On the Population Ecology of the Zebra Seabream Diplodus Cervinus Cervinus (Lowe 1838) from the Coasts of the Canarian Archipelago, North West Africa

Home , Diplodus

On the population ecology of the zebra seabream Diplodus cervinus cervinus (Lowe 1838) from the coasts of the Canarian archipelago, North West Africa

Jose´ G. Pajuelo, Jose´ M. Lorenzo, Rosa Dom´ınguez, A. Ramos & Muriel Gregoire Departamento de Biolog´ıa, Universidad de Las Palmas de Gran Canaria. Campus Universitario de Taﬁra, 35017 Las Palmas de Gran Canaria, Spain (e-mail: [email protected])

Received 14 March 2002 Accepted 13 June 2003

Key words: population structure, recruitment, reproduction, growth, mortality

Synopsis

Zebra seabream, Diplodus cervinus cervinus, caught off the Canary Islands is characterized by protogynous hermaphroditism. The male : female ratio is in favour of females (1 : 2.16). The reproductive season extends from spring to summer, with a peak in spawning activity in May–June. Males reach maturity at a larger total length, 327 mm (5 years old) than females 273 mm (4 years old). Recruitment occurs from late October to January in shallow waters of 0.5–8 m depth along the coastal line. The recruits are located over rocky substrates with an important algae vegetation forming schools lower than 2 m2. During the spawning season, schools of adults from 3 to 8 fish are observed. The schools are formed by one large individual and a few moderate size individuals. Mating takes place in small groups formed by one dominant male and a group of several females (polygamy). Moderate size individuals are often observed mixed in large schools (up to 30 individuals) of Diplodus sargus cadenati. Subadults form groups of a few fish (<5 individuals) or more commonly mixed groups (>15 individuals) with individuals of species of similar size. Otoliths age readings indicate that the population consists of 18 age groups, including a very high proportion of individuals between 2 and 4 years old. The von Bertalanffy growth parameters for the −1 whole population are: L∞ = 603 mm,k= 0.149 year , and t0 =−0.22 year. The mean rates of total, natural and fishing mortality are 0.551, 0.215 and 0.336 year−1, respectively. The length at first capture is 183 mm. The exploitation rate indicates that the stock is overfished. The direct effects of fishing on the population result in changes in the abundance, with a reduction to 85% of the unexploited equilibrium level. The length at first capture by the commercial fishery is less than the length at maturity. With 58% of the total catch below this length there is a danger of recruitment overfishing.

Introduction bottoms, down to depths of about 300 m, but usually on bottoms up to 80 m. This species is distributed in The zebra seabream Diplodus cervinus (Lowe 1838) the eastern Atlantic coast from the Bay of Biscay to consists of 3 subspecies, D. cervinus omanensis the Cape Verde Islands, from Angola to South Africa, (Bauchot & Bianchi 1984), D. cervinus cervinus (Lowe and around the Madeira and Canary Islands. It is also 1838) and D. cervinus hottentotus (Smith 1844), dis- found in the warmer zones of the Mediterranean Sea tributed in the Oman waters, eastern Atlantic and (Bauchot & Hureau 1990). Information on the biology Mediterranean Sea, and Indian Ocean, respectively of the D. cervinus subspecies is scarce and only bio- (de la Paz 1975). metric aspects of D. cervinus cervinus in the Egyptian D. cervinus cervinus is a demersal marine ﬁsh con- Meditterranean waters have been published (Wassef gregating in schools of 4 or 5 individuals over rocky 1985). 408

In the Canary Islands, the zebra seabream is caught We established recruitment of D. cervinus cervinus mainly with traps at depths between 3 and 70 m. It is into nursery areas by underwater visual census. We also captured year round with significant seasonal differ- observed the schools of adult and subadult individu- ences in the landings. No limits are currently imposed als. We carried out the visual census fortnightly along on its fishery and only minimum size legislation coastal transects in a protected area located in the north (200 mm) has been implemented. coast of Gran Canaria. Census were conducted along The need for an ecologically based management shore, from the surface to 10 m of depth. As visual strategy and the paucity of data available on the ecology counts were performed with fortnightly periodicity, it of this species prompted an investigation into aspects is assumed that the date of first count was not very of its life history including population structure, sexu- different from the date of recruitment. ality, spawning cycle, maturity, recruitment, age and We determined the age by interpreting growth rings growth and mortality. We examined this ecological on the otoliths. We examined the whole otoliths placed aspects in order to understand the life cycle strategy in a blackened bottom watch glass containing water of this fish and to compare its population aspects with under a compound microscope (10×) with reflected the information available for the other D. cervinus light. Counts of the growth bands were made without subspecies. knowledge of the size, sex or previous results for the individual. Counts were made for otoliths of each individual on two separate occasions, and only coincident Materials and methods readings were accepted. We evaluated the periodicity of bands formation by We caught D. cervinus cervinus specimens with arti- noting the visual appearance of the otolith margin and sanal demersal fishery traps fortnightly at depths of expressing it as a percentage of the monthly sample. 3–70 m off Gran Canaria, Canary Islands. We mea- Once the periodicity and timing of rings formation were sured a total of 1 759 individuals to the nearest mm for verified, we determined the age of each fish by enumer- total length (Lt, mm) from October 2000 to September ating the marks, and assigned each individual to an age 2001. We taken a random subsample of 618 specimens class. We considered the 1st of June as the birthdate to for biological analysis. We weighed each of these fish assign the individual ages to age groups. We described to the nearest 0.01 g for total body mass (Wt). We taken length at age by the three-parameters specialized von − ( − ) the eviscerated mass (W ) to the nearest 0.01 g and the k t t0 e Bertalanffy growth model: Lt = L∞(1 − e ), gonad mass (W ) to the nearest 0.001 g. We assessed g where t0 is the age at zero length, Lt is the length-at- the sex and the stage of maturation visually and we age, L∞ is the predicted asymptotic length and k is the classified the stages of maturation as follows: I, imma- growth rate. We fitted the model to data by means of ture; II, resting; III, ripe; IV, ripe and running; V, spent. the Marquardt’s algorithm for non-linear least squares We removed, cleaned and stored dry sagittal otoliths parameter estimation (Saila et al. 1988). for later age determination. We obtained estimates of the instantaneous total We calculated the overall sex ratio (males : females) mortality rate (Z) by means of catch curve analy- and the sex ratio by size classes considering the rela- ses (Pauly 1983). We obtained an estimate of total tion between the number of males and females. We mortality rate from the negative of the slope of the estimated the length at maturity determining the pro- straight line fitted to points greater than the age at portion of reproductively active fish in each size class full recruitment using the program FiSAT (Gayanilo (stages III–V). and by fitting a logistic ogive: et al. 1996, Gayanilo & Pauly 1997). We also obtained Z from the Beverton & Holt’s (1956) mean length in = a , P − · the catches and the Ault & Ehrhard’s (1991) method. 1 + ((a − b)/b) (e c Lt ) We estimated the instantaneous rate of natural mortal- where P is the percentage of fish mature at length Lt, and ity (M) using different classical empirical equations a, b and c the model parameters (Saila et al. 1988). We (Beverton & Holt 1959, Tanaka 1960, Taylor 1960, estimated the spawning season using different meth- Rikhter & Efanov 1976, Pauly 1980). To delimit a range ods; by a gonadosomatic index which was calculated of values of this rate that includes its real value, we esti- by expressing gonad mass as a percentage of evis- mate the longevity for each value of M using the method cerate body mass (Anderson & Gutreuter 1983) and of Alagaraja (1984). We calculated the instantaneous calculating the proportion of maturity stages. rate of fishing mortality (F) from the difference between 409 the instantaneous rates of total and natural mortality. Results We estimated the exploitation ratio (E) by dividing F by Z (Gulland 1971). We calculated the individuals The gonads of the zebra seabream are elongated and selected by the fishing system using the logistic pat- are suspended by a dorsal mesentery in the posterior tern: Sa = 1/(1 + exp(−r · (L − S50))), where Sa is region of the visceral cavity. In general, both gonadal the selectivity of the gear on a fish of length a, S50 lobes are equally well developed. Of the fish exam- is the length at 50%-selectivity and r the parameter ined, 151 were males, 327 females and 16 intersexuals. which determines the width of length-specific selectiv- The sex of the remaining 124 fish could not be deter- ity function (Saila et al. 1988). We fitted the ogive to the mined macroscopically because they were immature ascending limb of the length catch curve and taken the as they had very thin and translucent gonads. Fish mode of the length frequency distribution to represent ranged in size from 51 to 565 mm, weighing between 100% selectivity. 4.1 and 3 490.3 g. Males ranged between 193 and We determined the biomass per recruit (SBR) as a 565 mm in size, and between 97.2 and 3 356.3 g in = 17 function of F as: SBRF i=0 BiwiNi, where Ni is the mass. Length of females ranged from 160 to 528 mm relative proportion of fish at age i and wi is the mass and mass from 73.8 to 2 762.8 g. Intersexuals ranged of fish at age i, and Bi the proportion of mature fish at in size from 237 to 452 mm, weighing from 254.4 to age i (Booth & Buxton 1997). We examined from the 1 695.2 g. spawner biomass per recruit curves two biological ref- The overall ratio of males to females was 1 : 2.16; erence points, expressed in terms of F. These included thus both sexes were not equally represented and FSB40 and FSB50, which are the instantaneous rates of the hypothesis that the sex ratio was 1 : 1 must be χ 2 = . >χ2 = . ; = . fishing mortality at which the spawning biomass is rejected ( 64 8 t 1,0.05 3 84 p 0 0001). reduced to below 40% and 50% of its unexploited Females predominated in smaller size intervals, males equilibrium level, respectively (Booth & Punt 1998). in larger ones, and intersexuals were intermediate in FSB50 strategy is the most suitable, since it is sufficient size between males and females (Figure 1). Sex ratios to protect the spawner stock in slow growing, long-lived by size intervals had significant departures from 1 : 1 χ 2 >χ2 = . species (Booth & Buxton 1997). ratio for most size categories ( t 1, 0.05 3 84;

Figure 1. Size distributions of male, female, intersexual and immature individuals of D. cervinus cervinus off the Canary Islands. 410

Figure 2. Mean monthly frequency of maturity stages for males Figure 3. Monthly development of the gonadosomatic index and females of D. cervinus cervinus off the Canary Islands. Matu- (GSI) for males and females of D. cervinus cervinus off the Canary rity stages: (II) resting, (III) ripe, (IV) ripe and running and Islands. The vertical bars indicate the standard deviation. (V) spent. p = 0.0001), except for the middle size groups (300–380 mm). Males and females with ripe gonads (stage III) were recorded between March and May, being dominant in April; ripe and running males and females (stage IV) appeared in April and became dominant in May and June; and spent males and females (stage V) were recorded from June to August (Figure 2). The GSI values followed the same pattern for males and females, with values of females being higher than those of males; the highest values occurred between March and August, with a maximum in May–June (Figure 3). The sexual maturity ogive for males and females are shown in Figure 4. The smallest mature males and females were 260 and 220 mm, respectively. Individ- uals smaller than 210 mm showed little evidence of sexual activity. A significant difference in length at first maturity was found between males (327 mm) and females (284 mm) (t-test, t = 2.61 > t0.05, 234 = 1.96; = . p 0 0001). Figure 4. Sexual maturity ogive for all individuals of D. cervinus Recruitment occurred from late October to January cervinus off the Canary Islands. a, b and c are the parameters of in shallow waters of 0.5–8 m depth along the coast line. the sexual maturity curve, r is the determination coefficient and n The recruits were located over rocky substrate with is the number of fish. 411 an important algae vegetation forming schools lower Otoliths showed a seasonal variation in the formation of than 2 m2. hyaline and opaque rings. Opaque and hyaline edges During the spawning season, schools of adults down were noted in all the months, but the general pattern to 8 fish were observed. The schools were formed by indicated that two rings, one opaque and one hyaline, one large size individual (>300 mm) and a few mod- were deposited during one year. The opaque ring was erate size individuals (200–300 mm) of similar size. formed between April and September, mainly in July During the rest of the year the larger size individuals and August, and the hyaline ring during the remaining were observed solitary or in small groups, while the months (Figure 5). moderate size individuals are observed in schools Fish aged 0–17 years were found (Table 1). Age of of a few fish (<8 individuals). In many occasions, males ranged between 3 and 17 years and of females the moderate size individuals were observed mixed between 2 and 14 years. The parameters of the von in large schools (up to 30 individuals) of D. sargus Bertalanffy growth equation for males, females and all cadenati. The subadult individuals (<200 mm) were individuals are given in Table 2. Significant differences observed forming groups of few fish (<5 individuals) in the growth parameters were found between sexes 2 2 = . > 2 = . or in the majority of the cases forming mixed groups (Hotelling’s T -test, T 23 1 T0 0.05, 3, 410 7 89; (>15 individuals) with fish of similar size located in p = 0.0001), with females growing at slightly faster coastal waters, such as D. vulgaris, D. sargus cadenati, rate than males. Oblada melanura or Sarpa salpa. Age frequencies derived from the transformed length The use of sagittal otoliths for estimating the age of frequency data provided estimates of Z (Figure 6). Esti- the zebra seabream proved straightforward, with dis- mates of Z obtained from the Pauly’s length-converted tinct opaque and hyaline bands surrounding a white catch curve (Z = 0.540 year1), the Beverton and opaque nucleus. Of 618 otoliths processed for annual Holt’s mean length in the catches (Z = 0.562 year−1) age estimation, 35 (5.7%) were considered unreadable. and the Ault and Ehrhard’s method (Z = 0.552 year−1) Of these otoliths, 1 was completely translucent, 7 were were very similar. The three estimates were averaged broken, and 27 had poorly defined growth zones and no to obtain a first approximation of total mortality rate age estimates were obtained from them. Of the remain- at Z = 0.551 year1. The values M in accordance ing 583 otoliths, 542 (92.9%) of the readings coincided with the longevity values (more than 17 years) ranged at least twice while 41 (7.1%) yielded conflicting ages between 0.186 and 0.244 years−1, with a mean value and were excluded from the analysis. Annual marks of 0.215 years−1, and the corresponding values of were equal in both the anterior and lateral otolith fields. longevity ranged between 18.9 and 24.7 years. The

Figure 5. Monthly percentage of otoliths with opaque and hyaline edge for all individuals of D. cervinus cervinus off the Canary Islands and monthly evolution of the sea temperature. 412

Figure 6. Length-converted catch curve for all individuals of D. cervinus cervinus off the Canary Islands. a and b are the parameters of the regression line, r is the coefﬁcient of determination and n the number of ﬁsh. The initial data points and the last one marked by were not used in the regression.

Table 1. Observed mean length-at-age (mm) and expected mean Table 2. Parameters of the von Bertalanffy growth curve for length-at-age (mm) according to the von Bertalanffy growth males, females and all fish of D. cervinus cervinus off the Canary curve for all fish of D. cervinus cervinus off the Canary Islands. Islands. N is the number of fish. 2 L∞ k t0 r n Age n All fish (mm) (year−1) (years) (years) Length Length Length Males 619 0.147 −0.84 0.971 114 observed expected range Females 584 0.154 −0.76 0.989 298 (mm) (mm) (mm) All Fish 603 0.149 −0.22 0.987 542 0 4 67 19 51–83 1 10 98 100 72–131 The mean length of fish caught was 271 mm total 2 88 173 169 120–213 length. 3 195 232 229 172–281 4 123 286 281 233–329 Spawner biomass per recruit curve declined quickly 5 55 332 325 300–373 with increasing value of F. At the current level of 6 24 371 364 339–402 exploitation, spawner biomass is much lower than half 7 14 400 397 366–449 of the unexploited level (Figure 7). 8 9 426 425 404–449 9 8 446 450 428–469 10 5 471 471 449–489 Discussion 11 5 491 489 478–509 12 3 507 505 497–515 13 3 519 518 508–529 Among the numerous families of teleosts, sparids 14 2 532 530 523–541 exhibit some of the most diversified expressions of 15 1 547 540 547 sexuality. In this family, both forms of sequential 16 1 551 549 551 hermaphroditism (protogyny and protandry) have been 17 1 565 556 565 recognized, as well as rudimentary hermaphroditism leading to secondary gonochorism (Buxton & Garratt values of F and E were, respectively, 0.336 years−1 1990). This variability is probably linked to the peculiar and 0.61. Fish are first caught at 0 years of age and configuration of the gonad, an ovotestis, that is charac- are fully selected by 3 years of age. Mean length at teristic of all species of the family. The zebra seabream

ﬁrst capture (S50) was estimated at 183 mm (2.2 years). off the Canary Islands exhibits hermaphroditism. This 413

(1988) indicated that the sex ratios of protogynous sparids may be skewed towards the females. In the Canary archipelago, the reproductive season of the zebra seabream extends from spring to summer. Similar results has been obtained for D. cervinus hottentotus in the South African waters (Mann & Buxton 1998). This suggest that the reproduction of D. cervinus subspecies is protected (5–6 months) and occurs when the temperature is comprised between 21◦C and 24◦C. The sexual maturity size differ between sexes and it is mainly determined by the nature of the sexual change. Females attain maturity at 273 mm total length (fourth year of life). Similar results has been observed for D. cervinus hottentotus in the South African waters of the Indian Ocean (Mann & Buxton 1998). This suggest that the maturity at a relatively late age seems Figure 7. Spawning biomass per recruit (SBR) for all individuals to be a characteristic of the D. cervinus subspecies of D. cervinus cervinus off the Canary Islands, with the limits of independently of their sexual typology. the instantaneous rates of natural and fishing mortality of (M = The extension of the recruitment period may relate . −1, = . −1 = . −1, = 0 186 year F 0 365 year ) and (M 0 244 year F to the protracted spawning period observed in the adult 0.305 year−1). population. The recruitment pattern described concurs with the observed for different species of the genus Diplodus in the Mediterranean (Biagi et al. 1995). The characteristic has also been observed for D. cervinus recruitment during late autumn and winter, when the hottentotus in the South African waters of the Indian environmental conditions are more variable suggest Ocean (Mann & Buxton 1998), and for all studied that juveniles present a low level of growth due to cold Diplodus species present in the Canarian archipelago water temperature and limited food available (Planes (Pajuelo & Lorenzo 2001, 2002). The observation of et al. 1999). individuals with well-developed ovotestes and bimodal In their natural environment, large males are often size frequencies, with females occupying the smaller found together with a number of females as discrete size classes, and females biased sex ratios suggest groups over extended periods of time. This suggests the occurrence of protogynous sex changes in this that the mating in D. cervinus cervinus takes place species. However, this sexual pattern is not coincident in a smaller groups formed for one dominant male with the late gonochorism observed for D. cervinus and a group of various females (polygamy). Simi- hottentotus in South Africa. This species is character- lar spawning schools behaviour has been described ized macroscopically for no separation in modal size for other protogynous hermaphrodite sparids such between males and females, for the absence of indi- as Chrysoblephus laticeps (Buxton & Garratt 1990). viduals with well developed ovotestes and for a similar Emilin & Oring (1977) pointed out that the pre- sex ratio between sexes (Mann & Buxton 1998). The requisites for the development of a polygamous mating presence of intersexual individuals in a wide size range system is that at least one of the partners is free from (230–450 mm) suggests that the sex conversion does parental care. This condition is satisfied when consid- not occur simultaneously for all females. The scarcity ering the Diplodus spawning pattern, where, in general, of individuals with both developed ovarian and tes- appears to be pelagic spawners with pelagic larvae and ticular tissues in the samples indicates a rather brief exhibit no parental care. transitory phase between sexes for each individual. The Otoliths show the ring pattern common to teleost absence of females in the largest size classes implies fishes. One calcified opaque ring and one less calci- that sex conversion is essential for all fish. fied translucent ring are laid down each year on the The sex structure of the population, with a predom- otoliths, allowing age determination with relative ease. inance of females on males, is mainly determined by The opaque rings are formed during spring–summer the nature of the sexual change. Related to this, Smale months, when the sea temperature reaches the highest 414 values and the spawning occurs, and the hyaline rings sexual succession and, possibly, the largest females in during winter months, when the temperature reaches an age group are the first to change sex. the lowest values. The water column is well mixed dur- The length at first capture is less than the length at ing the winter and an isotherm is formed during the first maturity, with a 57.8% of the total catch below of spring–summer. The average seawater temperature of this length indicating a danger of recruitment overfish- Canary Islands is 18◦C in February, rising abruptly to ing. Changes in the size structure is due to the size- 24◦C in August–September. This abrupt rise in water selective properties of the gear used. These changes temperature could introduce changes in the metabolic have significant implications for the reproductive out- activity of D. cervinus cervinus during the spring and put because fecundity tends to increase with body size. summer and could be the main factor responsible for So, this population, with a low proportion of larger fish, opaque zone deposition. Lang & Buxton (1996) and has a lower reproductive potential. The average esti- Mann & Buxton (1997) also found that the opaque mate of fishing mortality was higher than the natural zone formation in the otoliths of D. cervinus hottentotus mortality suggesting that D. cervinus cervinus is too takes place during the rapid growth season, when the heavily impacted by fishing pressure. Unfortunately spawning occurs. The data available suggests that the the recruitment into the commercial fisheries occurs increase in seawater temperature affects the physiol- before individuals attain the size at sexual maturity, ogy of otolith growth of the D. cervinus subspecies and all spawner biomass is accessible using the current and results in the formation of the annulus. This is in fishing pattern. This together with the low growth rate, good agreement with Fowler & Doherty (1992) who should not provide sufficient surplus production and pointed out that the physiology of otolith formation is yield per recruit to offer a certain degree of resilence independent of the other somatic and reproductive pro- to high fishing pressure. cesses, taking place within the fish is an independent The direct effects of fishing on the species result physiological response to environmental variations. in changes in the abundance, with a reduction to 85% The oldest fish found in this study was 17 years old. of the unexploited equilibrium level and in the size Mann & Buxton (1998) examined 33 years-old speci- structure, with a decrease of the large size individuals. mens of D. cervinus hottentotus in the South African Related to this, Pope et al. (1988) pointed out that the waters of the Indian Ocean. The differences observed exploitation tends to remove larger individuals from between the studies can be attribute to the differences ecosystems and consequently, increases the abundance in the environmental conditions between the Indian and of smaller individuals and species. the Atlantic Ocean; however, Mann & Buxton (1998) To understand where the D. cervinus subspecies indicated that it is possible to overestimate the age of fit into this life history classification continuum, var- D. cervinus hottentotus as a consequence of the impact ious life history parameters such as maximum length, of cold upwelling on fish growth that may result in maximum age, growth rate, size and age at matu- the deposition of check rings in fish otoliths, which rity must be analyzed together. In this context, the could complicate age estimations. The growth rate of life history parameters of the zebra seabream sug- D. cervinus cervinus is low (0.149 year−1) and very gest that this species has a specialistic life history similar to that obtained by Mann & Buxton (1998) for style. Fisheries based on k-selected sparid species are D. cervinus hottentotus (0.148 year−1). This result indi- more susceptible to growth overfishing and popula- cated that the D. cervinus species are characterized by a tion depletion (Booth & Buxton 1997). Ricker (1963) low-growth rate and a slow attaining of their asymptotic suggests that fish populations which include upwards lengths. of 12 age groups in appreciable quantities prior to The difference in growth between males and females exploitation are extremely sensitive to fishing. In addi- seems to be a characteristic of the protogynous species. tion, slow growth might result in a lower yield per Shapiro (1984) indicated that the mean length of sex unit stock, because of a lower production/biomass ratio reversed individuals is slightly bigger than the average and a slower recovery rate after overexploitation. In length of the females at the same age. Therefore, the consequence, the longevity, the slow growth and the difference in length between males and females of the moderate-low instantaneous rate of natural mortality same age cannot be considered as evidence of inter- of this species make the stock more prone to overex- sexual difference in growth rates because males and ploitation due to a rapid reduction in surplus production females are the same individuals at different phases of (Booth & Buxton 1997). 415

In the Canary Islands a minimum size limit has been Booth, A.J. & C.D. Buxton. 1997. Management of the panga implemented for the target species. In the case of the Pterogymnus laniarius (Pisces: Sparidae), on the Agulhas zebra seabream, the minimum size regulation is of lim- Bank, South Africa using per-recruit models. Fish. Res. 32: ited benefit because the minimum length which may 1–11. Booth, A.J. & A.E. Punt. 1998 Evidence for rebuilding in the be legally kept is smaller than the length at first matu- panga stock on the Agulhas Bank, South Africa. Fish. Res. 34: rity. The practical problem is that this species is only 103–121. one component of the exploited multispecies demersal Buxton, C.D. & P.A. Garratt. 1990. Alternative reproductive fish community and it matures at a different size than styles in seabreams (Pisces: Sparidae). Environ. Biol. Fish. 28: the other species caught jointly (Pajuelo & Lorenzo 113–124. 1995). Therefore, it is susceptible to exploitation at a de la Paz, R. 1975. Systematique´ et phylogenese` des Sparidae du genere Diplodus Raf. (Pisces, Teleostei). Trav. Doc. ORSTOM size when many other coexisting demersal species are 45: 1–96. mature or immature. Another protection strategy has Emilin, S.T. & L.W. Oring. 1977. Ecology, sexual selection, and been introduced with the building of artificial reefs. evolution of the mating systems. Mar. Biol. 86: 109–112. This protection appears to cover only the earlier stages Fowler, A.J. & P.J. Doherty. 1992. Validation of annual growth of life cycle and it encompass only limited areas. When increments in the otoliths of two species of damselfish from immature individuals move out of reefs, they are sub- the southern Great Barrier Reef. Aust. J. Mar. Fresh. Res. 43: 1057–1068 ject to high exploitation level because fishermen deploy Gayanilo, F.C., P. Sparre & D. Pauly. 1996. FAO-ICLARM stock a large number of traps around the reef. assessment tools (Fisat). User’s manual. FAO Computerized A possible option which may improve the situation Information Series (Fisheries), no. 8. FAO, Rome, 126 pp. for all fish species of the benthic community would be Gayanilo, F.C. & D. Pauly. 1997. FAO-ICLARM stock assess- to protect part of the spawning stock and the recruits in ment tools (Fisat). Reference manual. FAO Computer- marine reserves which encompass the coastal inshore ized Information Series (Fisheries), no. 8. FAO, Rome. 262 pp. areas with important algae vegetation or seagrass beds, Gulland, J.A. 1971. The Fish Resources of the Oceans. Fishing and to establish a minimum fishing depth of 30 m to News (Books) Ltd., West Byfleet, 255 pp. protect the nursery areas located in shallow areas. Lang, J.B. & C.D. Buxton. 1996. Growth characteristics in the otoliths of selected South African sparid fish. S. Afr. J. Mar. Sci. 17: 205–216. References Mann, Q. & C.D. Buxton. 1997. Age and growth of Diplodus sargus capensis and Diplodus cervinus hottentotus (Spari- Alagaraja, K. 1984. Simple methods for estimation of parameters dae) on the Tsitsikamma coast, South Africa. Cybium 21: for assessing exploited fish stocks. Ind. J. Fish. 31: 177–208. 135–147. Anderson, R.O. & S.J. Gutreuter. 1983. Length, mass, and asso- Mann, Q. & C.D. Buxton. 1998. The reproductive biology of ciated structural indices. pp. 283–300. In: L.A. Nielsen & Diplodus sargus capensis and Diplodus cervinus hottentotus D.L. Johnson (ed.) Fisheries Techniques, American Fisheries (Sparidae) off the south-east Cape coast, South Africa. Cybium Society, Bethesda. 22: 31–47. Ault, J.S. & N.M. Ehrhardt. 1991. Correction to the Beverton Pajuelo, J.G. & J.M. Lorenzo. 1995. Analisis´ y prediccion´ de la and Holt Z-estimator for truncated catch length-frequency pesquer´ıa demersal de las Islas Canarias mediante un modelo distributions. Fishbyte 9: 37–39. ARIMA. Sci. Mar. 59: 155–164. Bauchot, M.L. & J.C. Hureau. 1990. Sparidae. pp. 790–812. In: Pajuelo, J.G. & J.M. Lorenzo. 2001. Biology of the annular J.C. Quero, J.C. Hureau, C. Karrer, A. Post & L. Saldanha seabream Diplodus annularis (Sparidae), in coastal waters of (ed.) Check-list of the Fishes of the Eastern Tropical Atlantic, the Canary Islands. J. Appl. Ichthyol. 17: 1–5. Clofeta II, UNESCO, Paris. Pajuelo J.G. & J.M.Lorenzo. 2002. Growth and age estimation of Beverton, R.J.H. & S.J. Holt. 1956. A review of methods for Diplodus sargus cadenati (Sparidae) off Canary Islands. Fish. estimating mortality rates in exploited fish populations, with Res. 59: 93–100. special reference to sources of bias in catch sampling. Rapp. Pauly, D. 1980. On the interrelationships between natural mortal- P.-v Reun.´ CIEM 140: 67–83. ity, growth parameters, and mean enviromental temperature in Beverton, R.J.H. & S.J. Holt. 1959. A review of the lifespans 175 fish stocks. J. Cons. Int. Exp. Mer 39: 175–195. and mortality rates of fish in nature, and their relation to Pauly, D. 1983. Some simple methods for the assessment of growth and other physiological characteristics. pp. 142–180. In: tropical fish stock. FAO Fish. Techn. Pap. 234: 1–52. G.E.W. Woilstenholme & M. O’Connor (ed.) Ciba Fundation, Planes, S., E. Macpherson, F. Biagi, A. Garc´ıa-Rubies, Colloquia on Ageing, Churchill, London. J. Harmelin, M. Harmelin-Vivien, J.Y. Jouvenel, L. Tunesi, Tunesi L., Biagi, F. & M. Vacchi. 1995. Visual underwater cen- L. Vigliola & R. Galzin. 1999. Spatio-temporal variability in sus of sparid juveniles of the genus Diplodus in the waters of growth of juvenile sparid fishes from the Mediterranean littoral Liguria and Toscana. Biol. Mar. Mediterr. 2: 461–463. zone. J. Mar. Biol. Ass. U.K. 79: 137–143. 416

Pope, J.G., T.K. Stokes, S.A. Murawski & S.I. Idoine. 1988. Shapiro, D.Y. 1984. Sex reversal and sociodemographic process A comparison of fish size composition in the North Sea and in coral reef fishes. pp. 103–117. In: G.W.Potts & R.J. Woottom on George bank. pp. 146–152. In: W. Wolff, C.J. Soeder & (ed.) Fish Reproduction, Strategies and Tactics, Academic F.R. Drepper (ed.) Ecodynamics, Contributions to Theoretical Press, London. Ecology, Springer Verlag, Berlin. Smale, M.J. 1988. Distribution and reproduction of the reef fish Ricker, W.E. 1963. Big effects from small causes: two examples Petrus rupestris (Pisces: Sparidae) off the coast of South Africa. from fish population dynamics. J. Fish. Res. Board. Can. 20: S. Afr. J. Zool. 23: 272–287. 257–264. Tanaka, S. 1960. Studies on the dynamics and management Rikhter, V.A. & V.N. Efanov. 1976. On one of the approaches to of fish populations. Bull. Tokai Reg. Fish. Res. Lab. 28: estimation of natural mortality of fish populations. ICNAF Res. 1–200. Doc. 76: 1–12. Taylor, C.C. 1960. Natural mortality rate of Georges Bank Saila, S.B., C.W. Recksiek & H. Praguer. 1988. Basic fishery sci- haddock. U.S. Fish Wildlife Service, Fish. Bull. 58: ence programs. A compendium of microcomputer programs 1–7. and manual of operation. Develop. Aquacul. Fish. Sci. 18: Wassef, E.A. 1985. Comparative biological studies of four 1–230. Diplodus species (Pisces, Sparidae). Cybium. 9: 203–215.