopted to analyze the data variation. Results: Sardinella sp. is a gonochoristic fish. The overall female to male ratio was not statistically different for both species (χ2 = 0.68 for Sardinella aurita and χ2 = 1.04 for Sardinella maderensis), although it varied seasonally and according to the length of the fish. The monthly changes in the gonadosomatic index and the macroscopic characteristics of gonads showed that round Sardinella in the South of Morocco spawns between February and July and between November and December with a spawning peak on April. For the flat Sardinella, it spawns between February and March and in July with a spawning peak on July. Females round Sardinella reach first sexual maturity at a smaller size than males (26.17 and 26.78 cm, respectively). Concerning the flat Sardinella, it was the opposite. Males reaching sexual maturity are smaller than females (20.75 and 21.76 cm, respectively). Conclusion: It is concluded that the size at first maturity revealed that mature females in the South of Moroccan Atlantic Ocean were smaller than males for the round Sardinella and the opposite was observed for the flat Sardinella. The spawning of S. aurita presented a pick in April and for S. maderensis in July. As a shared stock these findings will be used for stock assessment in the North West Africa area.
INTRODUCTION
Fish had developed reproductive strategies and traits that ensure the survival of the species under variable and often unfavourable conditions1. The reproductive strategy of each of these species was expressed by certain characteristics such as age and size fecundity, time duration and frequency of spawning, size at first maturity and reproductive behaviour1,2. All these characteristics are useful for managing fisheries3, particularly for pelagic fishery species.
The Sardinella is a marine pelagic fish that is widely distributed throughout the tropical and subtropical seas of the world, including the entire Mediterranean and the Black sea4. It is a key species inhabiting the ecosystem of the Northwest African upwelling region5. The biomass of Sardinella had known fluctuations last years. Production of Sardinella during the period 1990-2014 varied from year to year. Those fluctuations were especially linked to the migrations of the species. The average catch during the last 5 years was around 73 340 t. The South of Cape Boujdor area represented 90% of the average catch of Sardinella 6. The Sardinella represented as the second pelagic species caught in this area after the Sardine (Sardina pilchardus), the round Sardinella represented the most dominant species in the studied area.
The identification of spawning period and spawning frequency were important prerequisites for understanding the dynamics of these resources, thus providing a basis for rational exploitation7. The reproductive biology of round Sardinella has been thoroughly studied in the Western8,9 and Eastern Atlantic10,11.
In contrast, information were limited for the Atlantic Moroccan coast and it has been studied across its Mediterranean distribution. Such as the study of reproduction of Sardinella aurita in Algerian12,13, Tunisian waters14 and Egyptian15 waters. Previous studies on Sardinella maderensis included those on the fishery by Longhurst16, Tobor17 in Cameroon by Djama et al.18, in Senegal by Postel19 and in Congo by Rossignol20; on food and feeding habits by Facade and Olaniyan21,22; on breeding age and growth by Marcus23 and on reproduction patterns by Youmbi et al.24.
However, the study of stock dynamics of these species exploited was rarely initiated. The lack of study was rather surprising given the considerable catches of Sardinella and the strong contributions in the total catch in the Southern of Moroccan Atlantic coast25. The aim of the present study was to investigate the following aspects of the reproductive biology of Sardinella aurita and Sardinella maderensis in the Southern Moroccan Atlantic: The time and duration of the spawning, the annual reproductive cycle, in terms of monthly changes in maturity stages, the sex-ratio, the sex-ratio variation on the size and the size at first sexual maturity.
MATERIALS AND METHODS
A total of 580 specimens of Sardinella aurita and 96 of Sardinella maderensis were collected monthly from February, 2015 to January, 2016 in the area between Cape Boujdor and Cape Blanc (zone C) from artisanal catches and in Al Amir Moulay ABDELLAH research ship (Fig. 1). Sampling frequency depended on the availability of Sardinella because it was not always present in fishing areas especially the flat one. Catches were sorted, identified, inventoried and weighted. The data collected concerned the measure of the Total Length (TL), the Total Weight (TW), the Gonad Weight (GW) (0.01 g), sex and maturity stages.
Sex ratio: The sex ratio was defined as the proportion of each sex, determined by macroscopic observation of gonads in a given population. The principal hypothesis supposed that there were equal sex ratios. This was evaluated with a chi-square test.
Sexual maturity: The macroscopic sexual maturity included five stages26 is shown in Table 1.
| Table 1: | Five-point maturity scale for partial spawners26 |
| Fig. 1: | Sampling area of Sardinella sp., in the South of Moroccan Atlantic ocean |
Size at first sexual maturity (L50): The total length at which 50% of specimens attains maturity (stage 3 was retained as the point at which the fish is considered mature) was deduced using theoretical maturity curve which corresponded to the regression between P parameter depending on the fish size (P = 1/(1+e-(a+b×L))27; where, P is the mature proportion by class size, L is a total length, a is an intercept and b is a slope). The linearization of this formula by introducing the natural logarithm gave:
-ln ((1-P)/P) = a+b×TL
The regression between Ln (P/1 - P) and Total Length (TL) made finding the parameters a and b. So:
L50 = -a/b
Gonadosomatic index: Variations in the gonad were almost estimated with parameters such as the length of the body, the total body weight or the somatic weight28. The expression used in this study was the gonadosomatic index (GSI), equals both gonads weight divided by the total weight of the body. It expressed the gonad weight as a percentage of body weight29:
GSI = GW×100/TW
Condition factor: The condition factor (K) reflected the ecological and physiological conditions30. In this study, it was calculated using the formula31:
K = (TW/TL3)×100
Statistical analysis: One way analysis of variance (ANOVA)32 was applied to test the differences between sex, sizes and seasons using STATISTICA software version 6.1.
RESULTS
Sex-ratio: Sardinella was a gonochoristic fish. External morphological and colour differentiations were not observed at any stage of its life cycle (monomorphism). In overall, 52% of Sardinella aurita sexed were females and 48% were males. Also, 45% of Sardinella maderensis sampled in the Southern Moroccan Atlantic area during the study period were males and 55% were females. The F:M ratio was 0.93 for S. aurita and 0.81 for S. maderensis and did not differ significantly (Table 2).
| Fig. 2: | Sex-ratio (%) as a function of total length for round Sardinella, South of Moroccan Atlantic ocean |
| Fig. 3: | Sex-ratio (%) as a function of total length (TL ranges (cm)) for flat Sardinella Males (M) and Females (F), South of Moroccan Atlantic ocean |
| Table 2: | Comparison of proportions of males and females of Sardinella sp., during the period February, 2015 and January, 2016 |
Sex-ratio depending on the size: The size-specific sex-ratio of Sardinella aurita showed that the number of females was higher for sizes (length) lower than 22.5 cm, whereas, the number of males was higher for sizes between 22.5 and 28.5 cm. The percentages of males and females were equal for size ranged between 28.5 and 32.5 cm. Females generally were dominant at sizes greater than 32.5 cm (Fig. 2). The sex-ratio differed statistically between the size classes (p = 0.001). For Sardinella maderensis, the size-specific sex-ratio showed that the number of males was higher for sizes lower than 24.5 cm. Females generally dominated the sizes greater than 24.5 cm (Fig. 3). The sex-ratio differed statistically between the size classes (p = 0.009).
| Fig. 4: | Seasonal variability of the sex ratio of Sardinella aurita Males (M) and Females (F) |
| Fig. 5: | Seasonal variability of the sex ratio of Sardinella maderensis Males (M) and Females (F) |
Sex-ratio depending on the season: During the year, the population of Sardinella aurita was constituted of a slightly higher percentage of males from autumn to spring, while in summer the sex ratio was in favour of females (Fig. 4). The sex-ratio did not vary significantly with seasons (p = 0.18). In contrast, Sardinella maderensis presented a higher percentage of females from autumn to spring. While in summer, males were slightly dominant (Fig. 5). The sex-ratio for this specie also didn’t vary significantly with seasons (p = 0.5).
Gonad stages and time of spawning: The sexual maturity stages were determined by the Food and Agriculture Organization (FAO) scale, 5 stages were identified for Sardinella26. Fish with gonads at stage greater than or equal to 3 were considered mature33. The monthly changes of different maturation stages are shown in Fig. 6 and 7. For Sardinella aurita, immature individuals were dominant from September-December and absent in April and June. Whereas, for Sardinella maderensis, the immature stages were present only for males and during February and November. The mature individuals of the two species were present along the year except in September and October for the round Sardinella. Although, the reproductive cycle was characterized by intense gonadal activity during February, March and April for S. aurita, while for S. maderensis during March, April and July. The GSI monthly values for both sexes are presented in Fig. 8 and 9. Males and females of S. aurita showed a maximum GSI of 5.11 and 3.78, respectively in April and a minimum GSI of 0.01 for males and 0.06 for females in October. For S. maderensis the maximum of GSI was observed in July for males (3.06) and females (3.23) and a minimum in November for both sexes.
| Fig. 6(a-b): | Monthly percentage of maturity stages of (a) Female and (b) Male round Sardinella, South of Moroccan Atlantic ocean |
Condition factor: The mean monthly changes in the condition factor are shown in Fig. 10 and 11 for both sexes. Overall, there were no significant differences between the months studied. For Sardinella aurita, the lowest value of condition factor was recorded for males in December (0.89) and the highest value in July (1.03). The lowest value of condition factor for females occurred in January (0.88) and the peak value (1.03) in April. For Sardinella maderensis, the lower value for males was recorded in July (0.87) and the highest value in March and December (0.97). For females, the lower condition factor was occurred in July (0.89), while the peak value in April (1.07).
Size at first sexual maturity (L50): The L50 was 26.78 cm for males and 26.17 cm for females of S. aurita (Fig. 12), whereas, S. maderensis males have an L50 lower than the females (20.75 cm for males and 21.76 cm for females) (Fig. 13).
DISCUSSION
The sex-ratio is in favour of females for both species (52% for Sardinella aurita and 55% for Sardinella maderensis). These results are in agreement with those found by Bensahla-Talet et al.13 on Algeria and Lawson and Doseku34 on Nigeria. The dominance of females must be due to its rise to the spawning site that is usually later than males28,35. The determining of sex proportions is very helpful for a better understanding of demographic structures. Thus, Boely36 points out that for Clupeidae, females often slightly outnumbered males. Dahel et al.37 in the Algerian Eastern coasts, Conand38 and Boely39 on the Senegalese coast and Cheibany40 in the Mauritanian Exclusive Economic Zone (EEZ) noted a significant predominance (p<0.05) of females, especially during the breeding season.
| Fig. 7(a-b): | Monthly percentage of maturity stages of (a) Female and (b) Male flat Sardinella, South of Moroccan Atlantic Ocean |
| Fig. 8: | Mean monthly changes in gonadosomatic index for both sexes of Sardinella aurita |
| Fig. 9: | Mean monthly changes in gonadosomatic index for both sexes of Sardinella maderensis |
| Fig. 10: | Mean monthly changes in condition factor (K) for both sexes of Sardinella aurita |
| Fig. 11: | Mean monthly changes in condition factor (K) for both sexes of Sardinella maderensis |
| Fig. 12: | Size at first sexual maturity of Sardinella aurita males (M) and females (F) in the South of Moroccan Atlantic Ocean |
| Fig. 13: | Size at first sexual maturity of Sardinella maderensis males (M) and females (F) in the South of Moroccan Atlantic Ocean |
| Table 3: | Average values of the sex ratio found by different authors |
It should be noted that the sex-ratio varies according to size ranges. There is a predominance of males among the first individuals arrived, followed by a numerical inequality of females and males and a female predominance in late migration35. For Libyan waters, Pawson and Giama41 had reported differences in the sex-ratio depending on the size that were related to sexual differences in growth, mortality or energetic cost of reproduction. In the Northern Aegean, Algerian and Tunisian waters females generally dominated the higher size classes13,14. Fairly significant seasonal variation (p<0.05) in sex ratio is also observed in Sardinella but it’s more pronounced in the flat one. The comparison of the average values of the sex ratio found in Senegal and Mauritania are shown in Table 3.
The results of the study realized by Diouf et al.35 about Sardinella aurita and Sardinella maderensis sampled in the Senegalese coast during the period between 1995 and 2007, showed an average sex-ratio lower than those carried out by other authors as presented in Table 3 on the same species in Senegal and Mauritania. These differences were likely due, in part, to the peculiar sampling of each fishery and the average size of samples. In addition, the relative distribution of sexes and fisheries in time and space may explain the observed differences in the results.
| Table 4: | Reproduction periods of round Sardinella (S. aurita) by country |
| Table 5: | A review of the reproductive periods of flat Sardinella (S. maderensis) by country |
In the Southern Morocco, the spawning starts in February and lasts until July for Sardinella aurita. While for Sardinella maderensis, it takes place in spring and summer. According to GSI monthly variations and maturation stages of the fish, a maximum of GSI for the round Sardinella is recorded in spring (April) and for the flat Sardinella in summer (July). As for most marine fish, to ensure the synchronization of larvae appearance and the peak of primary production, the time of spawning of Sardinella has evolved42,43. However, the yearly variation of the spawning season onset of Sardinella is owing to temperature differences and other factors such as population-related changes and food availability44. Furthermore, Ben-Tuvia45 noted that the ideal water temperatures for a gonad maturation of round Sardinella are above 20°C. Ettahiri et al.46 also related Sardinella spawning to high water temperatures. Sardinella might be a model species for understanding climate change mediated effects on fish populations due to the flexible strategy that results from its demographic plasticity47 and its wide geographical range.
The reproductive period of round Sardinella in the present study was long, whereas in the Northern Aegean the reproductive period was short: Two months lasting. In other areas of its distribution (Table 4), the reproduction of round Sardinella is highly variable regarding the time and duration of spawning. Consequently, its reproduction lasts throughout the year in the North-west African coast10, exhibiting intra-annual variations with one10 or two47 peaks of reproductive activity. At the sub-region, all the authors who have studied the monthly variation of females and males GSI of the round Sardinella or who have made larvae prospecting campaigns agreed on the existence of sexual activity vary over the year with two main spawning seasons separated by biological rest periods more or less marked35,47-51. In the Mauritanian area, spawning takes place from May to July52. Chavance et al.53 also highlighted two breeding seasons, the first from July to August and the other from December to January. The study of Pascual-Alayon et al.54 concluded that in the same area, there was a main spawning period from June to August and a second in November and December.
For Sardinella maderensis, the sexual activity is intense in March, April and July with a maximum in July. The peak of reproduction highly varied inter-annually35,36,49,51,55,56. The spawning period is minor in November-December51,55. The results obtained by Diouf et al.35 show a continuous reproduction for S. maderensis throughout the year. The reproductive activity period shows less marked fluctuations with minimum values in the cold season (October, November, December and January) and maximum in the beginning of the warm season (March, April and May). Gonad maturation is more continuous for S. maderensis females. The results of Samba51 also highlight two main breeding periods for Sardinella maderensis, the first occurs from May to August during the hot season and the other occurs in October and November during the cold season-warm season transition. So it seems that the dates and the importance of laying period peaks vary from one year to another (Table 5).
| Table 6: | Size at first sexual maturity (L50) of Sardinella aurita found in different area |
| L50: Size at first sexual maturity, FL: Fork length, TL: Total length, (TL = 1.21×FL-0.857)48, F: Female, M: Male | |
| Table 7: | Size at first sexual maturity (L50) of Sardinella maderensis found in different area |
| L50: Size at first sexual maturity, FL: Fork length, TL: Total length, FL conversion to TL by the relationship (FL = 0.843×TL)50, F: Female, M: Male | |
In the South of Moroccan Atlantic Ocean, round Sardinella females were smaller at maturity than males. Indeed, maturation usually occurs at the end of the first year of life for short-lived species57. Bimaturism, which is common in species with promiscuous mating, external fertilization and indeterminate growth58, was also observed for other round Sardinella populations14. Besides the environmental and genetic factors2,59, size at first maturity can be influenced by other factors such as long-term fishing pressure3. This may pose severe impacts on size at first sexual maturity forcing the population to mature at a smaller size in order to ensure the survival of the species60. The size at first sexual maturity (L50) has been reported for Atlantic stocks of round Sardinella (Venezuelan waters, Ghana waters, Table 6). In the Mediterranean, however, round Sardinella reaches sexual maturity at a smaller size (Table 6).
For the flat Sardinella, the total length at which 50% of specimens attain maturity were estimated by logistic regression as 20.75 and 21.76 cm for males and females respectively. In Senegal, the work performed by Boely36 and Levenez50 showed that the L50 in this area was 20 cm. More recent studies in Senegal give annual average sizes of first sexual maturity of 23.6 cm (TL) and 25 cm (TL) for females and males, respectively36 and 22 cm (TL) for both sexes51 (Table 7). Note that the sizes of first sexual maturity found in Senegal and Morocco were slightly higher than that observed in Guinea Bissau. This could be explained by the higher growth rate observed in Senegalese waters39. The small size at first sexual maturity found in the Rio Grande de Buba (Guinea Bissau) could be linked to increased salinity conditions that can lead to the size reduction61.
CONCLUSION
It is concluded that the sex-ratio of Sardinella sp. was in favour of females for both species. The size at first sexual maturity of Sardinella aurita was determined as 26.78 cm for males and 26.17 cm for females, while for Sardinella maderensis the L50 was about 20.75 cm for males and 21.76 cm for females. In line with the GSI, the spawning peak for S. aurita occurred in April, while for S. maderensis it was in July.
The results of the size at first maturity showed that mature females in the South of Moroccan Atlantic Ocean were smaller than males for the round Sardinella and the opposite was observed for the flat Sardinella.
SIGNIFICANCE STATEMENTS
| • | This study discovers that results will be used for the stock assessment and fishery management of Sardinella sp. |
| • | The identification of spawning period and spawning frequency will provide a framework for better understanding the reproductive patterns of Sardinella sp. |
ACKNOWLEDGMENTS
This study was conducted at the National Fisheries Research Institute (INRH) in collaboration with the Faculty of Sciences of Rabat, Mohammed V University. We thank the staff of Biology and Ecology Laboratory in the INRH of Casablanca and Mr. Sidahmed Baibat from the INRH of Dakhla.