by
P. Cayré, J.B. Amon Kothias, T. Diouf and J.M. Stretta
Reproduction is the fundamental physiological phenomenon by which a species assures its survival. General mode of reproduction can differ from one species to another; variants of a given mode of reproduction can at times appear within a same species in response to particular environmental conditions in the broad sense of the term.
For highly migratory oceanic pelagic species like yellowfin (Thunnus albacares), skipjack (Katsuwonus pelamis) and bigeye (Thunnus obesus), it is important first to define the general mode of reproduction (size at first maturity, periods and spawning zones, number of spawnings, fecundity etc…) before attempting to understand the specific potential variants. This synthetic approach is of course incomplete and must be completed by meticulous studies of variants that can introduce, in a given reproductive pattern, fishing, variations of the physico-chemical environment (climatic variations, regional specificities…) or biology (food, predators, competitors…).
These two approaches are necessarily complimentary and require specific methods, notably in sampling, if exception is made of studies on fish held in captivity. The synthetic approach can in general only be done with a vast sampling plan that must ideally cover simultaneously (and for a duration of at least one year for species living more than one year) the entire area of distribution and all sizes of the species studied. The extent of these tasks regarding tuna, explains that this synthetic approach is often done only a posteriori and that the general modes of reproduction are often only deduced from a mosaic meticulous regional studies. In order to show and eventually explain the variants of a given reproduction mode, it is necessary to assure a continuation of reproduction studies for a long period and at different points in the geographical distribution of the species.
In the eastern tropical Atlantic we will attempt to demonstrate, using the most recent, complete and pertinent studies for each of the three species, yellowfin, skipjack and bigeye, the different components of reproductive modes: gonad maturation, reproductive periods and zones, size at first maturity, fecundity. When, for a given species, the spatio-temporal variants of the reproduction forms seem clearly demonstrated, they will be pointed out.
The determination Atlantic yellowfin, skipjack and bigeye reproductive modalities have been derived from various methods based on one of following options:
Sampling of fish of different sizes caught at sea and more or less detailed examination of their reproductive organs (gonads).
Research cruises and collection of larvae.
No study of reproduction of fish held in captivity has been made in the study area.
6.1.1.2.1. Observation of gonads
Four types of analyses or observations can be made from gonads taken from sampled fish:
Macroscopic observation of the whole gonad: this observation permits determination of sex and a scale of gonad maturity (stages of maturation). The frequency of appearance of these different stages by time and area strata permits gross determination of locations and times of reproduction and sizes at first maturity.
Histological observation of gonads: from thin sections generally stained with hematoxylineosine, microscopic observation permits better determination and understanding of the process of gonad maturation.
Maturity index calculation: knowing gonad weight, two types of maturity index can be calculated:
a) the gonado somatic ratio, or GSR, for which the formula is:
 | W = weight of whole fish in grams |
| Wg = weight of gonads in grams |
b) the gonado somatic index or GSI
 | Wg = | weight of gonads |
| L = | fish length | |
| n = | a constant the value of which depends on the species and units chosen |
These two indices are intended to estimate, independent of size of the fish, the state of sexual maturity. High values of these indexes indicate the proximity of spawning; the spawning locations and periods can be identified by following the spatio temporal changes in average values of these indices.
- Ovocyte measurement: fragments of female gonads are taken, weighed, and dissected by various mechanical or chemical methods, in order to extract the ovocytes. The measurement of these ovocytes (generally the diameter) are made under a binocular microscope and the frequency distribution of these measurements is established. These results, associated with those of previously cited observations, allow a better understanding of the female sexual cycle development and hypotheses on the number of annual spawnings. Furthermore the count of ovocytes which have reached a size close to that at which they will be spawned gives an estimation of the number of eggs released at the time of spawning, a number designated as “partial individual fecundity”.
6.1.1.2.2. Collection of larvae
For the three species, yellowfin, skipjack and bigeye, the word larva designates an individual just hatched having a size around 1.5 to 3 mm (Roux, 1961; Kume, 1962; Mori et al., 1971; Ueyanagi et al., 1974), up until it has acquired most of its adult meristic characteristics; the larvae then has a size near 12mm at an age of about 15 days (Yatsukate et al., 1971; Inoue et al., 1974; Ueyanagi, 1978).
Larvae sampling is done during the day or night using of specially designed plankton nets. These nets, which are described in numerous works (Caverivière et al., 1980; Nishikawa et al., 1978 and 1985) have a diameter between 1 and 2 meters and their smallest meshes are around 0.5 mm; they are towed at relatively high speeds (2 to 3 knots), either horizontally at different depths exceeding rarely 50 meters and more often just under the surface, or obliquely in a manner to sample, in single tow, the entire layer of water between the surface and 50 meters, a depth below which nearly all authors acknowledege that larvae are very rare.
The results are expressed per unit of surface area (kilometer squared, mile squared) or in a more or less extended geographic area, either in gross values (number of larvae) or in relative values (number of larvae per tow or per thousands of cubic meters of water filtered). These data are then plotted on maps and interpreted to determine the spawning locations and seasons, and occassionaly to evaluate the quantitative importance of spawnings. The limits that seem reasonable to keep in mind in the interpretation of data from larvae collecting cruises will be reviewed below.
For the three species yellowfin, skipjack and bigeye, sexes are separate; cases of hermaphrodism have occasionally been observed for skipjack. (Raju, 1960; Uchida, 1961). No external character permits distinction of sexes. The fertilization of ova is external and takes place in the water after they are released by the females.
The definition of size at first maturity differs according to authors. Some consider that size at first maturity corresponds to size (fork length) of the smallest individual in a reproductive state observed in samples; for other authors, size at first maturity is that in which 50% of the individuals are capable of reproducing. We will prefer the second definition for its more general character, rather than the first which designates what one can call “minimum size at first maturity”. Finally, other authors, more rarely, consider that size at first maturity is that at which all of the individuals are capable of reproducing. We will designate this size by the term “size at complete maturity”.
6.1.1.4.1. Yellowfin
Males
In the eastern Atlantic, even the most recent and most complete study on yellowfin reproduction in the Gulf of Guinea (Albaret, 1977) gives no indication on size at maturity of male yellowfin; it is therefore necessary to make a hypotheses that is similar to that given for females.
Females
Size at first maturity: not given by Albaret, estimated from published data to be at fork length between 97 and 101 cm
Size at complete maturity: 108 cm (Albaret, 1977)
Minimum size at first maturity: in the region of 50 – 60 cm (Rossignol, 1968).
No study of possible temporal or spatial variability of these sizes has been undertaken in the Atlantic. This variability probably exists, as indicated by work carried out in the Pacific (Cole, 1980), and as seems to be shown by observations made on reproduction of yellowfin fished at depth by longline in the Gulf of Guinea (Fontana and Fonteneau, 1978; Yanez and Barbieri, 1980).
6.1.1.4.2. Skipjack
Males
Size at first maturity: 45 cm (Cayré and Farrugio, 1986)
Size at complete maturity: can be estimated from Cayré and Farrugio (1986) at 50 cm.
Minimum size at first maturity: 38 cm (Cayré, 1985)
Females
Size at first maturity: 42 cm (Cayré and Farrugio, 1986)
Size at complete maturity: can be estimated from the same authors at 47 cm
Minimum at first maturity: 38 cm (Cayré, 1984)
Sizes at first maturity mentioned here are similar to those currently accepted for the Pacific Ocean. No analysis of possible spatio-temporal variability of these sizes has been done. At this time, no study, even in the Pacific Ocean (Matsumoto et al., 1984), indicates that such variability could exist.
6.1.1.4.3. Bigeye
No research on size at first maturity of bigeye has been done in the Atlantic. For information only, we will mention the results compiled in a synthesis on Pacific bigeye (Calkins, 1980):
Size at first maturity D(males and females): between 100 and 130 cm
Minimum size at first maturity: females - 93 cm, males - 110 cm.
The maturation of genital products is a complex process as it includes different organs, secretions (hormones) and cells; the development in time of this process, which can be continuous or fragmented, is difficult to determine from samples of fish taken in their natural environment, especially when these fish are pelagic, migratory and widely distributed in the ocean. Attempts to study the progression of this process are mainly limited to studies of its effects on the genital organs (gonads) in attempting to divide the progression of the process into a definite number of characteristic phases or stages.
In the three species that interest us here, four methods have been used to characterize these different stages of maturity. We will describe briefly these four methods and results that they have produced for each of the three species: yellowfin, skipjack and bigeye of the eastern tropical Atlantic.
6.1.1.5.1. Histology
Method
Gonads, male or female, are taken from fish caught at sea. After being weighed, they are cut into pieces which are fixed in Bouin's fluid for several days. After washing and dehydration, these pieces are embedded in paraffin then cut in sections from 7 to 10 microns in thickness; these sections are then stained according to various methods (hematoxylin - eosine, ?? trichrome of Masson or Prenan…) and examined under the microscope. Different stages of maturity are then defined according to appearance of the section, its cellular composition, and for females, the development of ovocytes (size and quality).
Results
We will not present the descriptions of the different stages of maturation known for each species given by different authors, which are most often illustrated by photographs; we will refer the reader to original works limit the citation of these authors to the number of stages described for each species.
| Yellowfin | : | Ducros, 1964 and Rossignol, 1968 | : 6 stages |
| : | Albaret, 1976 | : 5 stages | |
| Skipjack | : | Cayré and Farrugio, 1986 | : 5 stages |
| Bigeye | : | No histological study available; Soviet works of | |
| : | by Alexseeva (1976) will be cited below. |
6.1.1.5.2. Macroscopic observation of gonads
The simple visual examination of the external appearance of male and female gonads is without doubt the oldest and simplest method used to determine the state of sexual maturity of tuna. The criteria that permit the distinction of different stages of gonad maturation are:
Several scales of maturity based on observation of gonads for the three species in the Atlantic have been proposed. We will mention the most recent.
Scale of yellowfin maturity
The scale of maturity of yellowfin from the Gulf of Guinea proposed by Albaret (1977) concerns mainly the females of this species. This scale has 6 stages in which 2 are subdivided, for a total of 8 “characteristic” steps of maturation.
Albaret points out the increasing difficulty to classify gonads in a precise stage of maturity when maturation is advanced, as the criteria defining different stages are imprecise and almost as variable within a given stage as between the different stages. We will add that the gonads examined are frequently from frozen fish which can modify their appearance and making the determination of their stage of maturity by visual examination even more arbitrary. The description of different stages of maturity corresponding to this scale is given in the appendix of this chapter.
Scale of skipjack maturity
This scale described by Cayré (1981) and revised by Cayré and Farrugio (1986), has 6 stages for males and females. The same general remarks as those formulated for the yellowfin maturity scale can be applied here.
Scale of bigeye maturity
A scale of maturity applied to eastern Atlantic bigeye was proposed by Gaikov (1983); it is similar to the one proposed for skipjack and is composed of 6 stages.
6.1.1.5.3. Maturity index
Yellowfin
A correspondence between the sexual maturation stage and either the gonado-somatioc ratio (GSR) or the gonado-somatic index (GSI) has been established by Rossignol (1968) for Atlantic yellowfin.
However if the GSR used by this author corresponds well to the definition mentioned in paragraph 6.1.1.2.1. (GSR = gonad weight × 100/body weight), the definition used for GSI is rather specific and to avoid all confusion we will denote this index, GSIR (R for Rossignol):
GSIR = volume of gonads (cm3) × 10 / cube of the length (cm)
Here we give the relationship established by this author between the maturity stage, GSR and GSIR, emphasizing the impossibility of comparing values of “GSIR” that he proposes with the traditional gonado-somatic index (GSI) *
Stage | State of Maturity | GSR | GSIR |
I | Immature | <0.085 | <0.165 |
II | Start of maturation | 0.095 – 0.20 | 0.165 – 0.38 |
III | Maturation | 0.20 – 0.60 | 0.38 – 1.03 |
IV | Advanced maturation | 0.60 – 1.0 | 1.03 – 1.67 |
V | Vitellogenesis | 1.0 – 2.5 | 1.65 – 4.4 |
VI | Spanwing | >2.5 | >4.4 |
Other authors have partially established the relation between maturity and the average values of maturity index but in a more unrefined way, their goal being mainly to distinguish individuals at maturation or close to spawning from others. One finds however in the works of Albaret (1977), a figure that permits one to assign an average value of GSI* to the different stages of maturation that he distinguishes:
Stage | State of Maturity | GSI |
I | Immature | <10 |
II | Start of maturation | 11 – 16 |
III | Maturation | 24 – 26 |
IV | Prespawning and spanwing | 30 – 50 |
V | Postspawning | 20 |
VI | Sexual resting | 11 |
Skipjack
For Atlantic skipjack, Cayré and Farrugio (1986) have made calculated average values of the GSI separately for males and females:
and have correlated them with maturity scales determined by macroscopic observation of gonads, and also for females by measurement of ovocytes (paragraph 6.1.1.5.4.).
* Formula utilized by Albaret (1976) to calculate yellowfin GSI:
Stage | State of Maturity | GSI Males | GSI Females |
I | Immature | 2 | 5 – 10 |
II | Sexual resting and start of maturation | 7 | 13 – 16 |
III | Active maturation | 32 | 45 – 50 |
IV | Pre-spawning | 54 | 733 - 82 |
V | Post-spawning | 5 | 24 – 27 |
These authors, was well as Cayré and Laloe (1986), emphasize that the GSI values that one can actually observe at each stage of maturity, although roughly characteristic of these stages, are very variable and can overlap from one stage to another; the same value may be observed on fish at different stages of maturity, notably when in the active stage of maturation (figure 6.1).
Bigeye
No actual maturity scale has been established based on a maturity index for Atlantic bigeye. Kume and Morita (1977) separates female bigeye into three categories according to their GSI values (weight of ovaries (g)/length at fork cubed (cm), ×104); this separation is made according to the scale proposed by Kikawa (1962) for Pacific bigeye
| 1.6< | GSI | <1.5 | Immature |
| GSI | <3 | Start of maturation | |
| GSI | >3.1 | Advanced maturation |
6.1.1.5.4. Size frequency distribution of ovocytes
The use of ovocyte measurements to follow the process of ovary maturation is based on the axiom according to which the degree of maturity of an ovocyte is directly proportional to its size. This method depends directly on products of sexual maturation. It is therefore more precise and less subjective than a simple superficial examination of the ovaries.
Generally for the three species, yellowfin, skipjack and bigeye, as for the very numerous other fish species, female ovocytes in the sexual maturation period change (grow) in successive groups. This is indicated by the presence of successive modes in the size frequency distributions of these ovocytes (figures 6.2., 6.3 and 6.4). It is the number of these modes and the size of the largest ovocytes that permits several stages in the maturation of females to be characterized.
Yellowfin
From size frequency distributions of ovocytes of yellowfin caught in the Gulf of Guinea, Albaret (1977) finds six stages of maturity (figure 6.2) which correspond to different GSI values (paragraph 6.1.1.5.3.). The extreme transience of the spawning stage (stage IV (2) of Albaret) and the period preceding the spawning explains the absence of ovocytes over 600 microns in the samples. Indeed during the period immediately preceding the spawning, the volume of ovocytes increases suddenly by penetration of water (Zharov, 1966); their diameter is then on the order of 1 mm.
Skipjack
Size frequency distributions of Atlantic skipjack ovocytes established by Cayré and Farrugio (1986) permits recognition of the five maturity stages of the scale adopted by these authors (figure 6.3.). Cayré and Farrugio explain, as Albaret for yellowfin, the rarity of large ovocytes (> 500 microns) by the extreme brevity of the stage immediately preceding spawning. One will notice the overlap of the GSI values observed by these authors for each stage.
 |  | ||
| Figure 6.1 | Mean gonadosomatic indices (and standard deviations) corresponding to different macroscopic maturity stages (I to V) of skipjack (after Cayré and Farrugio, 1986). | Figure 6.2 | Frequency distribution of yellowfin (Thunnus albacares) ovocyte diameters at different stages of maturation (after Albaret, 1977). |
 |  | ||
| Figure 6.3 | Size-frequency distribution (diameter) of skipjack (Katsuwonus pelamis) ovocytes corresponding to different macroscopic maturity stages. The number of samples (n), the extreme values observed of the gonadosomatic index (GSI) and the mean gonadosomatic index (GSI). The modal classes characteristic of each stage are noted: R(reserve stock), A, B, C, D,(after Cayré and Farrugio, 1986). | Figure 6.4 | Size frequency distribution (diameter) of bigeye ovocytes at 6 characteristic stages of maturity (after Alekseev and Alekseeva, 1980). |
Bigeye
A partial correspondence between maturity stage and size frequency distributions of ovocytes can be found in Alekseev and Alekseeva (1980). Among the numerous stages and supplementary stages distinguished by these authors, five seem to be able to be characterized by size distributions of ovocytes (figure 6.4).
6.1.1.5.5. Discussion and conclusion
Theoretically if the stages of maturation correspond to biological reality, one should find for a given species, an exact correspondence between the stages determined by the different methods exposed here. This is far from being the case: numerous authors have also pointed out the very subjective appearance and therefore somewhat imprecise determination of the stage of maturation by a simple macroscopic examination of gonads (Albaret, 1977; Cayré and Farrugio, 1986; Gaikov, 1983). Some of these authors have also pointed out the absence of relation between the GSI and ovocyte size when they exceed a certain value (300 microns).
We repeat the conclusion of Cayré and Laloe (1986) by stating that sexual maturation is a more or less continuous phenomenon, the complexity of which can be reduced the distinction of a few stages with difficulty, regardless of the definition criteria (with the exception of very precise histological criteria). The difficult is more severe when the process of maturation is well advanced. The significance of the four methods exposed here resides less in the possibility of following the process of maturation, than in the understanding of development (histology, ovocyte measurement) and determinatopm of the moment of spawning as closely as possible. To this effect, the use of a maturity index (such as GSI) is particularly useful as it permits a simple distinction of fish ready to reproduce from others (Cayré and Laloe, 1986).
6.1.1.6.1. Methods
The determination of spawning locations and seasons for east tropical Atlantic yellowfin, skipjack and bigeye has mainly been made by following variations in time and space of macroscopic maturity stage, maturity index (GSI or GSR) or again numbers or densities of collected larvae (paragraph 6.1.1.2.2.).
6.1.1.6.2. Reproduction zones and periods
- Yellowfin
Examination of gonads
Different studies on the state of gonad maturity of tropical Atlantic yellowfin involve, according to author, the four following regions:
The Senegal-Guinea region between 10°N and 20°N from the coast to 25°W (Postel, 1955; Frade and Postel, 1955; Rossignol, 1968; Yanez and Barbieri, 1980)
The equatorial zone, from 5°N to 5°S and from the coast to 15°W (Bane, 1963; Rossignol, 1968; Albaret, 1977; Fontana and Fonteneau, 1978; Yanez and Barbieri, 1980)
the Angolese region from 7°S to 15°S from the coast to 10°E (Da Franca, 1959)
the central and west Atlantic (Yanez and Barbieri, 1980).
From works concerning the Senegal-Guinea zone, it has been shown that yellowfin do not reproduce much in this region, and that in any event, the reproductive season is limited to the summer period from June to September. Reproduction in this region seems to be of little significance as evidenced by fairly low average values of the GSR observed by Postel (1955) even in summer, the presumed period of reproduction (during the month of July the average GSR is only 0.47). It is necessary however to point out that sampling carried out by Postel contained mainly fish with a size under that at first maturity.
The observations of Rossignol (1968) show that many yellowfin more than 110 cm in length are at a prespawning stage and have high GSR (from 0.7 to 0.9) starting in June.
For the south tropical region (Angola), Da Franca (1959) shows, based on fairly limited samples, that the GSR values increase from May to October; Rossignol (1968) indicates that these values are always less than those corresponding to an advanced maturity stage. The measurements of ovocytes done by Da Franca indicate a size increase not exceeding 300 microns. Rossignol (1968) and Bane (1963) conclude from the works of Da Franca (1959) that the reproduction of yellowfin in this region is not significant and limited to the warm season months (November to April).
In the equatorial zone, the average GSR values found by Bane (1963) show that this index increases regularly from November (GSR average = 0.257) to January (GSR average = 0.642) then decreases until March. These GSR observations joined to various other observations (macroscopic stage of maturity, size of ovocytes) brings this author to the conclusion that the spawning season of yellowfin in the Gulf of Guinea region off Liberia is spread out over several months (January to May) and that there would even be spawning of variable intensity all year long in this region. Rossignol (1968), from numerous observations of maturity stages, arrives at a similar conclusion, in specifying that the maximum spawning is between February and April for the eastern part of the Gulf of Guinea and between April and June for the western part (Liberia - Guinea). The large concentrations of large yellowfin exploited in the equatorial region mainly during the first semester, but at times outside of this period, very probably correspond to concentrations of individuals in reproduction; this observation seems to confirm the conclusions of Bane (1963) and Rossignol (1968) and indicates that the equatorial region is a more or less permanent active reproductive zone mostly during the first semester.
Albaret's important work (1977) on yellowfin from the Gulf of Guinea shows that there is a well marked seasonality in spawning of yellowfin caught at the surface by purse seine (figure 6.5). The geographical distribution of samples (figure 6.6) permits Albaret to specify that the zone in the inner Gulf of Guinea, to the east of the Greenwich meridian, on both sides of the equator, is an important yellowfin reproductive zone and that the maximum spawning period corresponds to the months of January and February. On the other hand, the comparison of GSI calculated from yellowfin fished at the surface in the Gulf of Guinea with those of individuals caught in the deep by longline in the same region (Fontana and Fonteneau, 1978), indicates that the sexual maturation of surface fish is more precocious (figure 6.7) and that the maximum spawning of fish caught by longline in the Gulf of Guinea occurred mainly in the third quarter. Yanez and Barbieri (1980), based on average monthly GSI observed from yellowfin fished by longline in the entire Atlantic zone is between 15°N and 10°S and to the east of 20°W, shows clearly that there are definitely two reproductive seasons for these fish in the first and third quarters (figure 6.8).
All studies on yellowfin reproduction in the Atlantic ocean taken from gonad analysis permits the definition of the following reproductive pattern (figure 6.9):
Significant limited spawning occurs during the warm season in the north tropical regions (Senegal, Cape Verde Islands, Guinea) from June to September and south (Angola) from November to April.
In the equatorial region situated to the east of 20°W and in the Gulf of Guinea, spawning seems to be distributed throughout most of the year with a maximum intensity in the first semester. One important spawning of surface yellowfin takes place in the first quarter in the inner Gulf of Guinea. There were however two spawning seasons for deep yellowfin in the first and third quarters in all of the Gulf of Guinea and off Liberia.
In the west and central regions of the Atlantic, the GSI values found for fish caught by longline (Yanez and Barbieri, 1980) also indicate the existence of two maximum spawning seasons in the first and third quarter (figure 6.8). The most important spawning zone is north of Brazil.
Figure 6.5 Geographic distribution of yellowfin samples captured by purse seine used by Albaret for his study of reproduction of the species by examination of gonads (after Albaret, 1976).
Figure 6.6 Variation of the mean monthly gonadosomatic index during the years 1974 and 1975 and the first quarter of 1976 (after Albaret, 1976).
Figure 6.7 Mean gonadosomatic index (GSI) calculated for yellowfin caught in the Gulf of Guinea by purse seine at depth by longline (after Fontana and Fonteneau, 1978).
Figure 6.8 Monthly variations of the mean gonadosomatic index (1957-1974) of bigeye caught by longline in the eastern, central and western Atlantic (after Yanez and Barbieri, 1980).
Figure 6.9 Pattern of the spatio-temporal distribution of yellowfin reproduction in the Atlantic. There is, on one hand, a vast equatorial area of more or less permanent reproduction, including two strata of maximum reproduction at the beginning of the year and in the third quarter, one situated in the east (Gulf of Guinea), the other to the west, and on the other hand, secondary seasonal zones of reproduction situated off Senegal, off Angola and in the Gulf of Mexico.
Distribution of larvae
Numerous larval tuna studies have been conducted in the Eastern Atlantic since 1956; the results are in numerous publications (Marchal, 1963; Richards, 1969; Richards et al., 1969 and 1969a; Richards and Simmons, 1971; Ueyanagi, 1971; Rudomiotkina, 1983; Caveriviere et al., 1976; Nishikawa et al, 1978; Caveriviere and Suisse de Sainte Claire, 1980; Nishikawa et al., 1985).
Given the life span of larvae is around 15 days and knowing that certain currents can reach significant speeds (2 knots and more) in the layer of water where larvae are present (0 – 50 meters) (Piton and Roy, 1983; Richardson and McKee, 1984, Gouriou present work), there are many uncertainties about the spawning area when larvae may have drifted for 15 days. The conclusions drawn from larvae collections would be unacceptable if the collections were made in a reduced space-time stratum without taking into account the system of currents and the size of larvae caught. Fortunately in the present case, data from numerous larval collection cruises have been accumulated and cover rather well the entire area concerning this synthesis; on the other hand, larvae of the three species are widely distributed in space and time. It is not possible, in view of the diverse methods or conditions of capture and the capacity of these larvae to escape sampling devices by swimming, to make precise quantitative estimations of their abundance. We will limit ourselves to presenting spatio-temporal distributions of larvae with, when possible, indications on their abundance which will assumed to correspond to spawning.
Yellowfin larvae have been sporadically sampled throughout the year in a vast zone situated on both sides of the equator (5°N – 5°S) including the Caribbean sea and the entire Gulf of Guinea (figure 6.9), in waters where the temperature is in general over 25°C (figure 6.10) and more often from 28 –30°C Caveriviere et al., 1976). The region of the Gulf of Guinea between Cape Palmas, the equator and 5° east, is the zone where the largest average density of larvae has been observed; Caveriviere and Suisse de Sainte Claire (1980) indicates that this agrees well with results obtained by Albaret (1977) on gonads, and concludes that that is the most important yellowfin reproductive zone, at least for the Eastern Atlantic. They point out that this abundance is maximum at the beginning of the year (January to May).
Relatively large quantities of larvae have been collected between 7°N and 17°N, off Senegal and the Cape Verde Islands only during the warm season (July to October). This confirms the existence of a secondary and seasonal spawning zone in this region.
Very few larvae have been collected in the south tropical zone off Angola, but the research cruises in this region are few. It is not really possible to conclude the existence of a notable reproductive zone in this region.
In the central Atlantic yellowfin larvae have been gathered most of the year in small quantities between 10°N and 20°S (figure 6.9). In the Western Atlantic, scattered larvae have been collected at the beginning of the year especially in the Gulf of Mexico (Richards and Potthoff, 1980), in the Caribbean Sea and off the coasts of Venezuela and Brazil Nishikawa et al., 1978 and 1985).
Yellowfin larvae collected from the entire tropical Atlantic clearly confirm the reproductive schema deduced from gonad studies.
- Skipjack
Examination of gonads
Numerous works concerning the determination of spawning areas and seasons of Atlantic skipjack have been conducted; most of these generally concerned limited periods or very specific regions (Postel, 1955; Gorbunova and Salabarria, 1967; Simmons, 1969; Batts, 1972; Chur et al., 1980; Cayré, 1981…). More recently, a study on skipjack reproduction on an Atlantic scale (Cayré and Farrugio, 1986) was conducted during the International Program of Research on Atlantic skipjack. We will refer to the results and conclusions of Cayré and Farrugio (1986) and add those of Batts (1972) although he studied more specifically skipjack coming from the north-west Atlantic.
Figure 6.10 Diagram of surface temperature and salinities in water where yellowfin, skipjack and bigeye larvae have been observed in the eastern tropical Atlantic (after Caverivière et al., 1976).
Figure 6.11 Spatio-temporal distribution of skipjack (Katsuwonus pelamis) in the Atlantic (after Cayré, 1984).
The regular monthly change in average GSI values in different regions of the Atlantic has identified several skipjack reproduction zones and periods (figure 6.11):
Eastern Atlantic:
A vast zone situated on both sides of the equator, including the Gulf of Guinea and to 20°W, where skipjack reproduce most of the year with variable intensity in time and space. The maximum spawning is observed during the period from November through March; certain regions such as that off Liberia seem to be particularly large spawning areas (figure 6.11).
In the north-east tropical region, around the Cape Verde Islands and only during the warm season (July to September), a notable number of reproductive individuals is observed.
the south-east tropical region (Angola coast): no significant sampling of gonads.
Western Atlantic:
Gonad observations are confined to two regions: the south coasts of Brazil (20°S – 30°S) and the coasts of North Carolina (30°N – 37°N).
Off Brazil, reproduction takes place from December to March as indicated by large average GSI values observed during this period. This period corresponds to the warm season. Off the American coasts (30°N to 37°N), the principal period of reproduction is also in the warm season (June-July) that according to Batts (1972). There is a the lack of significant observations in the west equatorial zone (Gulf of Mexico, east-north coast of Brazil and Venezuela). Sporadic observations of gonads (Golderg and Au, 1986) indicate that skipjack reproduce actively, notably during summer and the beginning of autumn.
From these observations, and taking into account the fact that as soon as the temperature of the water exceeds 24°C, one can observe skipjack in reproduction, Cayré and Farrugio (1986) propose the following reproductive schema for skipjack in the Atlantic ocean:
“Reproduction is opportunistic. Zones where the temperature is over 24°C and in which the phyto- and zoo- planktonic biomasses are large, seem particularly favorable to reproduction. As soon as one gets further from the equatorial zone in the direction of the north or south tropical regions, favorable reproductive periods are more and more limited in time to estival seasons only, during which the water temperature is over 24°C.”
Distribution of larvae (figure 6.11)
The references to the principal works; concerning the collection of tuna larvae in general and skipjack larvae in particular are identical to those mentioned for yellowfin. Some more specialized works on skipjack larvae can be added such as Rudomiotkina (1983a) and Matsuura (1986).
The similarity of the spatio-temporal distribution of skipjack larvae and those of yellowfin in the Atlantic is pointed out by Caveriviere et al., (1976) (figure 6.10) as well as by Nishikawa et al., (1985). The conclusions of different works on the distribution of skipjack larvae corroborate the reproductive schema deduced from the observation of gonads (figure 6.11):
In the equatorial region between 5°N and 5°S, skipjack larvae are observed all year with relatively greater abundance during the first quarter (January-March).
In the Gulf of Mexico and the Caribbean Sea, larvae are mainly present during summer (July to September) where they are more abundant than in the Gulf of Guinea.
As gonads in an advanced stage of maturation, larvae are almost exclusively found in waters where the temperature (figure 6.10) is over 24°C (Caveriviere et al., 1976; Matsuura, 1986), so that they are observed in the north or south tropical regions only during the estival season.
- Bigeye
Examination of gonads
The study of bigeye reproduction has to date not been done with the same precision and detail as yellowfin or skipjack.
All observations concerning the state of gonad maturity of bigeye were made on individuals caught by longline (Sakamoto, 1969; Alekseeva, 1976; Kume and Morita, 1977; Alekseev and Alekseeva, 1980; Gaikov, 1983). Apart from Sakamoto (1969) or Kume and Morita (1977) who calculated average maturity indexes (GSI) by zones on an annual or monthly basis, all other works are based on macroscopic observation of gonads, a method for which we have pointed out an inaccuracy.
Nevertheless, various conclusions common to these different works stand out:
The reproduction area of bigeye is limited mainly to a zone situated on both sides of the equator (15°N – 15°S) in relatively warm waters from the Gulf of Guinea to the American coast (figure 6.12).
Within this vast area of reproduction, one can observe individuals in reproduction more or less all year with two clearly marked maxima, as for yellowfin in the first and third quarter. Elsewhere within this area, reproduction is more significant in the western part, off the north-east coast of Brazil, and notably in the center of the Atlantic, than in the Gulf of Guinea.
Some individuals in advanced stages of sexual maturity have sometimes been observed in the south tropical regions (10°S to 20°S), off Angola or Brazil and in the north-east (Senegal) during summer months, from November to February and from June to September respectively. This indicated that these regions correspond to sporadic spawning zones which are secondary in relation to the large equatorial reproductive zone of bigeye (figure 6.12).
Figure 6.12 Schematic spatio-temporal distribution of bigeye in the Atlantic, based on the observations of larvae and gonad maturity. The density of the points on the figure indicates the relative intensity of the presumed spawnings. Spawning occurs in a more or less permanent manner in a vast equatorial zone and a major stratum of reproduction is situated off the northeast coasts of Brazil and Venezuela in the third quarter.
Distribution of larvae
Generally, almost all authors having worked on tuna larvae have pointed out that bigeye larvae are always decidedly more rare than those of yellowfin or skipjack. Caveriviere and Suisse de Sainte Claire (1980) have shown statistically that the presence of yellowfin and bigeye larvae (and in a smaller measure of skipjack) are strongly correlated, which, as with the direct observation of gonads, indicates a very similar reproductive schema (zones and periods) for these two species.
Bigeye larvae are very rarely found in waters under 24°C (Rudomiotkina, 1983 b) and most often in waters over 28°C (Caveriviere et al., 1976) (figure 6.10). They are more or less present all year in a vast zone around the equator from the coasts of Brazil to the Gulf of Guinea (figure 6.12). Some are found in the north tropical regions (Senegal, Cape Verde Islands) and south (Congo-Angola) during the summer months from July to September and November to February (Rudomiotkina, 1983).
These results confirm the reproductive schema deduced from the observation of gonads.
6.1.1.6.3. Number of egg releases (table 6.1)
The determination of the number of spawnings or egg releases of which an individual is capable, is a particularly difficult problem to resolve from fish caught in their natural environment. This problem is much more delicate to resolve when the areas and periods of reproduction are extremely extended, as we have seen for yellowfin, skipjack and bigeye. It is therefore actually impossible from work conducted in the Atlantic on these three species to state precisely how many spawnings per year they are capable of, and one is obliged to be content with hypothesis.
Table 6.1 Partial and total fecundity (expressed in millions of eggs spawned) of yellowfin, skipjack and bigeye in the eastern tropical Atlantic. (1) Bigeye: The absence of in depth studies of the fecundity of this species in the Atlantic and the fragmentary information collected in the Pacific lead to extrapolation from yellowfin results to this species as a preliminary approximation.
| SPECIES | PARTIAL FECUNDITY (number of eggs emitted per spawning) | TOTAL NUMBER OF SPAWNINGS | ANNUAL TOTAL FECUNDITY (number of eggs emitted) |
| YELLOWFIN | 1 to 6 millions | 4 to 10 | 4 to 60 millions |
| BIGEYE (1) | id | id | id |
| SKIPJACK | 0.1 to 1 million | 76 | 7.6 to 76 millions |
From ovocyte measurements on female gonads in an advanced maturity stage for the three species (Albaret, 1977; Cayré and Farrugio, 1986; Alekseeva and Alekseeva, 1980):
the size frequency distributions of ovocytes are plurimodal (several distinct groups of ovocytes in maturity),
occasionally large atresic ovocytes (in the course of reabsorption), that are the remnants of a recent spawning can be observed in these gonads.
These two observations have forced the conclusion that yellowfin, skipjack, and bigeye have several successive spawnings.
From the number of ovocyte groups (or modes) visible in frequency distributions in females in an advanced stage of maturity (figures 6.2., 6.3 and 6.4), and assuming that each one of these groups will be spawning and that other groups do not immediately appear after those spawnings, the following hypotheses on the number of potential spawnings can be made:
| Yellowfin | : | 3 spawnings |
| Skipjack | : | 4 spawnings |
| Bigeye | : | 3 spawnings |
These different spawnings are made successively during a given spawning period. It is proper, therefore, to multiply these numbers by the estimated number of spawning periods for each one of the species; this estimation of the number of spawning periods leads to other more uncertain hypotheses based on the observation of maturity index change in a given zone and on possible migrations from one zone to another. Yellowfin and bigeye may have two or three periods of reproduction per year which could lead to 5 to 10 spawnings (table 6.1).
With skipjack, it is again more delicate as they seem capable of reproducing throughout most of the year without a well marked period, and complete their maturity cycle very rapidly (Cayré, 1985). Recently this aptitude for skipjack to have very closely spaced successive spawnings seems to have been confirmed by the remarkable work of Hunter, Beverly and Macewicz (1986) on Pacific skipjack; after a very detailed histological study of skipjack gonads, these authors arrive at the conclusion that this species can spawn every 1.18 days for the whole duration of its reproductive period. Hypothesizing that the reproductive season lasts at least 3 months, one ends up with an estimation of 76 spawnings per year.
We emphasize once again on the hypothetical character of all of these results. In general, fecundity can vary according to multiple factors: size and age of individuals, climatic and environmental variations, etc…
 |  | ||
| Figure 6.13 | Relation between individual partial fecundity and size for yellowfin in the eastern tropical Atlantic. | Figure 6.14 | Relation between fecundity and fork length (FL) for skipjack in the Eastern Atlantic. |
The term “fecundity”, is in fact taken to mean “partial individual fecundity”. It is derived from the definition adopted by the “working group on reproduction of exploited species in the Gulf of Guinea” (ISRA-ORSTOM, 1979): “the number of ovocytes of the last mode present in the ovaries at the prespawning stage, before spawning begins”. This number is intended to correspond to the number of eggs spawned at the time of release. To be rigorous, the annual “total fecundity” of an individual of a given species, will be equal to the sum of partial fecundities corresponding to each of the spawnings made by this individual during the course of a year.
6.1.1.7.1. Partial Fecundity
Fecundity is a function of various parameters specific to each species and to each individual (size, weight of fish, weight of gonads, maturity index…); it is more generally expressed as a function of the length of individuals.
Yellowfin
The fecundity (partial) - fork length relation has been calculated here from data collected by Albaret (1976), it is expressed by:
F = 39.62 FL - 3056
with r = 0.343 and n = 198 (number of observations)
F = fecundity in thousands of eggs
FL = fork length in centimeters
Depending on its size (figure 6.13), a yellowfin, can release 1 to 6 million eggs per spawning (table 6.1). The low correlation coefficient value (r) indicates a very high variability in fecundity for a given size. For yellowfin, the reasons for this high variability have not yet been explored.
Skipjack
The fecundity - fork length relation (Cayré and Farrugio, 1986) is expressed by:
F = 17.817 FL - 544.811
with r = 0.527 n = 231 (number of observations)
F = fecundity in thousands of eggs
FL = fork length in centimeters
Therefore from 100,000 to a little more than 1 million eggs (table 6.1) can be released at one time by a skipjack depending on its size (figure 6.14). This fecundity can also be expressed in the average number of eggs emitted (at one time) per gram of body weight of the entire animal; this is what is designated by the term “relative partial fecundity”. In the case of skipjack, the relative partial fecundity seems to decrease slightly as the size of individuals increases. It is in the average of around 100 eggs released per gram of total weight (Cayré and Farrugio, 1986). Moreover, Cayré and Farrugio (1986) have shown that the strong fecundity variability for a given skipjack size seems to be linked to the catch zone of the fish: thus the fecundity of individuals sampled decreases when one moves away from the equatorial zone toward the north or south tropical regions.
The weak correlation coefficient (r) and the dispersion of points observed in the yellowfin length-fecundity relation (figure 6.13), could be explained in the same way as for skipjack; however the yellowfin that Albaret used to establish this relation come from a much smaller area (Gulf of Guinea) than that for the skipjack sampled by Cayre and Farrugio (20°N – 10°S).
Bigeye
No fecundity study has been made at this time in the Atlantic. In the Pacific, a previous study (Yuen, 1955) seems to indicate that bigeye have a partial fecundity similar to that of yellowfin (from 2.9 to 6.3 million eggs per spawning).
6.1.1.7.2. Total fecundity
In order to know the total fecundity of each of the three species, it is necessary to determine the annual number of releases and the partial fecundities corresponding to each release. We have already mentioned the difficulty in determining the number of spawnings. This number seems variable according to age of individuals (Rossignol, 1968; Albaret, 1977) and probably according to biological (abundance of species considered, abundance of food and predators) and physico-chemical environment.
Albaret (1977) made the hypothesis according to which the partial fecundity of yellowfin would be the same for 2 or 3 successive spawnings in the same spawning season. This hypothesis has not been verified and possible differences in partial fecundity from one spawning season to the other have not yet been analyzed where there seems to be 2 or 3 seasons.
From analyses conducted on skipjack fecundity, Cayre and Farrugio have shown that fecundity was variable geographically, but they hypothesize that this variability was linked more to the order of release than to the catch location of individuals.
For bigeye, no analysis has been done; the results obtained on yellowfin will be extrapolated to this species.
Taking into account these uncertainties and completely neglecting all causes of variability, the total fecundity can be estimated with extreme caution by multiplying the partial fecundity of each species by the annual number of estimated spawnings; the results for the annual total fecundity of the 3 species are:
Yellowfin and bigeye (table 6.1): from 5 to 60 million eggs per year; these numbers are very probably underestimates if, as for skipjack, a more rapid and frequent series of releases during the spawning season is accepted.
Skipjack (table 6.1): minimum estimation from 7.6 to 76 million eggs spawned per individual per year; the average total fecundity would be around 34 million eggs assuming an average partial fecundity of 450,000 eggs per release.
From different results and the most probable actual or hypothetically most probable information presented in this chapter, certain common traits in the reproductive strategies of yellowfin, skipjack and bigeye can be deduced:
separate sexes and external fertilization
spawning seems to be carried out in warm surface layer waters (0 – 50 meters)
egg size is very similar for these 3 species: diameter is 1 to 1.5 mm.
hatching occurs rapidly (24 hours) after fertilization and the larval stage lasts only 15 days.
spawning zones are vast; there is a large more or less permanent spawning area situated on both sides of the equator as well as in the two tropical zones (north and south), where the spawning season is limited to the warm season.
for the three species, reproduction is carried out in multiple successive spawnings.
This reproductive strategy explained the low variability in recruitment (from 1 to 5 for yellowfin (Fonteneau, 1985) and from 1 to 2 for skipjack (Cayre, 1985) that is estimated at present for these species. In this general common reproductive strategy for the three species, there are details specific to each species. Since the main points concerning bigeye reproduction have been deduced from work on yellowfin, only the specific features or “reproductive tactics” that seem to differentiate yellowfin and skipjack will be emphasized.
- Fecundity and reproductive cycle:
Yellowfin has a higher partial fecundity (number of eggs released at one time) than skipjack, as its size at reproduction and the size of its ovaries are greater than those of skipjack for eggs of approximately the same volume.
On the basis of cohort analyses (chapter 8) it is confirmed that skipjack are more numerous than yellowfin in the Atlantic. In order to compensate its lower partial fecundity and assuming larval survival rates, that to a first approximation, are estimated to be identical for the two species, skipjack reproduce very actively all year in the equatorial zone, according to an “opportunist” tactic (Cayré and Farrugio, 1986), while yellowfin in the same zone reproduce preferentially at specific times and in specific areas. Skipjack would be therefore capable of carrying out much more numerous and frequent spawnings than yellowfin, which is made possible by a very rapid maturation cycle of gonads and ovocytes.
For yellowfin, the relation between deep dwelling and surface individuals, as well as the role of these two groups (or stocks ?) in the reproduction of the species (Fontana and Fonteneau, 1978; Yanez and Barbieri, 1980) remains to be clarified, as it is probably due to a very precise reproductive tactic.
Although poorly studied, the reproductive strategy of bigeye, similar to those of yellowfin and skipjack, seems to indicate major migrations toward equatorial reproduction areas for large individuals which are found in abundance in very high latitudes (50°N - 50°S). This apparent constraint remains to be demonstrated and the whole reproductive schema for bigeye should be better defined.
Numerous other points, notably the variability of fecundity (or the reproductive schema itself) and the causes of this variability, remain to be explored for the three species.
Sex ratio is defined as the relation between the number of males to the number of females: nevertheless numerous authors designate this term to be the proportion of males or females expressed as a percentage of the total number of individuals where sex has been determined. Sex ratio is expressed either for all of the sampled population or more precisely for the size classes of individuals that compose the sample.
Table 6.2 Sex-ratio and percentage of male and female yellowfin (Thunnus albacares) observed in catches made in the Atlantic by different fishing gear.
| Authors | Location | Fishing gear | Total number males + females | Sex-ratio | % males | % females |
| POSTEL (1955) | CAPE VERDE | pole and line | 252 | 1.27 | 56.0 | 44.0 |
| ROSSIGNOL (1968) | CAPE VERDE | pole and line | 982 | 0.78 | 43.8 | 56.2 |
| LENARZ et al.,(1974) | Atlantic | pole and line + seine | - | 1.06 | 51.5 | 48.5 |
| longline | - | 1.44 | 59.4 | 40.6 | ||
| YONEMORI and HONMA (1975) | East Atlantic | seine | 197 | 1.22 | 53.8 | 46.2 |
| ALBARET (1977) | Gulf of Guinea | seine | 1540 | 1.45 | 59.2 | 40.8 |
Sex ratio has often been calculated globally for all yellowfin sampled (Postel, 1955; Rossignol, 1968; Lenarz et al., 1974; Yonemori and Honma, 1975; Albarret, 1977). From these different works, it is concluded (table 6.2) that sex ratio is generally unbalanced, favoring males when the samples come from surface gear (pole and line and purse seine) and favoring females in longline fisheries. The global predominance of females in samples collected from longliners, is in fact due to a significant overabundance of females among individuals of less than 150 cm in fork length (figure 6.15). The predominance of males among individuals larger then 140 cm clearly appears in samples caught by purse seine (Albaret, 1977) as well as in those over 150 cm. caught by longline (figure 6.15).
This phenomenon noted in yellowfin from the three oceans can be explained in four ways:
Lower catchability for females than males starting at 140 cm.
Sexual inversion of large females that become males.
Differential growth of two sexes and notably a smaller maximum size for females than for males.
Natural mortality higher for females.
If the two first explanations seem to be able to be rejected (Albaret, 1977), it is necessary to retain the last two to explain the observed change of sex ratio with size. The similar proportions (at least for surface samples) of the two sexes up to 140 cm. seems to indicate that up to this size, the growth and mortality of males and females are similar. From 140 cm., females may have either a slower growth and especially a smaller maximum size than males and a higher natural mortality, or simply a higher natural mortality (linked to the spawning process?) than males with an identical growth. It is not possible at this time to choose between these two hypotheses; growth of yellowfin males and females has not been approached separately and that of large individuals is in general poorly defined.
The divergence of the sex ratio that appears in individuals less than 150 cm. caught by purse seine and longline (figure 6.15) is very probably significant; although at this time largely unexplained, it may be due to behavioral differences linked to reproduction of surface and deep dwelling individuals (paragraph 6.1.1.6.2.).
Figure 6.15 Changes of the percentage of male yellowfin as a function of length and according to the method of fishing (purse seine or longline). The total numbers (n) of individual males and females samples is indicated. N.B.: The unpublished data from individuals caught by longline were collected by the Far Seas Fisheries Research laboratory (Shimizu, Japan) and were generously communicated by Mr. S. Kume.
Cayré and Farrugio (1986) have shown from a large sample (n = 16547) of skipjack representative of the population exploited in the Atlantic (pole and line boats and purse seiners) that, contrary to yellowfin, the global sex ratio of skipjack does not differ from 1 (exact value: 0.99 or 49.7% males).
Analysis of this sex ratio by size classes shows, according to the same authors, that males and females are always in equal statistical proportion no matter what the size (table 6.3 and figure 6.16). This result contradicts a dominance of males in the larger sizes which has at times been observed in certain regions of the Pacific Ocean (Orange, 1961) or of the Indian Ocean (Stequert, 1976).
The sex ratio calculations by zones of the Atlantic Ocean (Cayré and Farrugio, 1986) indicate that too many males (Brazil, Liberia) or females (Canary Islands, Azores) can sometimes be observed locally without explanation according to habitual parameters (size of individuals, gear or fishing season).
Most of the sex ratio calculations of Atlantic bigeye have been taken from samples of individuals caught by longline (Sakamoto, 1969; Gaikov, 1983). From sex ratio data published by Sakamoto for different zones covering all of the fishery of this species, the global sex ratio is calculated to be 1.39 (for 5404 individuals sampled). Data published by Gaikov (1983) for different spatio-temporal strata permit the calculation of an average global sex ratio of 1.54. Bigeye males are therefore in the majority, regardless of zone.
Knowing that the fishing method (longline) mainly permits the sampling of large individuals, it can be reasonably considered, that as for yellowfin there is a progressive imbalance in sex ratio favoring males at a certain size. Although no analysis of sex ratio by length class is available for Atlantic bigeye, the results obtained in the Pacific (Kume and Joseph, 1966) seem to confirm this hypothesis, since the percentage of males increases with size to be around 75% from a size of 170 cm. Shomura and Keala (1963) state that the sex ratio of bigeye caught by longline near the Islands of Hawaii is progressively unbalanced favoring males for individuals 125 cm. and over.
In the current state of knowledge, the occasionally mentioned hypothesis of differential behavior of bigeye males and females cannot be totally eliminated to explain an overabundance of males (Gaikov, 1983), or even an overabundance of females in large size individuals (Zavala Camin, 1978), phenomena that can be observed in certain regions.
Figure 6.16 Sex ratio (number of males / number of females) of skipjack in the Atlantic by 5 cm (fork length) size class (after Cayré and Farrugio, 1986).
Table 6.3 Skipjack (Katsuwonus pelamis): sex ratio calculated by 5 cm size class (fork length) and corresponding to individuals captured throughout the Atlantic (after Caryé and Farrugio, 1986).
| Size class FL (cm) | 30–34 | 35–39 | 40–44 | 45–49 | 50–54 | 55–59 | 60–64 | 65–69 | 70–74 | 75–80 | Total |
| Number of observations | 12 | 431 | 2500 | 4395 | 4357 | 2904 | 1325 | 577 | 190 | 29 | 16720 |
| Sex-ratio males/females | 5.000 | 1.261 | 0.956 | 0.968 | 0.973 | 0.969 | 1.077 | 1.121 | 1.184 | 0.933 | 0.990 |
| CHI 2 | 2.67 | 4.96* | 1.25 | 1.15 | 0.80 | 0.73 | 1.81 | 1.89 | 1.35 | 0.03 | 0.46 |
* CHI 2 significant at 5% level
