253 (2000) 63–74
www.elsevier.nl / locate / jembe
Molecular and morphologic approaches to discrimination of
variability patterns in chub mackerel, Scomber japonicus
a ,* b,c a a
´ ´ ´ ´
Marıa Ines Roldan , Ricardo G. Perrotta , Martı Cortey , Carles Pla
a
`
Laboratori d’Ictiologia Genetica, Universitat de Girona, Campus Montilivi, E-17071 Girona, Spain
b
´
Instituto Nacional de Investigacion y Desarrollo Pesquero(INIDEP), Victoria Ocampo 1, 7600 Mar del Plata, Argentina
c
Departamento de Ciencias Marinas, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina
Received 18 March 2000; received in revised form 18 May 2000; accepted 26 June 2000
Abstract
The systematic status and the evolutionary biology of chub mackerel (Scomber japonicus) in the South West Atlantic Ocean is confusing with an unknown degree of genetic differentiation and reproductive isolation between units. Simultaneous genetic and morphologic analyses were made on 227 fish collected from two areas of the South West Atlantic Ocean and one from the Mediterranean Sea. The genetic analysis was based on 36 protein-coding loci, 16 of which were variable. The morphologic analyses include six morphometric length measurements and a meristic character. Correspondence between genetic and morphologic variability patterns indicates isolated Mediterranean and Southwest Atlantic subgroups of S. japonicus and, less clearly, possible additional divergence in two regional stocks within the latter group. The most conservative approach to management is to manage the stocks independently of one another. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Chub mackerel; Scomber japonicus; Isozymes; Morphology; Population structure; Fisheries
1. Introduction
Chub mackerel (Scomber japonicus) is a widely exploited pelagic species with a total catch of 2,423,235 metric tons in 1997, taking it to fifth place in the total world nominal catches (FAO, 1997). S. japonicus has a cosmopolitan distribution including warm and temperate waters of the Atlantic, Indian and Pacific Oceans and adjacent seas. As a
*Corresponding author. Tel.:134-972-418-961; fax:134-972-418-277. ´
E-mail address: [email protected] (M.I. Roldan).
consequence of its broad distribution and the existence of oceanographical barriers, the species may be comprised of multiple disjunct populations. In the South West Atlantic Ocean, many studies of local fishing grounds have highlighted different aspects of the
´
species’ biology (Perrotta, 1992, 1993; Pajaro, 1993; Perrotta and Christiansen, 1993; Perrotta et al., 1997) and the fishery (Perrotta and Pertierra, 1993; Perrotta et al., 1998b). Two fishing stocks of chub mackerel (north and south of latitude 398009S) have been designated by their seasonal occurrence, observed behaviour and environmentally induced morphometric characteristics. These stocks are operational units used in fishery management, with small purse-seining boats (Lampara net) operating in the Mar del
´
Plata area and large trawling boats in El Rincon (Perrotta et al., 1998a).
Allozyme data have clarified intraspecific relationships in two mackerel species (Scomber scombrus, Jamieson and Smith, 1987, and references therein; Scomberomorus
cavalla, Johnson et al., 1994). Nevertheless, in spite of the interest to fisheries, no study
has been published on S. japonicus.
This paper examines the population structure of chub mackerel in the South West Atlantic Ocean based on genetic variation at 16 protein-coding loci and seven morphologic characters. Moreover, we summarize current information on growth, migration and spawning time and propose a possible mechanism to explain the observed patterns with regard to the water circulation of the area. We also compare levels of genetic diversity and differentiation with the North Atlantic population (Mediterranean Sea).
2. Methods
2.1. Sample collection
Chub mackerels (136–423 mm total length) were caught at about 50 m depth by INIDEP’s research vessels in the Argentinian Sea and immediately frozen with dry ice.
´ ´
Two geographical areas, Rıo de la Plata (sample 1: 358269S, 548319W) and El Rincon (sample 2: 408129S, 608099W), were sampled (N5102) during May and August 1996, respectively. The Mediterranean sample was captured in December 1997 (sample 3: 468509N, 58159E) approximately in front of Pals (Fig. 1). All individuals were stored at 2808C prior to electrophoretic analysis.
2.2. Genetic analysis
Tissue extractions, electrophoresis and procedures for visualizing proteins generally followed the methods outlined by Aebersold et al. (1987). Extracts from liver, eye and skeletal muscle were electrophoretically screened for resolution and activity with the buffer systems and stain procedures detailed in Table 1. Genetic interpretations of these patterns followed the principles outlined by Utter et al. (1987). Alleles were denoted according to their mobility relative to the most commonly observed allele, which was assigned a mobility of 100 units. Genetic nomenclature follows Shaklee et al. (1990).
Fig. 1. South West Atlantic distribution of Scomber japonicus (diagonal lines), spawning area (grey), samples sites (1 and 2) and Mediterranean sample site (3).
samples were tested by contingency chi-square, and the sequential Bonferroni technique (Rice, 1989) was used to adjust significance levels. Within-sample variation was assessed by mean unbiased expected heterozygosity per locus (He) (Nei, 1978). Genetic differentiation of populations was assessed by F-statistics (Wright, 1978). Pairwise multilocus comparisons between samples were calculated by Nei genetic distance (Nei, 1972) and Cavalli-Sforza and Edwards chord distance (Cavalli-Sforza and Edwards, 1967).
2.3. Morphologic analysis
Table 1
a
Enzyme systems, loci abbreviations and tissues with strongest expression in S. japonicus
Enzyme E.C. No. Locus Tissue Buffer Stain
Aspartate aminotransferase 2.6.1.1 AAT-1* L, E 2, 4, 5, 1 1 AAT-2* M, L, E
Creatine kinase 2.7.3.2 CK-2* M, L, E 2, 3, 6, 1 1
CK-3* M
Esterase 3.1.1.- EST-2* M, L, E 3, 1 1
Fumarate hydratase 4.2.1.2 FH* L, M 6, 4, 1, 2 1
b-N-Acetylgalactosaminidase 3.2.1.53 bGALA* L 3, 2, 6, 4 1 Glyceraldehyde-3-phosphate 1.2.1.12 GAPDH-1* M, L 5, 2 1
dehydrogenase GAPDH-2* M, L, E
Glycerol-3-phosphate 1.1.1.18 G3PDH-1* M 4, 5, 6, 2, 1
dehydrogenase G3PDH-2* M, L, E 3
N-Acetyl-b-glucosaminidase 3.2.1.30 bGLUA* L 6 3 Glucose-6-phosphate
b
dehydrogenase 1.1.1.49 G6PDH* M, L, E 7, 6, 4, 3 2
Glucose-6-phosphate isomerase 5.3.1.9 GPI-1* M 4, 3, 1 1
GPI-2* E
Glutamate dehydrogenase 1.4.1.2 GLUDH* L 3, 5 1
Glutation reductase 1.6.4.2 GR* L 3, 1 1
b
Isocitrate dehydrogenase 1.1.1.42 IDHP-1* M 2 2
IDHP-2* M, L
b
L-Lactate dehydrogenase 1.1.1.27 LDH-1* M, L 2, 4, 1, 3 2
LDH-2* E
LDH-3* M, L, E
Lactoylglutathione lyase 4.4.1.5 LGL* M, L, E 1, 5, 3 1
b
Malate dehydrogenase 1.1.1.37 MDH-2* M, L, E 2 2
MDH-3* M, L, E
Peptidase (leucyl-glycyl-glycine) 3.4.-.- PEP-LGG* M, L, E 4, 5 3 Peptidase (leucyl-tyrosine) 3.4.-.- PEP-LT* M, L, E 4, 5 3
Phosphoglucomutase 5.4.2.2 PGM-2* M, L, E 2, 4, 1 1
Phosphogluconate dehydrogenase 1.1.1.4 PGDH* L, M 2 1
Pyruvate kinase 2.7.1.40 PK-2* M, L, E 3, 6, 2, 1 5
Superoxide dismutase 1.15.1.1 SOD* M, L, E 2, 5, 1 1
a
Buffers: 1, TC / LB; 2, AC; 3, Poulik; 4, TBE; 5, TBE1NAD; 6, TP; 7, TP1NADP. Stains: 1, Aebersold et al. (1987); 2, Allendorf et al. (1977); 3, Jorde et al. (1991); 4, Verspoor and Jordan (1989); 5, Pasteur et al. (1988).
b
Stain modified with agar 2%.
Table 2
a
Estimates of the power function by linear regression analysis
Sample Relation Ln a b r
´
Rıo de la Plata Lc /Lt 0.444 0.639 0.769 (N535) B1 /Lt 23.457 1.048 0.769 B2 /Lt 21.701 0.908 0.757 Dp1 /Lt 20.132 0.808 0.787 Dp2 /Lt 20.007 0.910 0.920 Io /Lt 24.279 1.246 0.796 ´
El Rincon Lc /Lt 20.403 0.797 0.970 (N532) B1 /Lt 22.018 0.773 0.709 B2 /Lt 20.876 0.768 0.922 Dp1 /Lt 21.132 0.976 0.984 Dp2 /Lt 20.606 1.001 0.989 Io /Lt 21.659 0.771 0.863
Pals Lc /Lt 20.599 0.850 0.972
(N519) B1 /Lt 23.243 0.991 0.881 B2 /Lt 22.000 0.948 0.920 Dp1 /Lt 20.900 0.953 0.984 Dp2 /Lt 20.412 0.975 0.987 Io /Lt 22.189 0.863 0.882
a
Lt, total length; Lc, head length; B1, mouth width; B2, mandible length; Dp1 and Dp2, snout to dorsal 1 and 2 distances; Io, interorbital length. All variables in mm.
was 264.09 mm total length (average length of total samples). The relationship between
b
y versus Lt (total length) is y5aLt , which in lineal form is ln y5ln a1b ln Lt, where b is the allometric coefficient (Table 2). Principal components analysis and discriminant
functions analysis were performed (Bouroche and Saporta, 1983) by AMACP and AMDIS software.
3. Results
3.1. Genetic variation
We interpreted the banding patterns of 25 enzyme systems to reflect 36 genetic loci (Table 1), 20 of which were monomorphic, with apparent Mendelian variation detected
Table 3
Basic statistics of the pectoral fin rays of S. japonicus
for the remaining 16 loci (Table 4). In eight of these polymorphic loci, the frequency of the common allele was higher than 0.95 in all samples. The remaining loci were considered as highly polymorphic (PGDH*, G3PDH-1*, G3PDH-2*, G6PDH*,
GPI-Table 4
Allele frequencies of 16 polymorphic loci of S. japonicus (sample size)
Locus Allele South West Atlantic Mediterranean
Ocean Sea
´ ´
Rıo de la Plata El Rincon Pals
(102) (102) (23)
AAT-1* *100 0.980 0.995 1.000
*65 0.015 0.005
*125 0.005
AAT-2* *-100 0.995 0.990 1.000
*-108 0.005 0.010
PGM-2* *-100 0.995 0.995 1.000
*-108 0.005 0.005
PGDH* *100 0.899 0.931 0.957
*110 0.061 0.037
*117 0.035 0.021 0.043
*120 0.005 0.005
*83 0.005
G3PDH-1* *100 0.858 0.864 0.826
*125 0.142 0.136 0.174
G3PDH-2* *100 1.000 0.995 0.870
*105 0.005 0.130
G6PDH* *100 0.941 1.000 1.000
*115 0.059
GPI-2* *100 0.686 0.717 0.522
*76 0.309 0.222 0.435
*112 0.005 0.061 0.043
GR* *100 0.995 0.995 1.000
*93 0.005 0.005
IDHP-1* *100 1.000 0.990 0.978
*-200 0.005 0.022
*400 0.005
IDHP-2* *100 0.995 0.995 1.000
*82 0.005 0.005
LDH-1* *100 0.995 1.000 1.000
*110 0.005
MDH-4* *100 0.990 0.995 1.000
*133 0.005
*78 0.005 0.005
PEP-LGG* *100 0.966 0.970 0.804
*92 0.025 0.152
*117 0.010 0.030 0.043
PEP-LT* *100 1.000 0.975 0.870
*95 0.025 0.130
SOD* *100 0.853 0.824 0.913
*160 0.142 0.162 0.087
2*, PEP-LGG*, PEP-LT*, SOD* ) with the frequency of variant alleles exceeding 5% in one or more samples. The average proportion of polymorphic loci (0.05 criterion) among
´
the three collections was 13.9%, ranging between 11.1% (El Rincon) and 16.7% (Pals). Overall average heterozygosity for all 36 loci was 0.043 and ranged between 0.036 (El
´
Rincon) and 0.054 (Pals).
´ Only two of 35 tests for Hardy–Weinberg genotypic proportions were significant (Rıo de la Plata G3PDH-1*, G6PDH* ) due to a deficit of heterozygotes.
Allele frequency differences among samples (Table 5) were significant over all collections at five loci (G3PDH-2*, G6PDH*, GPI-2*, PEP-LGG*, PEP-LT* ). This significant variation is the basis for patterns of relationships and distinction among the collections that emerge through reinspection of Table 4, and the pairwise measures of genetic variation.
Collections from Atlantic and Mediterranean waters appear to be differentiated by several criteria. Differences in the distribution of allele frequencies are evident at
PGDH*110, G3PDH-2*105, GPI-2*76, PEP-LGG*92. Samples of both regions are separated in neighbour-joining clusters. Cavalli-Sforza and Edwards chord distance
´ ´
values between the Pals sample and Atlantic samples (Rıo de la Plata, 0.082; El Rincon, 0.073) are the highest detected. The Atlantic and Mediterranean division is further indicated by consideration of the variation over all loci. The higher gene diversity (F ,ST Table 5) over all collections (0.025) is similar to the Atlantic vs. Mediterranean (0.021) samples.
The allelic distribution among the Atlantic samples shows no clear differentiation with
Table 5
FST analyses at all loci for different groupings of S. japonicus. Probabilities are based on contingency chi-squared analyses
Locus Total Atlantic Atl. vs.
samples Med.
AAT-1* 0.002 0.005 20.003
AAT-2* 0.000 0.000 0.000
G3PDH-1* 0.002 0.000 0.002
G3PDH-2* 0.084* 0.000 0.084*
G6PDH* 0.035* 0.081* 20.050
GPI-2* 0.025* 0.005* 0.020
GR* 0.002 0.000 0.002
IDHP-1* 0.005 0.000 0.005
IDHP-2* 0.002 0.000 0.002
LDH-1* 20.002 0.002 20.004
MDH-4* 0.000 0.001 20.001
an incipient one only at G6PDH*115, GPI-2*112, PEP-LT*95. The overall similarity of these collections is further reflected in their small distance (0.048).
3.2. Morphologic variation
In Fig. 2 individuals are plotted into the space defined by the two principal components of the morphologic diversity matrix; these first two axes explained 48.62% of the total variability. The first component explained 28.79% of the variability and was strongly influenced by variables related to head size: mouth width, mandible length and interorbital length (factor loading 0.77, 0.65 and 0.64, respectively). All Pals individuals were placed together with negative values for both components, and clearly separated from Southern Atlantic fish. Although a small overlapping area (16.4%) was observed between the two Argentinian samples, most individuals were distinguished according to
´ ´
their original sample, from Rıo de la Plata or from El Rincon. Greater head length but
´ ´
lower mouth width and interorbital length in Rıo de la Plata compared with El Rincon is the primary character difference.
With respect to the discriminant function analyses, the number of individuals per sample correctly classified averaged 65.1%. The highest classification success rate was
´ ´
observed in Pals with 100%, with El Rincon and Rıo de la Plata samples showing 59.4 and 51.4%, respectively.
4. Discussion
The genetic and morphologic data reveal the clear existence of two groups, Mediterranean and Southern Atlantic, and some evidence of stock separations between
´ ´
Rıo de la Plata and El Rincon samples (Fig. 2). The magnitude of Nei’s genetic distance (Nei, 1972; 0.003) between Pals and Argentinian chub mackerel populations does not support the subspecific status (S. japonicus marplatensis) proposed by Lopez (1959) for the Southwestern Atlantic group. However, both data sets support genetic and mor-phological distinctions between Mediterranean and Southwestern Atlantic populations.
The distinction between the two Argentinian collections is less clear. The presence or absence of alleles at three loci in one or the other location is consistent with some subpopulation structures. However, alternatives such as localized reflections of transitory favorable survivals of individual matings (Hedgecock, 1994) or other sampling effects remain possibilities. We interpret the genetic differences to isolation within perhaps the last 100,000 years, with little or no migration. The relatively high number of alleles per locus (2.6) is consistent with large effective population sizes (Chakraborty et al., 1980) which would retard the divergence from genetic drift of the two demographic units. This conclusion is supported by the morphological data (Fig. 2). Despite the unknown environmental and genetic influences of these morphological distinctions, the presence of two discrete groups of individuals is consistent with the limited contemporary migration in two distinct environments. Further understanding of these relationships must await broader samplings throughout the species range, collections of potentially more discriminating molecular genetic data such as microsatellites with higher mutation rates (Grant et al., 1999), and physical tagging programs designed to measure long distance movements of chub mackerels.
Morphologic results provided details of chub mackerel shape, showing the importance of head size as a principal factor affecting differentiation between the samples examined.
´ ´
The El Rincon mackerels showed more posterior development than Rıo de la Plata mackerels, perhaps attibutable to growth responses to the differing habitats arising from the oceanographical and ecological conditions. The greater zooplankton productivity of
´
the Rıo de la Plata area could account for the adaptive trend towards the development of a larger head to enhance feeding activity. The progressive increase in the length of the body correlated with a decreasing head size would appear to be more closely related to a migration feeding strategy. This consideration is based on the findings of diet studies on
´
chub mackerel (Pajaro, 1993; Perrotta et al., 1999).
Results of both approaches along with water circulation data and previous biological information on S. japonicus suggest one plausible scenario with regard to chub mackerel stocks in Argentinian waters (Fig. 1). At this moment, only one spawning area has been detected, located from October to January off the Mar del Plata coast (coincident with the Mar del Plata fishing ground). Massive spawns in the area with four or five successive settings are associated with temperatures ranging from 16 to 188C (Perrotta and Christiansen, 1993). We propose that the larvae are transported near the coast in a northerly direction, where they develop into the early juveniles stages (age classes 0 and 1). The coastal current serves as an entrainment system for the young. As these young
´
´
feeding. The Rıo de la Plata area is abundant with juvenile stages throughout the year. These juveniles then recruit at the end of February to the adult stock caught in the Mar del Plata area during the fishing season (age classes 1 to 8; Perrotta, 1992).
´
Does the El Rincon area have an independent spawning population that utilizes the ´
southern currents for its life cycle? The San Matıas Gulf area (Fig. 1) is somewhat of an enigma. Only during November and December are chub mackerel detected in the northern area when the temperature ranges from 16 to 188C (Perrotta, unpublished data). The large size of the individuals suggests they are adults, but there is no information on their gonadal development. The existing evidence (especially environmental factors)
´ ´
suggests that San Matıas Gulf is not independent. A connection with the El Rincon area ´
is highly likely if we consider that adults living in the El Rincon area start gonadal development in August (Perrotta and Forciniti, 1994). Thus, the area may be occupied
´ ´
by individuals from El Rincon. Further investigations, especially in the San Matıas Gulf or based on a complete adult tagging program, would answer this question.
The absence of genetic data from the Mar del Plata spawning area restricts further genetic details, however the results endorse the present policy of managing northern and southern stocks of S. japonicus as two separate units. Since 1996, two fishing stocks of chub mackerel have been designated based on morphometric characteristics, Mar del
´
Plata and El Rincon (north and south of latitude 398009S) (Fig. 1). A two-stock hypothesis provides a more conservative approach to harvest management since it focuses attention on the maintenance of local population levels in the short term and on the preservation of local adaptations in the long term.
These fishing stocks need to be further investigated in order to be elevated to the status of genetic stocks (i.e., completely isolated reproductive populations of the same
´
species). Sampling of additional localities (Mar del Plata and San Matıas Gulf) is required to more firmly resolve the questions raised by this study. Meanwhile, the present data provide a necessary foundation for determining the population structure of chub mackerel in the South West Atlantic.
5. Conclusions
1. The systematic status of chub mackerel in the South West Atlantic is at the specific level of Scomber japonicus, not a subspecific level.
2. Genetic and morphologic results endorse the present policy of managing northern and southern stocks (north and south of latitude 398009S) of S. japonicus as two separate units.
Acknowledgements
We thank Anibal Aubone (INIDEP) for supplying AMDIS and AMACP programs
´ ´ ´
and Fred Utter, Emili Garcıa-Berthou and Jose L. Garcıa-Marın for useful comments on the manuscript. This work was supported by a research grant from INIDEP (Proyecto
´
References
Aebersold, P.B., Winans, G.A., Teel, D.J., Milner, G.B., Utter, F.M., 1987. Manual for starch gel electrophoresis: a method for the detection of genetic variation. NOAA Tech. Rep. NMFS 61, 1–19. Allendorf, F.W., Mitchel, N., Ryman, N., Sthal, G., 1977. Isozyme loci in brown trout (Salmo trutta L.):
detection and interpretation from population data. Hereditas 86, 179–190. ´
Bouroche, J.M., Saporta, G., 1983. L’analyse des donnees. Presses Universitaires de France, Que sais je? No. 1854, pp. 127.
Cavalli-Sforza, F.L.L., Edwards, A.W.F., 1967. Phylogenetic analysis: models and estimation procedures. Evolution 32, 550–570.
Chakraborty, R., Fuerst, P.A., Nei, M., 1980. Statistical studies on protein polymorphism in natural populations. III. Distribution of allele frequencies and the number of alleles per locus. Genetics 94, 1039–1063.
´ ´
Cousseau, M.B., Cotrina, C.P., 1980. Observaciones sobre diferencias morfometricas entre la merluza comun (Merluccius hubbsi ) y la Merluza austral (Merluccius polylepis). Rev. Inv. Des. Pesq. 2, 47–56. FAO, 1997. Fishery Statistics. http: / / www.fao.org / fi / statist.
´ ´
Grant, S., Garcıa-Marın, J.L., Utter, F., 1999. Defining population boundaries for fishery management. In: Mustafa, S. (Ed.), Genetics in Sustainable Fisheries Management. Fishing News Books. Blackwell Science, Oxford, pp. 27–72.
Hedgecock, D., 1994. Does variance in reproductive success limit effective population sizes of marine organisms. In: Beaumont, A.R. (Ed.), Genetics and Evolution of Aquatic Organisms. Chapman & Hall, London, pp. 123–134.
Jamieson, A., Smith, P., 1987. Atlantic mackerel (Scomber scombrus L.) stocks and genes: a review. J. Cons. Int. Explor. Mer. 44, 66–72.
Johnson, A.G., Fable, W.A., Grimes, C.B., Trent, L., Vasconcelos Perez, J., 1994. Evidence for distinct stocks of king mackerel, Scomberomorus cavalla, in the Gulf of Mexico. Fish. Bull. 92, 91–101.
Jorde, P.E., Gitt, A., Ryman, N., 1991. New biochemical genetic markers in the brown trout (Salmo trutta L.). J. Fish Biol. 39, 451–454.
´ ´
Lopez, R.B., 1959. La caballa del Mar Argentino. I. Sistematica, distribucion y pesca. Mus. Arg. Cienc. Nat. ´
‘B. Rivadavia’, Ciencias Zoologicas 3 (3), 95–130.
Nei, M., 1972. Genetic distance between populations. Am. Nat. 106, 283–292.
Nei, M., 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
´ ´ ´ ´
Pajaro, M., 1993. Consideraciones sobre la alimentacion de la caballa con especial enfasis en la depredacion de ´
huevos y larvas de peces. In: Perrotta, R.G. (Ed.). Estudio Biologico y Pesquero de la Caballa (Scomber japonicus Houttuyn, 1782), Vol. Doc. Cient. 2. INIDEP, pp. 19–29.
Pasteur, N., Pasteur, G., Bonhomme, F., Catalan, J., Britton-Davidian, J., 1988. Practical Isozyme Genetics. Ellis Horwood, Chichester, pp. 212.
Perrotta, R.G., 1992. Growth of mackerel (Scomber japonicus Houttuyn, 1782) from the Buenos Aires–North Patagonian region (Argentine Sea). Scientia Marina 56 (1), 7–16.
´ ´
Perrotta, R.G., 1993. Comparacion mediante el empleo de los caracteres merısticos y el crecimiento de ˜
´ ´
caballas originarias de varias regiones geograficas (Cataluna, Islas Canarias y Sudamerica). In: Perrotta, ´
R.G. (Ed.). Estudio Biologico y Pesquero de la Caballa (Scomber japonicus Houttuyn, 1782), Vol. Doc. Cient. 2. INIDEP, pp. 7–17.
´
Perrotta, R.G., Aubone, A., 1991. De nuevo sobre la morfometrıa de la caballa (Scomber japonicus). Frente ´
Marıtimo 8 (Sec. A), 37–41.
´
Perrotta, R.G., Christiansen, H.E., 1993. Estimacion de la frecuencia reproductiva y algunas consideraciones ´
acerca de la pesquerıa de caballa (Scomber japonicus). Physis 49, 1–14.
Perrotta, R.G., Forciniti, L., 1994. Un estudio preliminar del crecimiento de la caballa (Scomber japonicus) en
´ ´ ´
dos areas de su distribucion. Frente Marıtimo 15, 101–109.
´ ´
Perrotta, R.G., Pertierra, J.P., 1993. Sobre la dinamica poblacional de la caballa en la Pesquerıa de Mar del
´ ´
´ ´ ´ Perrotta, R., Aubone, A., Sanchez, F., 1990. Estudio comparado de los caracteres morfometricos y merısticos
´ de la caballa (Scomber japonicus Houttuyn, 1782) (Teleostei: Scombridae) del sur de Brasil y del area marplatense (Mar Argentino). Scientia Marina 54 (1), 47–53.
´ ´
Perrotta, R.G., Pajaro, M., Scarlato, N., 1997. Muestreo bioestadıstico de pescado en el puerto de Mar del ´
Plata. Caballa (Scomber japonicus). Perıodo 1986–1991. INIDEP Inf. Tec. 15, 25–51. ˜
Perrotta, R.G., Madirolas, A., Vinas, M.D., 1998a. Aggregation patterns of mackerel (Scomber japonicus) school in relation to the environmental conditions for two different fishing areas off the argentine coast. ICES CM 1998 / J:36.
˜ ´
Perrotta, R.G., Pertierra, J.P., Vinas, M.D., Macchi, G., Tringali, L., 1998b. Una aplicacion de los estudios ´
ambientales para orientar la pesquerıa de la caballa (Scomber japonicus) en Mar del Plata. INIDEP Inf. Tec. 23, pp. 24.
˜ ´ ´
Perrotta, R.G., Madirolas, A., Vinas, M.D., Akselman, R., Guerrero, R., Sanchez, F., Lopez, F., Castro ´ Machado, F., Macchi, G., 1999. La caballa (Scomber japonicus) y las condiciones ambientales en el area
´
bonaerense de El Rincon (30–40309S). Agosto, INIDEP Inf. Tec. 26, 1996, pp. 29. Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43, 223–225.
´
Roby, D., Lamber, J.D., Sevigny, J.M., 1991. Morphometric and electrophoretic approaches to discrimination of capellin (Mallotus villosus) populations in the estuary and Gulf of St. Lawrence. Can. J. Aquat. Sci. 48, 2040–2050.
Shaklee, J.B., Allendorf, F.W., Morizot, D.C., Whitt, G.S., 1990. Gene nomenclature for protein-coding loci in fish. Trans. Am. Fish. Soc. 119, 2–15.
Terry, D.B., Withler, R.E., Murray, C.B., Barner, L.W., 1988. Variation in body size, morphology, egg size, and biochemical genetics of pink salmon in British Columbia. Trans. Am. Fish. Soc. 117 (2), 109–126. Utter, F., Aebersold, P., Winans, G., 1987. Interpreting genetic variation detected by electrophoresis. In:
Ryman, N., Utter, F.M. (Eds.), Population Genetics and Fishery Management. University of Washington Press, Seattle, pp. 21–45.
Verspoor, E., Jordan, W.C., 1989. Genetic variation at the Me-2 locus in the Atlantic salmon within and between rivers: evidence of its selective maintenance. J. Fish Biol. 35, 205–213.
