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Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 10:357–367, 2018 © 2018 The Authors. ISSN: 1942-5120 online DOI: 10.1002/mcf2.10026

ARTICLE

Geographic Variation in the Reproductive Ecology of the Panamic Grunt in the Southeastern Gulf of California Raul E. Lara-Mendoza Pesquera–Ciudad del Carmen, Instituto Nacional de Pesca, Centro Regional de Investigacion Avenida Héroes del 21 de Abril, Número 26, Ciudad del Carmen, Campeche 24100, México

Felipe Amezcua* Instituto de Ciencias del Mar y Limnologıa, Universidad Nacional Autónoma de México, Avenida Joel Montes Camarena s/n, Mazatlán, Sinaloa 82040, México

Abstract Biological parameters pertaining to the reproductive ecology of the Panamic Grunt Pomadasys panamensis were investigated in 788 individuals sampled from the southeastern Gulf of California between November 2009 and October 2010. Length frequency distributions and mean TLs differed between sampling areas, with organisms from the coastal population exhibiting two clear modes that included most of the organisms (mostly adults; mean TL = 25.7 cm), while the open-sea population appeared to consist of several cohorts (mean TL = 19.5 cm). Significant differences were recorded in spawning activity, gonadosomatic index (GSI), gonad weight, and size at maturity between fish from the coastal area and specimens from the open sea. The highest gonad weights and GSI values were recorded in the coastal zone during spring, coinciding with a peak in the number of mature females. In the open sea, the mature individuals were reproductively inactive throughout most of the yearlong study period, as individuals in late maturity stages represented a small portion of the sample. Female TL at 50% maturity (i.e., L50) was significantly lower in the coastal zone than in the open sea. The results suggest a differential use of available habitats by Panamic Grunts and highlight a need to consider temporal and geographic differences in reproductive ecology when formulating an adequate management program for this species.

Understanding the processes responsible for variability in population dynamics presents one of the major challenges in ecology. High-fecundity species, such as many fish, commonly exhibit variability in population structure, and variation may have significant implications for reproductive potential (Einum et al. 2003)—that is, the capacity of a fish population to yield successful recruits to the adult

population or fishery (Marshall et al. 1999). Geographic and temporal variation in reproductive features, such as TL at maturity, spawning strategy, and gonad weight, may be the result of biotic and abiotic factors (Fowler et al. 2000), which consequently have the capacity to influence reproductive potential (Marshall et al. 1998) and thus the growth and abundance of a population in the long

Subject editor: Anthony Overton, Alabama A&M University, Normal *Corresponding author: [email protected] Received January 13, 2017; accepted February 27, 2018 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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term. High rates of mortality can alter the life cycle and life history traits and therefore the reproductive characteristics of populations (Worden et al. 2010; Botsford et al. 2011; Rouyer et al. 2011). If the removal of individuals from a population occurs over a long period of time, the demographic changes can be substantial and carry important ecological implications, such as diminished reproductive potential (Birkeland and Dayton 2005; Berkeley et al. 2012), changes in stock productivity (Conover and Munch 2002; Hsieh et al. 2006; Anderson et al. 2008; Stenseth and Rouyer 2008), and long-term changes in life history traits (Jørgensen et al. 2007). Specifically, intensive commercial fishing is one factor with the potential to critically affect fish stock biomass and productivity (Christensen et al. 2003); thus, an understanding of these effects is important for fisheries management and conservation. In populations where fishing mortality increases with size, early maturation may help to ensure future egg production and population stability as well as potentially extending reproductive life (Wootton 1993). On the other hand, early maturation may compromise growth, resulting in smaller individuals that are more vulnerable to predation (Rochet 1998). It is necessary to estimate size at maturity together with the body length structure of a population to identify the individuals that are involved in egg production (Anastasopoulou et al. 2006). This information is also useful in setting and refining size restrictions by fisheries managers and, along with mean body size, is an important predictor of exploitation risk (Reynolds et al. 2005). The Panamic Grunt Pomadasys panamensis is an abundant and commercially important species distributed along the tropical eastern Pacific from southern California to Peru (Allen and Robertson 1994) and is heavily exploited in the southeastern Gulf of California (SGC; Amezcua et al. 2006; Madrid-Vera et al. 2007; Rodrıguez-Preciado et al. 2012). According to the National Commission for Fisheries and Aquaculture of Mexico (CONAPESCA), reported landings of the Panamic Grunt in the SGC constitute approximately 32% of the total catch in the Mexican Pacific. This species is usually caught with gill nets and trawl nets (Amezcua 1996) and is regularly found as bycatch in the SGC shrimp fishery, representing 6.3% of the total biomass and 3.7% of the total abundance of demersal fish caught by the shrimp trawlers (Madrid-Vera et al. 2007; Rodrıguez-Preciado et al. 2012, 2014). Fishery regulation for this species is nonexistent in the Mexican Pacific, and information on population ecology, demographic parameters, and gonad investment that could form the basis for species management is lacking. The potential for changes in Panamic Grunt reproductive biology that might cause temporal and geographic variations in reproductive output has not been previously investigated.

Furthermore, the effects of various fisheries on Panamic Grunt population dynamics have not been quantified. Gonad investment of other grunt species in tropical and subtropical areas varies seasonally, peaking during spawning periods (Falahatimarvast et al. 2012; Marcelle et al. 2013). Factors thought to influence reproductive investment in fish generally include the duration of the spawning period (Brown-Peterson et al. 2001) and size at maturity (Charnov and Berrigan 1991; Wootton 1993), both of which may vary among populations of a species. Longer spawning periods are expected to yield more batches of spawned eggs (Bani and Moltschaniwskyj 2008), and there is a positive correlation between fecundity and fish length (Ferriz et al. 2007) whereby larger fishes with higher gonad volume make a larger contribution to overall egg production than their smaller counterparts. However, if large fish are experiencing high fishing mortality, then individuals that delay maturation may never have the opportunity to spawn (Rochet 2000). We sought to examine geographic variability in the reproduction of Panamic Grunts, with the aim of informing future fisheries management. The specific objectives of this work were to (1) identify differences in spawning period duration and size at maturity between fish in coastal and open-sea zones by using histological assessment of female reproductive condition (gonadal stage) and (2) identify which sections of the population are being extracted by local fisheries and how fishery operations may affect the egg production overall.

METHODS Study site.— Panamic Grunt samples were collected from coastal and open-sea zones along the coast of Sinaloa state and northern Nayarit state in Mexico (Figure 1). The coastal area extended from the shoreline out to a depth of 10 m. Monthly samples were collected between November 2009 and October 2010 from the landings of small-scale fisheries operating at fishing villages in the central and southern parts of Sinaloa. All specimens were captured from fishing skiffs using gill nets with mesh sizes of 6.25, 7.50, and 8.75 cm and a total net length of 300 m. Sampled specimens were stored on ice and transported to the laboratory, where they were frozen for later analyses. The open-sea population was sampled during routine demersal surveys undertaken by the Mexican National Fisheries Institute as part of its annual assessment of shrimp populations during February, March, May–July, October, and November 2010. Fifty-two stations were sampled monthly off the coast of Sinaloa and northern Nayarit over a period of 2 weeks onboard two commercial vessels using a stratified survey design by depth and area with fixed sampling positions. The boats were fitted with two commercial trawls having a 30-mm

REPRODUCTIVE ECOLOGY OF PANAMIC GRUNTS

liner in the cod end and an average door spread of 34.9 m. The trawls were towed at 4.26 km/h (2.3 knots) for 1 h, covering a trawling area of 14 ± 1.4 ha (mean ± SD). These vessels operated at depths of 10– 64 m. A subsample of fish was obtained after every fishing haul and was stored frozen until transportation to the laboratory. In the laboratory, all organisms were measured (TL; cm) and weighed (nearest g). Each Panamic Grunt was dissected and classified as male, female, or undetermined. Both gonad lobules were removed from female specimens and weighed (nearest g). The middle section of the right gonad lobule (deemed most suitable for determination of reproductive status by Samoilys and Roelofs 2000) was sectioned and fixed for histological analysis by immersion n et al. 2009). in Davidson’s solution (Pi~ no Analysis of total length.— Because two types of fishing gear were used in each zone (gill net for the coastal zone; trawl net for the open sea), we used length frequency histograms to compare the distribution of fish between the two zones, and we used a one-way ANOVA to compare the TLs in each zone. Homoscedasticity of variances was tested by using Cochran’s C-test, with zone as the factor. These analyses were performed to determine whether sample mean length differed because of gear type or differential use of habitat by Panamic Grunts. Additionally, to determine geographic differences in the length distribution of Panamic Grunts, a one-way ANOVA was conducted using zone (coastal or open sea) as a factor; homoscedasticity of variances was tested with Cochran’s C-test, and frequency polygons were plotted as separate normal distributions for TL in each zone. Histological description of maturity stages.— Sex ratios were calculated for comparison between sampling areas by using a chi-square goodness-of-fit test with continuity correction (Zar 1999) to detect any deviation of the female : male ratio from the expected 1:1. Based on the assumption that the maturation of male and female specimens is synchronous (King 1995), ovaries alone were used for histological analysis. Female gonads provide information regarding reproductive condition similar to the information provided by the examination of testes and offer additional insights into fecundity and spawning time. Gonad sections were processed, embedded in paraffin wax, mounted, and stained for examination by using the same n et al. (2009). Gonad morprocedure described by Pi~ no phology was examined from microphotographs taken with a Zeiss Stemi 2000 stereomicroscope fitted with an AxioCam ERc 5s digital camera under 4–40× magnification. Each slide was divided with a graticule into quadrats of 5 × 5 μm (25 μm2), and 50 random quadrats were observed from each slide for each specimen. Oocytes were assigned a developmental phase based on the terminology

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FIGURE 1. Study area indicating the Gulf of California fishing grounds where data were obtained from the small-scale fishery in the coastal zone (closed circles) and the sampling stations where the shrimp trawlers operated (open circles).

utilized by Palaz on-Fernández (2007) for the related White Grunt Haemulon plumierii and by Brown-Peterson et al. (2011), and the number of oocytes at each stage in each quadrat was recorded. Mean abundances and the number of oocytes at each developmental stage per 25 mm2 were then calculated. To estimate the relative abundance of oocyte development stages for each gonad, the mean number of oocytes for a given stage was divided by the mean total number of oocytes observed in each quadrat, and the resulting value was multiplied by 100. The gonadal stage of development present in the highest proportion was used to assign a gonadal stage to each sample (Saborido-Rey and Junquera 1998). Reproductive cycle.— The reproductive cycle of female Panamic Grunts was described by differentiating the relative frequency of oocyte maturity stages (and thus gonad development) for each month of the study. Combined with monthly variations in gonad weight and the gonadosomatic index (GSI = [gonad weight/gutted weight] × 100), these data were used to infer spawning season dates. The use of GSI and gonad weight provided a measure of gonad condition independent of body size. To determine differences in gonad weight and GSI between sampling zones, two-way ANOVAs were undertaken with zone and sex as factors and with gonad weight and GSI as the dependent variables. Differences in gonad weight and GSI were only analyzed for mature fish (as indicated by gonadal stage). Homoscedasticity was tested with Cochran’s Ctest, and if differences were found, Tukey’s honestly significant difference test was performed. Sexual maturity.— Mean body length at 50% maturity (L50), defined as the TL at which at least 50% of all

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females are sexually mature, was estimated. A female was considered mature if histological investigation showed gonadal development to be at stage III or beyond (see Table 1). Fish were grouped into 1-cm class intervals, and a logistic model was created that described the proportion of mature females as a function of TL, h i Pmature ¼ 1= 1 þ eðrþL50 ×LÞ ; where P is the proportion of mature fish in length-class L; r is the width of the maturity curve; and L50 is body length at maturity. We estimated the model parameters by using a square difference function through Newton’s direct search algorithm in Microsoft Excel (Bonnans et al. 2006). Percentage values for maturity were then fitted to lengthclass for the females in each sampling zone (coastal area or open sea). An analysis of residual sums of squares was used to compare the maturity curves between zones and thus to determine whether the females from different zones varied in terms of length at maturity (Chen et al. 1992). A detailed explanation of this procedure was given by Haddon (2011).

RESULTS For the 788 specimens of Panamic Grunt analyzed, TL ranged from 9.2 to 38.0 cm (mean ± SD = 23.2 ± 5.5 cm). In the coastal zone, the sample comprised 385 females (range = 14.5–35 cm), 96 males (range = 17.0– 31.0 cm), and 3 individuals whose sex could not be determined (range = 17.0–20.0 cm). In the open sea, the sample contained 154 females (range = 12.6–38.0 cm), 108 males (range = 9.2–31.0 cm), and 42 individuals whose sex was undetermined (range = 9.0–24.0 cm). Analysis of Total Length In the open-sea shrimp trawl net, 219 fish species were collected, ranging from 1.1 cm to over 2.0 m TL (mean ± SD = 15.7 ± 8.5 cm). In the small-scale gill-net fishery within the coastal zone, 130 fish species were collected (mean ± SD = 15.2 ± 8.1 cm). The differences in fish size were statistically significant (F1, 24,338 = 17.407, P < 0.01), although the length frequency histograms of all species caught with both fishing gears were similar. There were statistical differences (F1, 786 = 338.43, P < 0.01) between the mean TLs of Panamic Grunts collected from the coastal area (mean ± SD = 25.7 ± 3.2 cm) and those captured from the open sea (mean ± SD = 19.5 ± 6.2 cm). The length frequency histogram shows that most of the individuals caught in the coastal area were over 21 cm. The plot for the open sea revealed a multimodal distribution, while for the coastal zone there were two

clear modes that contained the majority of the organisms (Figure 2). Definition of Gonadal Stages In both study areas, there were more females than males; therefore, the annual sex ratio diverged significantly from the expected 1:1. In the coastal area, the sex ratio was 1.00:0.25 (female : male; χ2obs = 172.44 > χ2table = 3.84), while the ratio for the open sea was 1.0:0.7 (χ2obs = 7.73 > χ2table = 3.84). The macroscopic and microscopic characteristics of oogenic stages in female Panamic Grunts are described in Table 1 and illustrated in Figure 3. All examined gonads contained oocytes in different stages, indicating an asynchronous development of the gonads. This can be observed in Figure 3, with the exception of Figure 3A, where all the oocytes are in the perinucleolar phase. The remaining panels depict oocytes of different phases in the same gonad: Figure 3B shows oocytes from phase I (chromatin nucleolus), phase II (perinucleolus), and phase III (secondary vitellogenesis); Figure 3C depicts oocytes from phase II and from phase IV (mature oocytes); and Figure 3D shows oocytes from phase III and from phase V (atretic oocytes). Gonad Development The proportion of females at different stages of maturity varied between sampling locations (Figure 4). Note that no samples were collected from the open sea during the months of January, April, August, and September; thus, information on the proportion of gonads at different stages of maturity in that zone is not available for those months. In the coastal zone, the Panamic Grunts exhibited a reproductive season starting in spring and extending until July; by August, a high proportion of gonads appeared spent (Figure 4A). Meanwhile, in the open sea, mature female gonads were observed during all seasons, with no clear reproductive peak. However, the majority of female gonads assigned to stage IV were present in June, July, and November, which may indicate either a long spawning season or multiple shorter spawning seasons in which individuals migrate to coastal areas to spawn (Figure 4B). Female gonad weight showed a significant dependence on the combination of location and season (F2, 381 = 3.28, P < 0.05). Coastal samples had the highest gonad weights during spring, with values declining and leveling off such that autumn and winter weights were similar. No significant seasonal changes in gonad weight were observed (Figure 5A). The patterns exhibited by the GSI values were similar to those observed for gonad weight, with significant seasonal differences (F3, 400 = 4.55, P < 0.05). In contrast, although GSI values from open-sea specimens also


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TABLE 1. Reproductive phases and macroscopic and microscopic characteristics of female Panamic Grunt gonads according to Saborido-Rey (2008) and Brown-Peterson et al. (2011).

Phase

Macroscopic characteristics

I. Immature (never spawned)

Ovaries are small, thin, and translucent structures, without evidence of previous spawning. Oocytes are not visible to the naked eye.

II. Regenerating (sexually mature, reproductively inactive)

Ovaries increase in size, occupying one-half of the body cavity, and are pale or light yellow in color, with few blood vessels present. Oocytes are beginning to be visible to naked eye.

III. Developing (ovaries beginning to develop, but not ready to spawn)

Ovaries are pale yellowish in color, occupying about three-fourths of the body cavity; blood vessels are visible on the dorsal side, and oocytes are clearly visible.

IV. Spawning capable (fish are developmentally and physiologically able to spawn in this cycle) V. Regressing (cessation of spawning)

Ovaries occupy the entire body cavity; they are orange-yellow in color, with many blood vessels. Oocytes are visible to the naked eye and can stick to your fingers. Ovaries are reduced in size, flaccid, and empty or with few yolked oocytes remaining. Color is dark reddish at the posterior portion. Ovaries occupy about one-half of the body cavity.

Microscopic characteristics (mean oocyte diameter ± SD) Chromatin nucleolus (CN) stage. Oogonia and oocytes are connected or close to ovigerous lamellae. This stage is characterized by a strongly basophilic cytoplasm with a nucleus occupying up to 60% of the cell. Concentrations of the perinuclear material are seen in the ooplasm at this stage. Mean oocyte diameter in the CN stage was 35.12 ± 9.37 μm. An increase in nucleolus is observed, which occurs peripherally, and the lampbrush chromosomes are visible in the perinucleolar (PN) stage. Oocytes in the PN stage had a mean diameter of 63.64 ± 14.8 μm. Previtellogenic oocytes with lipid vesicles appear. This substage is termed the cortical alveolar (CA) stage. The follicular epithelium surrounding the oocytes is fully formed. The mean diameter of oocytes in the CA stage was 86.32 ± 22.07 μm. Oocytes are found in three substages: primary vitellogenesis (PV), secondary vitellogenesis (SV), and tertiary vitellogenesis (TV). In the PV stage, the true yolk formation begins. The yolk forms and pushes the cortical alveoli to the margins. Mean oocyte diameter in the PV stage was 149.7 ± 30.55 μm. The SV stage is characterized by the presence of many yolk globules in the cytoplasm, which give rise to the yolk. Mean oocyte diameter in the SV stage was 250.94 ± 33.97 μm. The TV stage is characterized by fusion of the small yolk granules and an increase in oocyte diameter. Mean oocyte diameter in this stage was 285.76 ± 44.36 μm. This is the most advanced stage of vitellogenesis; the nucleus moves to the animal pole, and the nuclear membrane disintegrates. Mature eggs predominate with the completion of yolk fusion, and the oocytes increase further in size as a result of fluid uptake. Mean oocyte diameter was 308.95 ± 39.33 μm. Postovulatory stage; the lamellae appear collapsed and contain mostly resting oocytes. In this stage, the oocytes stop developing and degenerate, losing their structural integrity. The oocyte is invaded by phagocytic cells, and atresia stages are presented in many cells.

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FIGURE 2. Total length (cm) frequency distributions of Panamic Grunts captured at each study zone in the Gulf of California (dashed line = coastal area; solid line = open sea).

decreased from spring to winter, the changes were not statistically significant. The gonad weight and GSI were in agreement with the highest values recorded during spring prior to the spawning season for the coastal area. Sexual Maturity In the coastal zone, the smallest female with mature gonads had a body length of 15.0 cm, and the L50 was 21.5 cm (Figure 6). The logistic model for the coastal zone was as follows: h i Pmature ¼ 1= 1 þ eð0:597þ21:48×LÞ : In the open-sea zone, the smallest female with mature gonads was 19.0 cm, and the L50 was 25.4 cm. The logistic model for the open sea was h i Pmature ¼ 1= 1 þ eð0:311þ25:42×LÞ : These differences were statistically significant (F41, 44 = 12.68, P < 0.01), indicating that the females in the coastal zone matured at a shorter body length than those in the open sea. At 26.0 cm, over 90% of coastal females had attained sexual maturity, while in the open sea, the smallest length-class exhibiting 90% maturity was 32.0 cm.

DISCUSSION To our knowledge, this is the first study of reproductive ecology in the Panamic Grunt, and our results suggest that each fishery has a different effect on the species’ population. The small-scale fishers utilize gill-net gears, as their main target is the Pacific Sierra Scomberomorus sierra, and they

operate close to the coast. On the other hand, the industrial trawl fishery uses a bottom trawl to catch shrimp (Litopenaeus spp. and Farfantepenaeus spp.) in deeper waters (SAGARPA 2012). Although the fishing gears used by the two fisheries are very different, they captured fish of similar TLs, as shown by the length frequency distribution of all fish species captured with each gear. Statistical differences were found, however, indicating that the fish captured in the open sea were 5.0 cm larger than those captured in the coastal zone. The reason for this is beyond the scope of the present paper, but a number of factors may have contributed to this difference, such as variation in species composition between zones, differential habitat use by certain species, or the selectivity of each gear. Nevertheless, the mean TL of Panamic Grunts was higher in the coastal zone than in the open sea, although the mean TL of the suite of fish species in the coastal zone was on average smaller than the mean TL of fishes from the open sea. The observed differences in the length frequency distribution of Panamic Grunts between sampling areas were attributable to a differential spatial distribution of sizes rather than to gear type differences. The coastal population of Panamic Grunts consisted predominantly of larger and mature individuals, while most individuals analyzed from the open-sea samples were immature (according to the estimated length at first maturity), and the frequency distribution for TL in the open-sea zone was indicative of many cohorts. The sex ratios observed in both areas differed significantly from the expected ratio of 1:1, with females significantly outnumbering males. A similar pattern was previously observed for this species in shrimp trawl fishery bycatch from southern Sinaloa and northern Nayarit (Domınguez-L opez 1989), and the difference has been attributed to differential survival rates between females and males (Lucano Ramirez et al. 2001). However, it is necessary to consider other factors that influence differences between sex ratios, such as the behavior of the species during different stages of its life cycle. The examination of gonad tissues indicated five distinct phases of development (oogenesis) as well as an increase in the diameter of oocytes as they advanced to maturity. These phases were named and described according to Brown-Peterson et al. (2011), but with modifications based on the description made by Palaz on-Fernández (2007) for the related White Grunt. In this work, we designated the regenerating phase of Brown-Peterson et al. (2011) as phase II because this would better describe the monthly reproductive variation in the gonad phases. Additionally, as Brown-Peterson et al. (2011) pointed out in their conceptual model of fish reproductive phase terminology, this is a cycle, and the regenerating phase can be considered as the beginning of the cycle for a mature organism.


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FIGURE 3. Gonads of female Panamic Grunts with oocytes at different stages: (A) phase II (perinucleolus [PN]); (B) phase I (chromatin nucleolus [CN]), phase II, and phase III (secondary vitellogenesis [SV]); (C) phase II and phase IV (mature oocytes [M]); and (D) phase III and phase V (atretic oocytes [Atr]). Additional abbreviations are as follows: Ci = cytoplasm, n = nucleolus, N = nucleus, YG = yolk globule, TV = tertiary vitellogenesis, and LV = yolk globules.

Asynchronous development of oocytes, which is a characteristic typical of tropical fish, was observed in the gonads of mature females and has previously been reported in several other grunt species (Haemulidae), such as the Bluestriped Grunt H. sciurus, Latin Grunt H. steindachneri (Rodrıguez 1985), Tomtate H. aurolineatum (Kossowski 1985), White Grunt (Palaz on-Fernández

2007), and Cottonwick H. melanurum (Granado 1989). In the present study, atretic oocytes were observed in spent gonads, as was also reported by Mateo and Appeldoorn (2001) and Palaz on-Fernández (2007) for White Grunts and by Granado (1989) for Cottonwicks. There are many reasons for the presence of atretic oocytes, such as environmental stress, changes in hormone levels associated

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FIGURE 4. Monthly reproductive stages (see Table 1) of female Panamic Grunts collected from the two study zones in the Gulf of California: (A) coastal area and (B) open sea.

with age, nutrition, physiological status, an imbalance in the sex ratio during the reproductive event (Mester et al. 1974; Guraya 1986), and a strategy to optimize fecundity given available energetic reserves (Kurita et al. 2003). However, we did not attempt to determine the proportion of atretic oocytes and its relation to season or TL; therefore, a conclusion on the reason for the appearance of such oocytes cannot be drawn from our results. Our study found evidence of temporal and geographic variability in the duration of spawning activity, reproductive investment, and TL at maturity between the two study locations. The population of Panamic Grunts sampled in the open sea appeared to mount a smaller reproductive effort than those in the coastal zone, which consistently exhibited a greater reproductive potential. Differences in reproductive effort between locations were evidenced by gonad weight and GSI, with individuals from the coastal zone having significantly heavier gonads than those from the open sea. This was particularly

FIGURE 5. Monthly variation in (A) gonad weight (g) and (B) gonadosomatic index (GSI) of Panamic Grunts collected from the two study zones in the Gulf of California (coastal area and open sea).

apparent in the buildup to the well-defined coastal spawning season. Overall, seasonal changes in gonad weight and GSI were very marked in the coastal zone, including a significant peak in spring and subsequent decline until winter, whereas the population from the open sea showed no significant seasonal variation in GSI or gonad weight. Previous studies suggest that seasonal changes in gonad weight are an indicator of reproductive investment (Devlaming et al. 1982; Tamate and Maekawa 2000). Therefore, an absence of such changes in gonad weight in the open sea suggests a lack of reproductive activity in that section of the population. In contrast, high GSI values together with a very high gonad weight in the coastal zone specimens during spring suggest high reproductive investment. These results, together with the gonadal development stage data, can be used to reliably estimate the duration of the reproductive season (Fowler et al. 2000; Brown-Peterson et al. 2001). Panamic Grunts in the coastal zone showed a single peak in GSI and gonad weight during spring, which coincided with an increase in the percentage of mature


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FIGURE 6. Total length (cm) at maturity of female Panamic Grunts collected from the two study zones in the Gulf of California (coastal area and open sea). Black circles and triangles represent observed data, while solid and dashed lines are estimates.

females from April to June, and then exhibited an increase in spent gonads during August, at the time that the GSI and gonad weight started to decrease. Thus, we infer that the reproductive season in the coastal zone is protracted: it begins in March and continues for 5 months until July– August, encompassing mid- to late spring and all of summer. In the open-sea zone, there was no clear reproductive season. There were no significant changes in gonad weight or GSI through the year, and there was no period in which the percentage of mature females was significantly increased. Some samples had spent gonads during February and July, but it was not possible to link these to a preceding reproductive period. Furthermore, most of the organisms collected in the coastal zone were adults, while most of those captured in the open sea were juveniles, according to the estimated size at first maturity. The reproductive capacity of fishes is strongly influenced by body length (Marteinsdottir and Begg 2002), and a population consisting of larger individuals with larger gonads has greater reproductive potential than a population of smaller individuals. From the current results, it is evident that the coastal zone population of Panamic Grunts has a higher reproductive capacity and a welldefined reproductive season that was not observed for their open-sea counterparts. The individuals captured in shallow areas are there for reproductive purposes only, whereas the majority of the population remains in the open sea. This would at least partly explain why size at sexual maturity is smaller in the coastal zone and why most individuals in this zone are ready to spawn, while those in the open sea are not. Panamic Grunts use the coastal zone, including estuarine systems and coastal lagoons, as a nursery area

(Chittaro et al. 2004, 2005). This may explain why the reproductive stock is associated with this area. The geographic reproductive variability of Panamic Grunts suggests that the performance and reproductive output of this species differ between habitat zones. This may be a consequence of (1) the specific size or age structure of the stock, (2) environmental conditions that influence movement patterns, or (3) fishing pressure. Assuming that reproduction is the main contributor to stock restoration, this variability could significantly impact the conservation status of future generations of each population. Thus, in coastal areas where the small-scale gill-net fisheries operate, it may be necessary to manage and preserve the reproductive stock. At present, there are no fishing regulations aimed at managing Panamic Grunts in the Mexican Pacific, and there is no proper management plan in place. This is an important species in terms of landings biomass (SAGARPA 2013), as it is a major component of the shrimp fishery bycatch and is also targeted by the smallscale fishery operating with gill nets in the coastal zone (Amezcua et al. 2006; Madrid-Vera et al. 2007). The only regulation currently enforced in this area is for finfishes in general and relates to the number of fishing skiffs in operation. The present work shows that the removal of spawning individuals by the small-scale fishery represents a potential negative impact for the long-term stability of the Panamic Grunt population (Bani and Moltschaniwskyj 2008). Establishing the spawning time of Panamic Grunts may help to manage fishing activity, especially for heavily exploited populations. However, while the risk of fishing in spawning grounds is higher during spawning periods, overfishing of immature individuals

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(e.g., in the open sea) is potentially no less damaging given that the sustainability and productivity of a fishery are dependent on the continued availability of juveniles. Because Panamic Grunts are caught by different fisheries using different fishing gears, management through the establishment of biomass or minimum size limits may be insufficient unless geographic and temporal variability in reproductive performance is also considered (Bani and Moltschaniwskyj 2008). This would imply a designated no-fishing zone in the coastal area where the small-scale fisheries operate. The small-scale fishers in tropical and subtropical zones of the developing countries are usually very poor, and such measures may have significant economic and social implications. It will be necessary to consider the economic and social aspects of the fishers as well as the ecology of the target species before developing adequate and effective methods for fisheries management in the area. ACKNOWLEDGMENTS We thank V. Hernández (Centro Regional de Investigaci on Pesquera–Mazatlán) for his assistance in the histology laboratory and G. Ramirez and C. Suarez for their help in editing the figures. Funding for this work was provided by the research project Programa de Apoyo a Proyectos de Investigaci on e Innovaci on Tecnol ogica (PAPIIT) IN217408. There is no conflict of interest declared in this article.

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