Age and growth of Octopus vulgaris Cuvier, 1797, along the East Coast of Tunisia.
Veterinary physiology (Research)
Mosbahi, Dalila Saidane
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: April, 2012 Source Volume: 31 Source Issue: 1|
|Topic:||Event Code: 310 Science & research Computer Subject: Company growth|
|Geographic:||Geographic Scope: Tunisia Geographic Code: 6TUNI Tunisia|
ABSTRACT We describe some growth aspects of Octopus vulgaris
located along the eastern coast of Tunisia. Age and growth parameters of
this species were studied from August 2004 to July 2005 using a modal
progression analysis. Dorsal mantle length (DML)--weight relationships
of O. vulgaris were established for males, females, and both sexes.
Statistical tests show that growth is isometric. Comparison of the
length (DML)--weight relationship for males and females does not show a
significant difference. Absolute growth has been studied according to
the Battacharya method, which allows one to determine the growth
parameters of the yon Bertalanffy model ([L.sub.[infinity]] K, and
[t.sub.0]) and the age-length relationship. The asymptotic length
([L.sub.[infinity]]) and weight ([W.sub.[infinity]]) were estimated to
be 28.3 cm and 6.8 kg, respectively. We compared results with other
studies in different regions. They show a comparable weight growth to
the octopus in the Gabes Gulf and Occidental Mediterranean, but not to
those in the Atlantic. The monthly growth rate of eastern octopus stock
is superior to that seen in the Gabes Gulf.
KEY WORDS: Octopus vulgaris, growth parameters, dorsal mantle length weight relationship, age length relationship, Sahel of Tunisia
The cephalopod Octopus vulgaris is a common species in the Mediterranean Sea. It is one of the most important benthic species in the fisheries of Tunisian waters. It represents half of the national cephalopod catches, and it is appreciated because of its economic contribution, especially to exports. Exploitation is carried out using artisanal gear such as trammel nets and specific pots, and by trawl. The Tunisian octopus fishery is regulated by a fishing period that extends from November 15 to May 15.
The growth of this species has been studied by several authors, including Guerra and Manriquez (1980) in the Occidental Mediterranean, and Hatanaka (1979); and by Domain et al. (2000) and Dia (1988) in the Atlantic. In Tunisia, until now, only 3 studies have been devoted to octopus growth: Ezzeddine-Najai (1992) and Zghidi-Barraj (2002) in the Gabes Gulf, and Khouri (2006) in Monastir (Sahel of Tunisia).
Age determination of cephalopods uses both direct and indirect methods. Direct methods include the examination of statoliths (Gonglaves 1993). Other aging studies have been conducted on octopus beaks (Hernandez-Lopez & Casto- Hernandez 2001, Raya & Hernandez-Gonzalez 1998), but they have so far proved inadequate for aging purposes. Octopus stylets, thought to represent a highly reduced internal shell, consist of a pair of small, widely separated chitinouslike rods embedded within the mantle muscle (Bizikov 2004). This technique was used successfully in aging Octopus pallidus in Australia (which is smaller than O. vulgaris) by Doubleday et al. (2006) and Leporati et al. (2008). However, interpretation is not always very simple (Doubleday et al. 2006) and should be validated using organisms in captivity. Other methods follow growth in captivity (Villanueva 1995) or from tagged organisms (Domain et al. 2000).
In Tunisia, no direct aging study has been conducted, and the validation with aquaculture for O. vulgaris is actually not possible. For these reasons, indirect methods were applied.
These modal progression analysis methods (indirect methods) are based on the analysis of size frequencies, such as Battacharya's method (Battacharya 1967). It consists of following the chronological evolution of length or weight size distribution in the samples that represent the studied population. There are several techniques of decomposing a polymodal structure into modal components.
Estimation of the growth parameters is based on the decomposition of the sample into modes that correspond to cohorts and are characterized by an average size. Using the dates of sampling, successive ages are contributed to these modes.
The management and the stock assessment of Octopus are more difficult than for other species because of its short longevity, fast growth, and size variation. The growth parameters are used in stock assessment models and are very useful to the management of the fisheries.
The aim of this work is to study the growth of O. vulgaris along the east coast of Tunisia (Sousse, Monastir, and Mahdia). Our objectives are to determine the growth parameters for the von Bertalanffy equation needed in assessment models and the age of Octopus in this area, and to characterize the octopus fishery in the eastern part of Tunisia.
MATERIALS AND METHODS
Relative Weight Growth
The application of the dorsal mantle length (DML)--weight relationship was carried out on 324 specimens (191 males and 133 females) collected from coastal and trawling fisheries operating in the same area studied. DML values, used as a reference length in the samples, ranged from 6.5-24 cm. The length weight equations were established for both sexes, separately and cumulated, using the following equation:
W = a x [DML.sup.b]
where W is the full weight, a is a constant (intercept of the regression), DML is the dorsal mantle length, and b is the allometry coefficient (regression coefficient). After logarithmic transformation, the relationship becomes as follows:
LogW = log a + b x log(DML)
To determine the nature of allometry, we have compared the value of the parameter b with the theoretical value 3 using the t-test at 5% (P < 0.05). Parameters a and b for the linear correlation were compared using Mayrat's test (Mayrat 1967). First, we proceeded by confronting the coefficients taken 2 by 2 using the regression coefficient b - test (bet) as follows:
bet = [([b.sub.1] - [b.sub.2])] / [([delta][y.sup.2]([b.sub.1] - [b.sub.2])).sup.1/2]
where df is n - 4, [delta][y.sup.2] is the variance of y and [b.sub.1] - [b.sub.2] (the regression coefficient b of the 2 curves.
If this difference is insignificant (bet < 1.96), the 2 coefficients are statistically equal and the growth is homogeneous for the 2 sexes. In this case, we proceed by comparing the parameter a of the linearized equation using the position test according to Mayrat (1967).
Samples were collected monthly from August 2004 to July 2005 from coastal and trawling landings. Size frequency histograms were determined for both sexes of O. vulgaris. A total of 3,100 individuals were sampled and measured monthly during 12 mo in the Sahel of Tunisia (Sousse, Monastir, and Mahdia; Fig. l).
Modal decomposition of the distributions was carried out according to Battacharya's method (Battacharya 1967) using the adapted software FISAT (Gayanilo et al. 1996).
To determine the growth parameters ([L.sub.[infinity]] and K), we applied the von Bertalanffy model:
[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]
where [L.sub.t] is the DML at moment t, [L.sub.[infinity]] is the asymptomatic length, to is the theoretical age corresponding to size 0, and k is the growth coefficient. The adjustment of the growth curve was made with STATISTICA software (Statistica 1984-2005, Statsoft, Inc.).
The growth in weight was also realized according to the von Bertalanffy model using the following equation:
[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]
where [W.sub.t] is the full weight at moment t, [W.sub.[infinity]] is the asymptomatic weight corresponding to the asymptomatic length [L.sub.[infinity]] b is the regression coefficient between the 2 variables [W.sub.t] and DML, k and [t.sub.0] are growth parameters obtained from the yon Bertalanffy equation.
Dorsal Mantle Length-Weight Relationship
Equations describing the DML-weight relationship for males, females, and both sexes are shown in Table 1. The values of the coefficient of correlation show that the DML and the total weight are significantly correlated.
[FIGURE 1 OMITTED]
The comparison of parameter b of different equations with the theoretical value 3 shows that the length (DML)-weight relationship is isometric for both sexes. The comparison of parameter b and parameter a using the linearized equation representing the length (DML)-weight relationship in males and females does not show any significant difference. (Test of bent comparison (bet) of parameter b is 0.5677 with df = 4; test of position comparison for parameter a is 1.4862 with df = 3.) So, the relative weight growth is the same for both sexes, and the 2 lines can be integrated into 1 line (Fig. 2).
The monthly distributions of the size frequencies are illustrated by the histograms in Figure 3. During the fishing period, defined by legislation as November 15 to May 15, the size distribution shows an increase from the beginning of the fishing period, which corresponds to the recruitment period, to the end of the period (May). The distribution decomposition using Battacharya's method allowed us to determine the parameters of the von Bertalanffy equation. The growth parameters were estimated without taking into account seasonal variations (monthly measurements are used indifferently). Thus, the relationship between growth O. vulgaris in the eastern region (Lt) and its age (t; Fig. 4) becomes the following:
[L.sub.t] = 28.3 x (1 - [e.sup.-1.122x(t-0.008)])
The combination of the von Bertalanffy equation and the DML-weight equation (W = 0.3992 x [DML.sup.2.9246]) allowed us to determine the equation that describes the absolute weight growth:
[W.sub.t] = 6800.91 x [(1 - [e.sup.-1.122x(t-0"008)]).sup.2.9146]
where [W.sub.t] is the total weight of the animal at time t (measured in grams and t is age (measured in years).
The keys for age-length and age-weight (Table 2) allowed us to calculate the average values of the monthly rates of mantle length and weight growth.
DISCUSSION AND CONCLUSION
The comparison of our results with the available literature, such as the works of Zghidi-Barraj (2002) on the octopi of the southern Tunisian coast, Guerra (1979) on octopi of the Occidental Mediterranean Sea, and Hatanaka (1979) and Dia (1988) on the coasts of the Atlantic (Table 3) has allowed to draw some conclusions about the weight growth of the octopus in these different areas.
Octopi of the eastern coast of Tunisia have a weight growth comparable with that of octopi in the Gabes Gulf (DML, 14 cm). Octopi from the southern coast are 200 g larger. The weight growth of octopi from Tunisia's southern coast is comparable with that of octopi in the Occidental Mediterranean Sea, although it is clearly inferior to that of the octopi of the northeastern coast of the Atlantic. As an example, at a size of 14 cm, an octopus from the eastern coast of Tunisia weighs 872.98 g whereas one from Mauritania weighs 1,460 g.
The relationships DML-weight show that the weight growth of octopi from the east coast of Tunisia is isometric for both sexes (parameter b does not differ significantly from the theoretical value 3). These results agree with those of octopi in the Gabes Gulf (Zghidi-Barraj 2002).
The von Bertalanffy parameters obtained in the current study were compared with results from other regions (Table 4). Thus, the values of [L.sub.[infinity]] determined in the populations of octopi in the Occidental Mediterranean Sea (Guerra 1979), in the Gabes Gulf (Zghidi-Barraj 2002), and along the coast of Mauritania (Hatanaka 1979), which are, respectively, 30 cm, 29.6 cm, and 27.68 cm, are not different from [L.sub.[infinity]] of octopi along the eastern coast of Tunisia ([L.sub.[infinity]] = 28.3 cm). This could be related to similarities in biotic parameters.
[FIGURE 2 OMITTED]
The asymptotic values [L.sub.[infinity]] and [W.sub.[infinity]] of the east-central Atlantic are, respectively, 40 cm and 20 kg. Guerra (1979) estimated the rate of linear growth to 13.4 mm/mo; so, the Atlantic octopus shows a greater length and weight growth in relation to octopi from the Occidental Mediterranean Sea and from those off the east coast of Tunisia. These results are in agreement with our conclusions made on the basis of the analysis of the DML weight equations.
[FIGURE 3 OMITTED]
[FIGURE 4 OMITTED]
The monthly rate of growth of octopi along the east coast of Tunisia is superior to that of octopi in the Gabes Gulf. This result shows that the weight and length growth of the latter are inferior to those of octopi from the East. The maximum theoretical asymptotic lengths of octopi from the south ([L.sub.[infinity]] = 29.6 cm, [W.sub.[infinity]] = 10,067.52 g) are, however, superior to those of the octopi from the East ([L.sub.[infinity]] = 28.3 cm, [W.sub.[infinity]] = 6,800.91 g), confirmed also by the octopi samples from the Monastir region published by Khouri (2006). In other words, the octopi of the East, although they grow relatively faster than the octopi of the south, reach inferior maximal sizes. In addition, Guerra (1979) noticed that the monthly growth rate of octopi from the Occidental Mediterranean Sea (10-12 mm) is comparable with that reached by octopi from the eastern coast of Tunisia, estimated at 12.1 mm/mo. In the Gabes Gulf, an octopus with a mantle that measures 6.92 cm (corresponding to 129 g in weight) reaches a mantle length equal to 16.65 cm in 15 mo, which corresponds to an average rate of linear growth of 0.81 cm/mo. This rate is significantly less than that of the octopi in the eastern region. The weight and mantle length growth of octopi from the Occidental Mediterranean Sea and along Tunisia are comparable. Guerra (1979) mentioned that octopi from the Occidental Mediterranean Sea, measuring 3 cm, reaches a DML equal to 19-20 cm in 17 mo, which corresponds to an average rate of linear growth of 10 mm/mo. This rate is comparable with that estimated for the octopi of the eastern coast of Tunisia (12.1 mm/mo).
The growth of O. vulgaris depends on abiotic factors (temperature) and on biotic factors (availability of trophic resources). The last factor seems to be determinant in the growth of octopi. The temperature influences considerably on the precocious growth of the animal during the planktonic postembryonic phase and during the first periods of benthic life. It does not seem to influence growth in adults and subadults (Semmens et al. 2004).
The weight growth of the Atlantic octopus is relatively superior to that of species living in East Tunisian waters and in the Gabes Gulf. It could be attributed to the abundance of the productivity and the food in the Atlantic favored by the presence of upwelling phenomena, or to a possible genetic difference between the 2 populations. The difference in weight in favor of the octopi from the Gabes Gulf compared with those of the eastern coast could be explained by temperature and the availability of trophic resources.
In the Sahel of Tunisia, the average sea surface temperature during 2006 was about 13[degrees]C in winter and 28[degrees]C in summer. Jabeur et al. (2010) demonstrated that fishery production was influenced positively by the cold season but negatively by hotseason temperatures. The influence of the temperature on abundance of octopi has also studied in Spain by Vargas-Yanez et al. (2009).
The difference in monthly growth rate could be explained by a shorter longevity resulting from precocious maturation of the octopi along the eastern coast of Tunisia relative to those of the octopi in the Gabes Gulf, or by a possibility of different populations in these 2 regions.
From hatching to adult, O. vulgaris goes through two distinct phases of growth. The first phase covers the planktonic period of postembryonic development, and the second period represents benthic life. During this phase, the weight and the length of the animal grow exponentially with age, with a constant rate of growth (Mangold & Boletzky 1973, Mangold 1983b). Beyond a certain weight, estimated by Mangold (1983a) to be 100-150 g at a temperature of 20[degrees]C, the rate of growth slows and a second logarithmic phase of growth starts.
The growth in length (DML) of O. vulgaris with age indicates a progressive decrease in growth with age (Fig. 4). The tendency toward an asymptotic length proves the existence of factors limiting growth. Indeed, it is because of the short lifetime of O. vulgaris, because its death occurs after laying eggs, that the asymptotic length [L.sub.[infinity]] as well as the asymptotic weight [W.sub.[infinity]] is never reached. In the case of the giant octopus of the Pacific, Mangold-Wirz (1963) noted that these individuals are not obligatorily so old; they have probably a rapid and important growth. The yon Bertalanffy model applied to O. vulgaris, which has a short life span, is useful in its exponential phase but less so in the asymptotic one. So, the global models seem to be more applicable to manage the stock of this species. The comparison between growth of females and males should be carried out by different maturity stages.
Samples used in this study come from landings that can probably induce a bias in estimated values, but sampling was made on different sizes that represent the population. Direct and indirect methods in aging of cephalopods have limits. A commonly applied method that uses mantle length as the defining measure of octopus growth--modal progression analysis--relies on the assumption that age is closely related to size (Challier et al. 2002). However, cephalopod growth in general is extremely variable (Semmens et al. 2004). Size variability is more important for total length than for DML. Variability related to the elasticity of the mantle was not avoided in this study. Measurements were released as possible on longed mantle. This could also influence the age-length relationship.
Direct methods such as aging from statoliths, beaks, and stylets also have their limits. Thus, the quantification of daily growth increments using statoliths have been used successfully to age many species of squid (Jackson 1994) and some cuttlefish (Bettencourt & Guerra 2001), but not for octopus (Tait 1980). Hernandez-Lopez & Casto-Hernandez
(2001) tested octopus beaks, but they proved inadequate for aging purposes. Perales-Raya et al. (2010) recommends the use of the lateral wall surface of the beak when aging adult common octopus. Baqueiro Cardenas et al. (2011) demonstrates the possibility of using the octopus eye lens as an age indicator. Octopus stylets, thought to represent a highly reduced internal shell, have been suggested that these unique and little known structures are a potentially useful aging tool as a result of the discovery of regular growth increments (Sousa Reis & Fernandes 2002). To determine whether such increments are age related, their periodicity or rate of formation needs to be assessed and validated.
Doubleday et al. (2006) explain that, despite the efficiency of using stylet increments in aging O. pallidus, several problems regarding this method were encountered, such as inadequate increment visualization in the inner region resulting from a combination of opacity or pigmentation, and narrow and faint increments. Otherwise, the interpretation of increments should be validated in captivity (by aquaculture).
In O. vulgaris, no test of aging by stylet was realized. This species is bigger than O. pallidus, and probably the stylet will be more opaque. Similarly, Baqueiro Cardenas et al. (2011) show that the use of stylets in aging Enteroctopus megaloeyathus has not given satisfactory age readings.
Mangold (1983a) indicates that cephalopods grow until they reach sexual maturity, at which point growth stops or even declines, so the model of von Bertalanffy, which is largely used for fish, is not the best for O. vulgaris, but it can describe the exponential phase.
The authors thank A. Afli, S. Souissi, Afifa, Manel and the reviewers for their comments to improve this manuscript. Thanks also to The INSTM center for the sampling.
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CHEDIA JABEUR, (1) * TAOUFIK NOUIRA, (2 [dagger]) WIDIEN KHOUFI, (1) DALILA SAIDANE MOSBAHI, (1) AND SOUFIA EZZEDDINE-NAJAI (2)
(1) Laboratory of Analysis, Treatment and Valorization of Products and Pollutants of the Environment Faculty of Pharmacy, 5000 Monastir, Tunisia; (2) National Institute of Sciences and Technologies of the Sea, 2025 Salammbo, Tunisia
* Corresponding author. E-mail: firstname.lastname@example.org
([dagger]) Chedia Jabeur and Taoufik Nouira both contributed equally to this manuscript.
TABLE 1. Dorsal mantle length (DML)-weight equations of Octopus vulgaris. Relationship 1 Male W = 0.4856 [DML.sup.2.8335] Female W = 0.3709 [DML.sup.2.9444] Both sexes W = 0.3992 [DML.sup.2.9146] Relationship 2 Allometry r Male log (W) = 2.8335 log (DML)--0.3137 Isometric 0.9606 Female log (W) = 2.9444 log (DML)--0.4307 Isometric 0.9758 Both sexes log (W) = 2.9146 log (DML)--0.3988 Isometric 0.9721 n t Male 133 1.678 (-) Female 191 0.8292 (-) Both sexes 324 1.5642 (-) W: full weight; DML, dorsal mantle-length; r: coefficient of correlation; t: student's test; (), significance of the t-test at 5%. TABLE 2. Age-length and age-weight keys of Octopus vulgaris along the east coast of Tunisia. Age (mo) DML (cm) Weight (g) 3 6.72 103.36 4 8.65 215.23 5 10.4 368.5 6 12 558.64 7 13.45 779.63 8 14.78 1,024.96 9 15.99 1,288.24 10 17.08 1,563.55 11 18.09 1,845.61 12 19 2,129.87 13 19.83 2,412.52 14 20.58 2,690.42 15 21.27 2,961.12 16 21.9 3,222.69 17 22.47 3,473.72 18 22.99 3,713.23 19 23.46 3,940.57 20 23.89 4,155.41 21 24.29 4,357.64 22 24.64 4,547.35 23 24.97 4,724.78 24 25.27 4,890.27 25 25.54 5,044.27 26 25.78 5,187 27 26.01 5,319 28 26.21 5,442 29 26.40 5,555.65 30 26.40 5,660.14 DML, dorsal mantle length. TABLE 3. Dorsal mantle length (DML}-weight relationships of Octopus vulgaris established in different areas. Unit of Authors Fishing Area Length Guerra and Catalan Sea (Occidental cm Manriquez Mediterranean) (1980) Dia (1988) Mauritanian coast cm (northeast Atlantic) Smale and Aquaculture mm Buchan (1981) Zghidi-Barraj Gabes Gulf cm (2002) (Tunisia, central Mediterranean) Current study Eastern coast of cm Tunisia (Oriental Mediterranean) Interval Authors DML-Weight Relationship of Validity r Guerra and M: W = 0.350 [DML.sup.2.988] -- 0.98 Manriquez F: W = 0.542 [DML.sup.2.804] -- 0.97 (1980) T: W = 0.420 [DML.sup.2.917] 3-22 cm 0.97 Dia (1988) M: W = 0.89 [DML.sup.2.84] 7-16 cm 0.91 F: W = 4.67 [DML.sup.2.12] 8-15 cm 0.87 T: W = 1.84 [DML.sup.2.53] 7-16 cm 0.89 Smale and M: W = 13.78.[10.sup.-4] 49-215 mm 0.95 [DML.sup.2.74] Buchan (1981) F: W = 86.83.[10.sup.-5] 46-215 mm 0.97 [DML.sup.2.83] T: W = 99.18.[10.sup.-5] 46-215 mm 0.97 [DML.sup.2.80] Zghidi-Barraj M: W = 0.3188 [DML.sup.3.076] 5-24 cm 0.94 (2002) F: W = 0.4514 [DML.sup.2.942] 4.5-27.5 cm 0.92 T: W = 0.3911 [DML.sup.2.997] 4.5-27.5 cm 0.93 Current study M: W = 0.4856 [DML.sup.2.8335] 8-24 cm 0.9606 F: W = 0.3709 [DML.sup.2.9444] 6.5-26.5 cm 0.9758 T: W = 0.3929 [DML.sup.2.9146] 6.5-26.5 cm 0.9721 F, female; M, males; T, total (both sexes); W, full weight. TABLE 4. von Bertalanffy equations and growth parameters of Octopus vulgaris reported in different areas. Authors and Regions von Bertalanffy Equation Guerra (1979), [L.sub.t] = 30 x ([1-e.sup.-0.06 x Occidental (1 - 3.0)]) Mediterranean Hatanaka (1979), -- Mauritanian coast Zghidi-Barraj [L.sub.t] = 29.6 x ([1-e.sup.-0.56 x (2002), Gabes Gulf (t + 0.225)]) Current study, [L.sub.t] = 28.3 x ([1-e.sup.1.122 x eastern Tunisian (t - 0.0008)]) coast Asymptotic Length Catabolic Authors and Regions [L.sub.[infinity]] (cm) Coefficient K Guerra (1979), 30 0.06 Occidental Mediterranean Hatanaka (1979), 27.68 0.48 Mauritanian coast Zghidi-Barraj 29.6 0.56 (2002), Gabes Gulf Current study, 28.3 1.122 eastern Tunisian coast
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