GROWTH AND MORTALITY OF LAGODON RHOMBOIDES (PISCES: ) IN A TROPICAL COASTAL LAGOON IN NORTHWESTERN YUCATAN, MEXICO CRECIMIENTO Y MORTALIDAD DE LAGODON RHOMBOIDES (PISCES: SPARIDAE) EN UNA LAGUNA TROPICAL COSTERA EN EL NOROESTE DE YUCATÁN, MÉXICO

José Luis Bonilla-Gómez1*, Jorge A. López-Rocha2, Maribel Badillo Alemán2, Juani Tzeek Tuz2 and Xavier Chiappa-Carrara2

ABSTRACT Growth and mortality were estimated for the Lagodon rhomboides pinfish inhabiting La Carbonera, a tropical coastal lagoon on the northwestern of the Yucatan Peninsula, Mexico. A total of 448 juvenile and adult individuals were collected monthly between April 2009 and May 2010. The length-weight relationship was calculated and the monthly variation in the condition factor was analyzed. Growth was estimated through the von Bertalanffy growth equation using a length frequency analysis. In addition, mortality was estimated and analyzed. Results showed that caught were between 2.1 and 20.0 cm long with an average length of 9.42 cm. The length-weight relationship showed isometric growth. The von Bertalanffy growth model parameters -1 were: L∞ = 21.0 cm, W∞ = 163.46 g, k = 1.1 year and t0 = - 0.158 years. Instantaneous mortality rates were 2.11 and 2.61 year-1 as estimated by the method used. According to the results, growth estimates of L. rhomboi- des along the northwestern coast of Yucatan are higher than those found in the population studied in Florida, suggesting a strong influence of environmental conditions in the growth pattern of this species. This study provides the first growth and mortality estimates forL. rhomboides in the Yucatan Peninsula, which is relevant for the proper implementation of conservation measures for this species.

Keywords: Lagodon rhomboides, von Bertalanffy, ELEFAN I, length-weight relationship, natural mortality.

RESUMEN Se realizaron estimaciones de crecimiento y mortalidad del pez Lagodon rhomboides que habita en la laguna costera tropical La Carbonera, al noroeste de la península de Yucatán, México. Se obtuvieron 448 individuos en estadios juveniles y adultos recolectados mensualmente de abril del 2009 a mayo del 2010. Se obtuvo la relación peso-longitud y se analizó la variación mensual del factor de condición. El crecimiento se estimó a través de la ecuación de crecimiento de von Bertalanffy mediante un análisis de frecuencias de longitudes. Adicionalmente se obtuvieron estimaciones de mortalidad. Los resultados mostraron que los peces capturados presentaron tallas entre 2.1 y 20.0 cm de longitud total con un promedio de 9.42 cm. La relación peso-longitud mostró un crecimiento de tipo isométrico. Los parámetros del modelo de crecimien- -1 to de von Bertalanffy fueron: L∞ = 21.0 cm, P∞ = 163.46 g, k = 1.1 año y t0 = - 0.158 años. Las tasas ins- tantáneas de mortalidad presentaron valores de 2.11 y 2.61 año-1 según el método de estimación utilizado.

1 Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México. Circuito exterior S/N, Ciudad Universitaria, México D. F., México. C. P. 04510. *[email protected] 2 Unidad Multidisciplinaria de Docencia e Investigación de Sisal (UMDI-Sisal, UNAM). Puerto de Abrigo s/n, Sisal, Hunucmá, Yucatán, México. C.P. 97356. [email protected], [email protected], la_biologa@ hotmail.com, [email protected]

Recibido 29-III-2011 Aceptado 17-VIII-2011

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De acuerdo con los resultados, las estimaciones de crecimiento de L. rhomboides de la costa noroeste de Yucatán son más altas que las encontradas para la población de Florida, lo que sugiere una alta influencia de las condiciones ambientales en el patrón de crecimiento de esta especie. En este estudio se proveen las primeras estimaciones de crecimiento y mortalidad para L. rhomboides en la península de Yucatán, lo que es relevante para la adecuada implementación de medidas de conservación de la especie.

Palabras claves: Lagodon rhomboides, von Bertalanffy, ELEFAN I, relación talla-peso, mortalidad natural.

INTRODUCTION coastal lagoons, especially in meadows of Thalassia testudinum, and roots Growth increases size and weight of (Adams et al. 2004). Pinfish is a dominant an organism, as well as its structure, which species in many Yucatan coastal lagoons leads to an increase in total size. Ecologi- (Vega-Cendejas, 2004) and, in spite of its cal studies on fish, particularly those re- numerical abundance, frequency and wide lated to growth, are useful in determin- distribution, the species is not fished in ing the functional role of this group in an northwestern Yucatan peninsula. ecosystem (Martínez-Porchas et al. 2009). The purpose of this study is to esti- Age, length and weight are necessary mate growth and mortality of L. rhom- variables in understanding the dynamics boides in La Carbonera coastal lagoon of a population and, just as environmental in northwestern Yucatan peninsula. This factors, they are key in understanding the lagoon has two distinct features: its shal- importance of a population in a particu- lowness, which is about 30 cm average, lar habitat (Shervette et al. 2007). Growth and the confluence of waters from oceanic of juvenile fish is considered one of the and underground sources. most important factors contributing to the The results presented in this paper future progression of adult populations constitute the first assessment of growth within a habitat (Beck et al. 2001). parameters of this species off the Yucatan Studies have analyzed growth and coast and may serve as a basis for the de- natural mortality of Lagodon rhomboides velopment and implementation of a region- on the Florida peninsula in the northeast- al conservation and management plan. ern Gulf of Mexico (Nelson, 1998; 2002). L. rhomboides, a member of the Spari- MATERIALS AND METHODS dae family, is known colloquially as pin- fish, pin perch and bream (Muncy, 1984; Study area: Sampling was conduct- Carpenter, 2002) and locally as “sargo” ed monthly between April 2009 and May and “xlavita” (Canto-Maza and Vega- 2010 in La Carbonera coastal lagoon, Cendejas, 2008). It is an estuarine depen- in the northwestern Yucatan peninsula, dent species with ecological, recreational Mexico (21°13’- 21° 14’ N; 89° 52’ - 89° and commercial importance (Robins et 54’ W) (Fig. 1). This lagoon is connected al. 1986). Pinfish inhabit coastal waters to the sea by a canal, or mouth, that was from Massachusetts to Florida and Ber- formed by Hurricane Gilbert which hit the muda, including the Gulf of Mexico, the Yucatan coast in 1988. The lagoon’s fresh Yucatan Peninsula and the northern part water comes from groundwater discharges of Cuba (Hoese and Moore, 1977). It is and rainfall. Due to differences in pre- commonly found in bays, estuaries and cipitation and temperature, this region has

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Fig. 1. Map of La Carbonera coastal lagoon with the sampling stations Fig. 1. Mapa de la laguna costera La Carbonera con las estaciones de muestreos three characteristic climatic seasons: dry between weight and total length was used (March-June), rainy (July-October) and to estimate growth through the power north winds (November-February) (Arceo- equation by Sparre and Venema (1995): Carranza and Vega-Cendejas, 2009). Tem- perature (ºC) and salinity were determined W=a Lt b (1). at each sampling station with a Yellow Springs Instrument (YSI), model 556 MPS. where W represents the weight (g), Lt Juvenile and adult organisms were is the total length (cm), parameter a is a caught with a 40 m long seine net, with constant and b is the slope of the model. 1 m deep and 1.27 cm (0.5 inch) stretch To determine parameters a and b in the mesh, in 9 sampling stations along the la- equation (1), a regression analysis and a goon during each field trip (see Fig.1). least square analysis were used. The es- Relationship between total length timated b parameter was evaluated with and weight: morphometric variables a t-student test to assess isometry in the were determined for each specimen: total length-weight relationship (Pauly, 1983). length (Lt ± 0.1 cm), measured from the Parameters of the von Bertalanffy tip of the upper jaw to the tip of the tail fin, growth function (VBGF) were determined and total weight (W ± 1.0 g). A relationship through the ELEFAN-I software included

Rev. Mar. Cost. ISSN 1659-455X. Vol. 3: 99-109, Diciembre 2011. 101 Bonilla, López, Badillo, Tzeek & Chiappa in the package FAO-ICLARM Stock As- The maximum longevity of individu- sessment Tools (FiSAT II) (Gayanilo et al. als (tmax) was calculated through Pauly´s 1997), using length frequency distribution equation (1983) defined as follows: with class intervals of 2 cm of total length. 3 The VBGF is expressed as follows: t = + t (6). max k 0 k (t t ) Lt = L (1 exp 0 ) (2). Total instantaneous mortality rate (Z) was determined by the length-converted where Lt is the length at age t, L∞ is asymp- totic length, K is the growth rate (year-1) catch curve (Pauly, 1983), which, in the ab- sence of exploitation in the area of study, is and t0 is the hypothetical age at which fish length is zero. equivalent to the instantaneous natural mor- In order to assess the variability of tality rate (M). Additionally, an independent k taking into account the uncertainty in estimate of M was obtained using the em- the estimation of asymptotic length, esti- pirical equation proposed by Pauly (1980): mated values of maximum length and its log M = 0.0066 0.279log L + 0.6543log k + 0.4634log ºC 95% confidence interval from the routine 10 10 10 10 (7). Maximum Length Estimate included in FiSAT II (Gayanilo et al. 1997) were used The relative condition factor of L. to obtain a range of possible values for k. rhomboides was analyzed through the rel-

The hypothetic age at which the fish ative condition index Kn (Le Cren, 1951), which allows to determine weight devia- length is zero (t0) was calculated sepa- rately using Pauly´s empirical formula tions (W) for a given size regarding the

(1979), defined as follows: expected weight (West) from the length- weight relationship of the species (equa- log10( t0 ) = 3.922 0.2752log10 L 1.038log10 k (3). tion 1). The index is expressed as follows: W Once parameters of growth in length K n = (8). were obtained, equation (1) was used to West obtain the VBGF by weight, expressed as follows: RESULTS

k(t t0 ) b W =W (1 exp ) (4). Average temperature was 28.6ºC (83.48 ºF) (ranging between 20.3 - 36.2ºC/68.54 - 97.16 ºF) and average where Wt is the weight at age t, W∞ is the asymptotic weight and b is the isometry salinity was 35.1 (ranging between 3.8 - coefficient. 52.7) during the sampling period. To compare different growth esti- Total length of the 448 organisms col- mates for this species, the growth index lected ranged from 2.1 to 20.0 cm and weight f’ proposed by Munro and Pauly (1983) ranged from 0.10 to 132.1 gr (Fig. 2). The es- was used: timated parameters of the length-weight rela- tionship were: a = 0.0153 and b = 3.05. Expo-

ø´= log10 k + 2log10 L (5). nent b was not statistically different from the isometric value (t = - 0.1279, P > 0.05) (Fig.3).

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Fig. 2. Temporal variation in the frequency of the total length of L. rhomboides in La Carbonera, Yucatan, Mexico Fig. 2. Variación temporal de la frecuencia de la longitud total de L. rhomboides en La Carbone- ra, Yucatán, México

Fig. 3. Total length-weight relationship of L. rhomboides in La Carbonera, Yucatan, Mexico Fig. 3. Relación peso y longitud de L. rhomboides en La Carbonera, Yucatán, México

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The VBGF parameters calculated 95% confidence interval). Instantaneous -1 were: L∞ = 21.0 cm, W∞ = 163.46, k = 1.1 natural mortality rate (M) was 2.11 year -1 year and t0 = - 0.158 years. The estimat- in relation to the average temperature of ed parameters were obtained using May the sampling period (28.6 ºC). of 2009 as starting sample and 4 cm as Significant differences of the relative starting length. The estimated maximum condition factor, related to observed and es- length was 22.57 cm (19.91 - 25.24 cm timated weight, were showed in the month- 95% confidence interval). The values of k ly values (ANOVA, F = 5.22, P < 0.001), ranged from 0.63 to 1.2 year-1. The maxi- where the highest value was September mum value of the score function (0.540) 2009 and the lowest March 2010 (Fig. 5). was estimated at k = 1.1 year-1. The estimated equations of the VBGF DISCUSSION for total length and weight were: Lt = 21.0 [1 - exp- 1.1 (t - 0.158)] and W = 163.46 [1 - exp- L. rhomboides is a euryhaline (John- 1.1 (t - 0.158)]3.05, respectively. son, 1978) and resident species inhabiting A new cohort was found during the the La Carbonera lagoon that has been north winds season (November to Feb- reported as hypersaline waters (Hellier, ruary), while the highest frequency of 1962; Vega-Cendejas and Hernández de adult sizes was observed in the dry season Santillana, 2004). Despite the environ- (March-June) (Fig. 4). mental variability of this region, La Car- The growth performance index (f') bonera coastal lagoon provides a favor- was 2.69, and the maximum longevity able habitat and breeding area due to its

(tmax) for L. rhomboides in the study areas shallow, sandy bottom and the presence of was estimated at 2.87 years. (Carpenter, 2002). The total instantaneous mortality rate Growth parameters for L. rhomboi- (Z) estimated by the length-converted des have not been previously reported for catch curve was 2.61 year-1 (1.36 - 3.86; coastal environments around the Yucatan

Fig. 4. Temporal variation of the growth curve based on total length frequency data computed in ELEFAN-I of L. rhomboides in La Carbonera, Yucatan, Mexico Fig. 4. Variación temporal de la curva de crecimiento basada en datos de frecuencias de longi- tudes totales computadas en ELEFAN-I para L. rhomboides en La Carbonera, Yucatán, México

104 Rev. Mar. Cost. ISSN 1659-455X. Vol. 3: 99-109, Diciembre 2011. Growth and mortality of Lagodon rhomboides

Fig.5. Monthly average of relative condition factor (± standard deviation) for L. rhomboides in La Carbonera, Yucatan, Mexico Fig. 5. Promedio mensual del factor de condición relativo (± desviación estándar) de L. rhomboi- des en La Carbonera, Yucatán, México

Peninsula, and few studies have been showing that this species has a proportional performed to estimate parameters with volume growth. This isometric growth has the von Bertalanffy growth function or been attributed to food availability, low length-weight relationship for this spe- density and productivity characterizing the cies in the Gulf of Mexico (table 1). In the study area, with productivity being in its northeastern Gulf of Mexico, VBGF pa- highest during the rainy season (Herrera, rameters obtained by Nelson (2002) were 1988). However, it is interesting to note -1 L∞ = 21.9 cm, k = 0.33year and t0 = - 0.10 that fish up to 5 cm long were recruited in years. The growth coefficient k estimated the study area during the dry season, pre- for the northern coast of Yucatan in this in- senting the highest values of temperature vestigation (k = 1.1 year-1) is significantly and salinity (Fig. 2 and 4). higher than the one estimated by Nelson These results support the view that L. (2002). According to Nelson (2002), only rhomboides could be reproducing at the end k showed a latitudinal difference in com- of the rainy season, around October. It has parison to this study. Nelson (2002) also been reported that during this season ma- reports that, while this species can live ture individuals migrate to (Muncy, up to 7 years (25.5 cm), most fish do not 1984; Darcy, 1985). Additionally, in Tampa reach this age, whereas the present study Bay, Florida, it has been reported that go- found a maximum longevity of 3 years. nads mature from October to December, In addition, the length-weight relation- which suggests spawning activity occurs ship exponent remains close to isometric, during these months (Nelson, 2002).

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After spawning, juveniles can reach mortality rate (Z = M) due to the absence a total length of 13.7 cm by the age of of fishing of this species in the study area one year (VBGF of this study), represent- (Table 1). The highest M values for the ing half of the time estimated by Nelson population of the northern Yucatan coast (1998) for the Florida population. Juve- compared to the population of Florida is nile of L. rhomboides of the northern Yu- consistent with the highest growth rate catan coast has a growth rate of 0.6 - 1.4 found in Yucatan, taking into account that cm month-1 during the first year, while in natural mortality increases in populations Florida the reported growth rate ranges with high growth rates. from 0.10 to 0.25 cm month-1 (Nelson, Differences in natural mortality can 1998), reaching the reproductive stage at be attributed to latitudinal dissimilarities two years when it has grown between 8 according to Bravo et al. (2009), who and 10 cm in size (Hansen, 1970; John- reported that variations of these param- son, 1978). The size reached by 50% of eters could be due to growth differences the population during maturity was esti- associated to species present at different mated at 13.2 cm (Hansen, 1970). The L. latitudes. Based on that research, environ- rhomboides population of the northern mental characteristics such as temperature Yucatan coast could reach the size at first and photoperiod, which are distinctive in maturity after the first year of life. each region, may vary seasonally and are The value of the growth index (f' = correlated with changes in the abundance 2.69) indicates a different growth pattern and quality of food, harvesting regimes to from the value reported by Nelson (2002). which they are subjected, and the meth- In the growth parameters provided by Nel- odology used to mark differences between son (2002) the estimated f' values ranged the study areas. between 2.17 and 2.21. This could be re- The information provided in this lated to the uncertainty associated with the study on the basic parameters of the growth rate (k) estimates obtained by the population dynamics of L. rhomboides length frequency analysis, or by variations represents fundamental knowledge of in the growth rates for populations inhab- the species to implement the measures iting different latitudes with particular and strategies for its conservation on the environmental and ecological conditions. northern coast of Yucatan. Pauly (1979) and Sparre et al. (1997) de- termine that the coefficient of variation of ACKNOWLEDGEMENTS f' should not exceed 4% for growth pat- terns to be considered statistically similar. This investigation was supported by This study presents the first estimates PAPIIT (IN207609) and FOMIX-Yucatan of mortality for L. rhomboides in the Yu- (103 229) research grants. We thank Al- catan Peninsula. Nelson (2002) reported fredo Torres Gallardo, Korynthia López, a total mortality rate (Z) between 0.88 Carmen Galindo, Joel Loera, and all the and 1.08 year-1, these values being lower members of La Carbonera project team than those estimated in this study (2.11 for their technical support during research. - 2.61 year-1). Estimates of total mortal- We also want to express our gratitude ity by the length-converted catch curve to Chelsea Combest-Friedman and the (Pauly, 1983) are equivalent to the natural anonymous reviewers whose comments

106 Rev. Mar. Cost. ISSN 1659-455X. Vol. 3: 99-109, Diciembre 2011. Growth and mortality of Lagodon rhomboides = hypothetic 0 t Texas** Locality adjacent waters. adjacent waters. Campeche Bay** Campeche Bay** Tampa Bay, Florida. Bay, Tampa Florida. Bay, Tampa Florida. Bay, Tampa Southern of Florida** La Yucatan. Carbonera, Tampa Bay, Florida and Bay, Tampa Florida and Bay, Tampa = growth constant, (cm) k Length 20.3 LS 20.3 LS 15-22 LF 14-23 LF 13-20 LF 9.2-17.3LS 2.1-20.1 LT 6.6-25.5 LS 11.2-24.5 LS 11.2-24.5 M 0.78 (/year) 2.11/2.61* = asymptotic length, = asymptotic ∞ en el Golfo de México L Z 1.08 0.88 0.88 (/year) 0 t in the Gulf of Mexico -1.10 -1.21 -1.16 L. rhomboides (year) -0.158 k 1.1 0.33 0.31 0.33 (/year) L. rhomboides = natural mortality, LT= total length, LS= standard length, LF= furcal length, m= males, length, LF= furcal length, LS= standard length, total LT= mortality, = natural ∞ M L (cm) 21.00 21.99 22.85 21.20 b 3.11 3.11 3.05 3.03 2.90 3.09 3.24 3.25 = total mortality, = total Z a 0.0153 0.0027 0.0450 0.0430 0.0444 0.0123 0.0059 0.0103 n 12 448 645 285 330 343 302 140 100 1988 1974 (f) 1974 (m) Reference (fall-winter) Present work Nelson, 2002 Nelson, 2002 Nelson, 2002 Arteaga, 1994. Claro & García- Nelson, 2002 (f) (spring-summer) Nelson, 2002(m) Olaechea & Sauskan, Olaechea & Sauskan, Bohnsack and Harper, Bohnsack and Harper, Table 1. Growth parameters and mortality registered in Table Cuadro 1. Parámetros de crecimiento y mortalidad registrados en of allometry, of the model, b= slope or parameter of the sample, a = parameter n= total age at which the fish length is zero, f= females 1983). *First value according to equation of Pauly (1980) and second catch curve (Pauly, **Data from Fish Base (www.fishbase.org)

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