Growth stanzas or abrupt changes in growth rates are present throughout the life span of fish. Identifying growth stanzas will help to adequately described growth taking into account that fishes are indeterminate growers. In this study, we used length-weight (L-W) relationships to analyze the growth stanzas in the Grouper-Snapper complex of Southern Gulf of Mexico. For this, the type of sexuality, sex and different sexual maturity phase were considered in the analyses of three species of gonochoric Snappers (Lutjanidae) and six species of protogynous hermaphrodite Groupers (Epinephelidae). Welch ANOVA tests were carried out to determine the existence of differences in length and weight between juveniles and adults per sex. According to the observed differences, L-W relationship parameters (a and b), standard error (SE b) and coefficients of determination (R2) were calculated for all species separately by sex and sexual maturity phase. Snappers’ juvenile-females b-value ranged from 2.44-2.77, juvenile-males from 2.16-2.94, adult-females from 2.63-2.80 and adult-males from 2.63-2.98. Groupers’ b-value ranged for juvenile-females 2.66-3.20, adult-females from 2.73-3.31 and for adult-males 2.93-3.29. For each relationship b-value was t-tested (t-Student) to explore differences from the allometric coefficient (b=3), which indicated changes in body form. Hypothesis test, for regression slopes (b) between Snappers’ juvenile-females vs. adult-females and juvenile-males vs. adult-males and Groupers’ juvenile-females vs. adult-females and adult-females vs. adult-males, indicated different growth stanzas related to gonadal development for Snappers, and to gonadal development and sex change in Groupers. The identification of growth stanzas is crucial to avoid an overestimation or misleading growth rate which is used in fisheries management to establish some target reference points, such as maximum sustainable yield or yield-per-recruit.
Distintos estados o estanzas de crecimiento descritos por cambios en el ritmo de crecimiento, se pueden observar en peces a lo largo de su vida ya que presentan crecimiento indeterminado. A través del análisis de relaciones longitud-peso (L-P), se identificaron distintas estanzas de crecimiento considerando el tipo de sexualidad, sexo y madurez sexual de individuos de tres especies de pargos (Lutjanidae) gonocóricos y seis de meros (Epinephelidae) hermafroditas protóginos. Pruebas independientes de ANOVA de Welch se aplicaron para conocer si existían diferencias estadísticas significativas en la media de la longitud y peso de juveniles, adultos, hembras y machos de pargos y en juveniles hembras, hembras y machos de meros. De acuerdo a las diferencias observadas, se procedió al cálculo de la relación L-P, parámetros a y b, error estándar (SE b) y coeficiente de determinación (R2) por separado (juveniles, adultos, hembras y machos) para cada especie. Los valores del parámetro b para todas las especies se encontraron dentro del rango esperado de 2.5 a 3.5 para pendientes de la relación L-P en peces. Los pargos tuvieron valores de b: juveniles de hembras de 2.44-2.77, juveniles de machos 2.16-2.94, hembras adultas 2.63-2.80 y machos adultos 2.63-2.98. Los meros tuvieron un valor de b para juveniles de hembras: 2.66-3.20, adultos hembras: 2.73-3.31 y adultos de machos: 2.93-3.29. Para cada relación, el valor de b fue probado a través de una prueba de t-Student para explorar diferencias significativas del coeficiente alométrico (b=3), lo cual indicaría cambios en la forma del cuerpo de los individuos. Finalmente pruebas de hipótesis sobre las diferencias entre pendientes obtenidas de las relaciones L-P mostraron distintas estanzas de crecimiento relacionadas en pargos con el desarrollo gonadal y en meros con el desarrollo gonadal pero también con el cambio de sexo. A través de este estudio se pudo observar la existencia de distintas estanzas de crecimiento en especies de alta importancia comercial para el Sur del Golfo de México. Por lo tanto se recomienda la obtención de las relaciones L-P por separado según el sexo y desarrollo gonadal de cada especie, para evitar una sobre estimación o un cálculo erróneo de la tasa de crecimiento poblacional la cual se utiliza en manejo de las pesquerías para determinar algunos puntos de referencia como el criterio de máximo rendimiento sostenible o bien el criterio de rendimiento por recluta.
Palabras clave: estanzas de crecimiento, relaciones longitud-peso, complejo mero-pargo, Golfo de México. ]]>
Length-weight (L-W) relationships are used to assess biomass of fish populations (Keller, & Kerstetter, 2013), as indicators of fish condition (Dubey et al., 2012), to compare life histories of certain species among regions (Pauly, 1993) or to allow the conversion of growth-in-length equations ]]>
The status of most reef fish stocks is unknown in the Southeastern United States and Mexico. Reef fishes must be conservatively managed because their communities comprise slow-growing and late maturing fish such as Groupers and Snappers ]]>
Lutjanus campechanus (Poey 1860), Lutjanus synagris (Linnaeus 1758) and Ocyurus chrysurus (Bloch 1791) whereas the other six species from the Epinephelidae family (Groupers), are protogynous hermaphrodites: Epinephelus morio ]]>
Epinephelus guttatus (Linnaeus 1758), Mycteroperca bonaci (Poey 1860), Mycteroperca microlepis (Goode and Bean 1880), Mycteroperca tigris (Valenciennes 1833) and Mycteroperca venenosa (Linnaeus 1758). Worldwide, E. morio, M. bonaci ]]>
and M. venenosa populations are considered as nearly threatened (IUCN, 2013), E. guttatus, M. microlepis, M. tigris as vulnerable with declining populations (Morris, Callum, & Hawkins, 2000) and L. campechanus as overfished in recovery (NOAA, 2011). For Southern Gulf of Mexico, E. morio populations are considered overexploited (Burgos, ]]>
Few growth studies take into consideration the presence of growth stanzas to calculate L-W relationships, which may lead to a growth rate overestimation if juveniles are not separated from adults or to a misleading growth rate ]]>
Methods and Materials
Collection site and field sampling: Specimens were collected on the Yucatan Peninsula continental shelf from 1999 to 2009, through monthly catches on a yearly basis, through a tropical sequential fishery by the artisanal (using hook and line) and technified fishing fleets (using automated long lines). Groupers were measured for total (TL cm) and standard length (SL cm) except for
E. guttatus (only TL) and weighed for total (TW g) and gutted weight (GW g). Due to their fork tail, Snappers were measured for total (TL cm), standard (SL cm) and fork length (FL cm) except for L. campechanus (only TL and SL), and weighed for total (TW g) and gutted weight (GW g). For all species fresh gonad weight (gW g) was recorded and gonadosomatic index (IG=100x[gW/GW]) was calculated. ]]>
Gonadal analysis: Type of sexuality, sex and gonadal developmental phase were determined for each specimen by microscopic examination of gonadal structure. Hermaphroditism was defined following the criteria established by Sadovy and Shapiro (1987) and Sadovy de Mitcheson and Liu (2008), and sex and gonad developmental stage following Brown-Peterson, Wyanski, Saborido-Rey, Macewicz & Lowerre-Barbieri (2011).
Groupers analyzed in this study, are protogynic hermaphrodites (specimens undergo a sexual transition from a functional female to a functional male) (Shapiro, 1987) therefore, no juvenile-males were registered while Snappers are gonochoric species with female and males-juveniles. Considering group sample variances were unequal, Welch (Welch, 1951) ANOVA (means are weighted by the reciprocal of the group mean variances) independent ]]>
Following the procedure established by Ricker (1973) with the proposed modifications by Froese (2006), L-W relationships were calculated by sex and gonad developmental phase, for each species, using the equation W=aLb where W is total ]]>
b-value according to Carlander (1969) (as cited in Keller & Kerstetter, 2013) should fall between the expected range for b=2.5-3.5 in fishes. The b-value for each relationship was afterwards t-tested ]]>
t-Student) to explore significant statistically differences from the allometric coefficient b=3 (Cinco, 1982) using the equation t=(b-3)sb (Sokal, & Rohlf, 1995) where t is t-student value, b is the slope and sb is the slope standard error. According to Froese (2006) b-value indicates changes in body form or condition: If ]]>
=3 individuals in the sample have the same form as large specimens, if b>3 specimens increased in height or width more than in length and if b<3 specimens become more elongated. Finally, hypothesis tests of differences between regression line slopes (b-value) were performed according to Zar (1999) among gonochoric Snappers’ female-juveniles vs. female-adults and male-juveniles vs. male-adults and for protogynous hermaphrodites Groupers’ juvenile-females vs. adult-females and adult-females vs. ]]>
b-value between regression slopes in each species were considered as different growth stanzas. All statistical analyses were performed using MATLAB R2012b (The MathWorks, Inc.).
Results
]]>
A total of 12 114 specimens of nine different species were sampled: Lutjanus campechanus (N=914), Lutjanus synagris (N=1 022), Ocyurus chrysurus (N=1 431), Epinephelus guttatus (N=1 522), Epinephelus morio (N=2 328), Mycteroperca bonaci (N=739), ]]>
Mycteroperca microlepis (N=1 083), Mycteroperca tigris (N=519) and Mycteroperca venenosa (N=2 556). Gonochoric Snappers’ juvenile-females ranged in total length (TL) from 13.5-49.9cm, juvenile-males from 14.0-58.5cm, adult-females ranged form 18.5-61.6cm and adult-males form 17.7-81.6cm. Protogynous hermaphrodite Groupers’ juvenile-females ranged form 1.9 to 61.0cm, adult-females from 25.6-123.5cm and adult-males from 29.0-124.5cm (TL). Mean gonadosomatic index percent ]]>
L. campechanus females (max-min monthly mean values±SE: 1.02±8.80-0.20±0.09%) and males (0.24±0.40-0.09±0.03%) for L. synagris females (3.00±0.18-0.50±0.03%) and males (0.90±0.13-0.20±0.02%) and for O. chrysurus females (2.30±0.13-0.50±0.03%) and males (3.30±0.23-0.50±0.03%). For Groupers mean IG% varied for
E. guttatus females (max-min values±SE: 10.57±0.71%-0.12±0.01%) and males (0.95±0.04-0.10±0.01%), E. morio females (2.14±0.21-0.07±0.02%) and males (0.29±0.08-0.14±0.01%), M. bonaci females (2.2±0.27-0.6±0.01%) and males (0.22±0.03-0.11±0.03%), M. ]]>
females (3.40±0.23-0.40±0.03%) and males (0.36±0.11-0.06±0.01%), M. tigris females (3.47±0.31-0.15±0.02%) and males (1.36±0.14-0.10±0.01%) and M. venenosa females (8.70±0.55-0.15±0.03) and males (5.83±0.40-0.05±0.03%). For all species, IG% was higher in females than in males (except for O. ]]>
) even though females of all species tend to be smaller in size and weight.
Welch ANOVA tests showed significant statistical differences (p<0.05) for all Snappers and Groupers species in TL, FL, SL, TW and GW (Table 1) between sex ]]>
Table 2). Linear regressions were significant for all species (females/males, juveniles/adults) (p<0.05) and coefficients of determination ranged from 0.96-0.99 indicating a strong relationship between variables. Length-weight b-values ]]>
b. Snappers’ b-values varied from 2.3 to 2.7 for juvenile-females, from 2.1 to 2.9 for juvenile-males, from 2.6 to 2.8 for adult-females and from 2.6 to 2.9 for adult-males. For Groupers, b-values ranged from 2.6 to 3.2 for juvenile-females, from 2.7 to 3.3 for adult-females and from 2.9 to 3.2 for adult-males (Table 2).
The t-test (t-Student) to explore differences from the allometric coefficient b=3 acknowledge differences for Snappers: in juvenile-females for the three species (b<3), in adult-females only for L. campechanus ]]>
b<3), in juvenile-males for L. synagris and O. chrysurus (b<3) and in adult-males for the three species (b<3). Lutjanus campechanus juvenile-females and adult-females displayed the same b-value (b<3) showing that ]]>
b=3) change their uniform body shape to an elongated one as they reach sexual maturity (b<3). On the contrary, L. synagris and O. chrysurus displayed changes from an elongated body shape as juvenile-females (b<3), to a more uniform body shape (b=3) ]]>
b<3) as they grow and mature (Table 3). Differences from b=3 for Groupers were registered: in juvenile-females of E. morio (b>3), M. bonaci (b>3), M. ]]>
(b>3) and M. tigris(b<3), in adult-females for all species (b<3 or b>3) except for M. tigris (b=3) and in adult-males only for E. morio (b>3) and M. venenosa (b<3). ]]>
Epinephelus morio displayed the same body shape becoming gradually thicker with size (b>3). For E. guttatus juvenile-females’ uniformity in body shape (b=3) change to an elongated form as they reach adulthood (adult-females b<3) and then change back to a more uniform body shape as adult-males (b=3). ]]>
M. bonaci and M. microlepis juvenile-females (b>3) and adult-females (b>3) continuously increase in height or width more than in length, whereas through sex change, this tendency ceases and adult-males display a more uniform body shape (b=3). Mycteroperca tigris exhibits changes from an elongated form in juvenile-females (b<3) ]]>
b=3). Mycteroperca venenosa show a uniform body shape (b=3) in juvenile-females, changing to an elongated form in adult-females (b<3) that conserve as adult-males (b<3) (Table 3).
]]>
Hypothesis tests on differences between regression lines slopes were performed in order to observe possible growth stanzas. Growth stanzas were accounted for Snappers’ L. campechanus and L. synagris from juvenile-females to adult-females and for the three species (including O. chrysurus) from juvenile-males to adult-males. For Groupers growth stanzas could be identified in
E. morio, M. bonaci and M. microlepis from juvenile-females to adult-females and for E. guttatus, E. morio, M. microlepis and M. tigris from adult-females to adult-males (Table 4).
]]>
Discussion
Growth stanzas are characterized by some kind of crisis or discontinuity in development (Ricker, 1979) described by changes in growth rate. Since fishes are indeterminate growers, growth models should be carried out in many different levels of detail (Craig, 1984; Enberg, Dunlop, & Jørgensen, 2008) ]]>
]]>
The evident difference between juveniles and adults for both sexes in gonochoric Snappers showed that growth stanzas could be observed from the juvenile phase to adults (sexually mature) if L-W relationships are obtained separately. Differences between sexes (for adults only) could also be appreciated even though we did not perform a direct comparison between adults: L. synagris, L. campechanus and O. chrysurus adult-females were bigger and ]]>
Ocyurus chrysurus than in females (2.30±0.13-0.50±0.03%) suggesting that there is an important deviation of surplus energy canalized to reproduction in males. Reproductive investment reduces the energy necessary for somatic ]]>
For hermaphrodite Groupers, growth stanzas were only observed in E. morio, M. bonaci and M. microlepis ]]>
E. morio, M. bonaci and M. microlepis (from 1.9cm to 33.4cm) in comparison to juveniles of E. guttatus, M. tigris and M. venenosa (20.5cm to 61.0cm). Since Groupers have slow growth rate and late sexual maturity (Coleman et al., 1999) and juveniles where characterized based on their gonadal developmental ]]>
Groupers’ growth stanzas from adult-females to adult-males were observed in E. guttatus, E. morio, M. ]]>
and M. tigris. Gonadosomatic index for all species was up to three times higher in adult-females than in adult-males, which indicate that there is also, an important amount of energy directed to gonadal development in females. Munday, Hodges, Choat and Gus (2004) registered the existence of a sex-specific growth effect in other species of protogynic hermaphrodites, suggesting that females that become males grow faster than other females before the age of sex change. Only the largest female in a social group becomes male, suppressing sex change in subordinate females (Francis, 1992). Therefore different growth ]]>
M. bonaci and M. venenosa did not register differences in L-W relationship slopes between adult females vs. males, even though M. bonaci displayed changes in body shape. Since M. venenosa maintain the same uniform shape regardless of the sex change, no growth stanzas between adult-females and adult-males could be observed.
Growth stanzas could be registered for gonochoric Snappers mainly due to gonadal development and in hermaphrodite Groupers due to gonadal development and sex change. These results corroborate that a single regression will not adequately describe the length-weight relationship of a species. It must be considered that growth rate is not constant and may change either continuously or abruptly during the fish lifetime (Katsanevakis et al., ]]>
Acknowledgments
This study was ]]>
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1.Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Departamento de Recursos del Mar, Unidad Mérida. Ant. Carr. a Progreso Km. 6. A.P. 73, Cordemex, Mérida, Yucatán, C.P. 97310. México; ximenarenan@me.com, tbrule@mda.cinvestav.mx
2.Galen University, 62.5 Western Highway, San Ignacio, Cayo District Belize, C.A. Belize; snapsprov@yahoo.co.uk
3.Centro de Bachillerato Tecnológico, Industrial y de Servicio, Antigua carretera a Progreso Km 6 Col. Chuburna de Hidalgo C.P. 97200, Yucatán, México; chacmola@hotmail.com ]]>
Received 30-VI-2014. Corrected 18-IX-2014. Accepted 20-X-2014.
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