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Abstract
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Champotón River is an unknown area within the Mesoamerican hotspot in Southestern México. Reproductive traits and population structure of Astyanax aeneus were analyzed along an environmental gradient of the upper, middle and lower sections of the river, where diverse environmental ]]> A. aeneus were collected from all sections with sweep nets (5 and 10m long by 5m deep, 0.03m mesh size) and a casting net (0.05m mesh size). At each study site and campaign, a total of 80 specimens (in average) were collected and were fixed in 10% formaldehyde for further analysis. Population structure by size was analyzed for each study site, based on the relative frequencies by standard length classes. The length-weight relationship was determined, and the identification of gonadal developmental stages, reproductive period, size at first sexual ]]> A. aeneus to maintain robustness  during the study period with tiny changes in condition factor. A. aeneus in the Champotón River, as opposed to South American river congeneric species of similar size, shows early sexual maturity, a short reproductive period with high gonadosomatic index ]]>

Key words: Astyanax aeneus, fish life history, first maturity, absolute fecundity, trade-off, ]]>

Resumen

El  Río Champotón es un área de  desconocimiento científico dentro del hotspot de Mesoamérica en el ]]> Astyanax aeneus fueron analizadas a lo largo de un gradiente ambiental en la porción dulceacuícola del río. Se estudiaron tres sitios: en la parte alta del río San Juan Carpizo, en la porción media San Antonio del Río y río abajo en Ulumal, en cinco períodos entre 2007 y 2008. Se registraron diversos factores ambientales en cada sitio de estudio. Los ejemplares de A.  aeneus ]]> A. aeneus mantuviera  una condición robusta durante el periodo de estudio con pequeños cambios en el factor de condición. Nuestros resultados indican que A. aeneus en el río Champotón, a diferencia de otras especies del mismo género y de la misma talla en ríos de Sudamérica, presenta una maduración sexual precoz, una  temporada reproductiva corta con elevados  valores del IGS, y una elevada fecundidad, lo que compensa la temporada de reproducción corta. ]]> A. aeneus tener éxito en un río con una alta frecuencia de huracanes.

Palabras clave: Astyanax aeneus, primera   maduración,  fecundidad  absoluta,  historia  de  vida,  huracanes, gradiente ambiental.

Organisms use various strategies in ]]>

To determine the impact of ontogeny ]]>

The  ]]>

Asymptotic length and length at first maturity are covarying life-history parameters that depend on individual growth rates, which are in turn affected by habitat ]]>
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Most studies comparing life histories in different types of habitat or in different species have considered relatively broad spatio-temporal scales (Magalhâes et al. 2003). However, few studies have focused on population variation at a small spatial scale, which is important in order to understand how fish populations persist under stress induced by environmental variability. To face local variability in habitat conditions, fish may display different patterns of energy allocation among survival, growth ]]>

An  interesting  aspect  of  fish  biology  is the  variety  of  reproductive  strategies  used by different fish groups. Knowledge of the reproductive biology of a species is essential to understand its population dynamics as well as to guide the management and conservation of organisms and their ]]>

The general pattern of reproduction displayed by a species or a population characterizes  its  strategies,  while  reproductive  tactics are traits that vary within this pattern and are evoked in response to ]]>

The aim of this study was to examine spatio-temporal variation in the population structure and reproductive biology of Astyanax ]]> (Günther 1860) along a longitudinal gradient in the Champotón River, through analysis of the reproductive period and its potential correlations with abiotic and biotic variables as well as determination of reproductive cycle stages, sex ratio, size at first maturity and reproduction-related morphological indexes. This type of study has been proposed because, in addition to clearing up aspects related to the biology of a species, it provides valuable information on the potential effects of environmental changes on species reproduction and survival.
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Materials and methods

Study area: The Southeastern Mexico has the most extensive and diverse aquatic ecosystems in Mexico, which are of great importance in terms of productivity and biodiversity. The Champotón River basin is classified as a priority hydrological ]]>

The Champotón River (19°24’10’’N - 90°46’15’’W and 19°16’47’’ N - 90°27’18’’ W), the main surface stream in the Yucatán Peninsula, is located in the humid subtropics of Southeastern Mexico, and contains high amounts of karstic material. This coastal river is ]]>

The climatic regime is hot subhumid with summer rain (June to September) and occasional winter ]]>

Three study sites were selected in ]]> Fig. 1): San Juan Carpizo (SJC) (19º18’29” N - 90º28’40” W) in the upper portion of the river (51.6km away from the river mouth), San Antonio del Río (SAR) (19º19’33” N and 90º33’39” W) in the middle portion (39km away from the river mouth), and Ulumal (U) (19º16.’30” N - 90º37’25” W) in the middle portion named “downstream” (25km away from the river mouth). Five campaigns were conducted at the study sites that include the seasonal changes affecting the study area: Winter in ]]>
Methods: Diverse environmental factors were recorded at each site using a Quanta multiparametric sonde: dissolved oxygen  (DO mg/L), temperature (ºC), pH and salinity (PSU). Biochemical oxygen demand (BOD5 mg/L) was quantified according to American Public Health Association procedures (2005).

For  habitat  characterization  the  following  variables  were  recorded:  altitude  above sea level (m), using an altimeter, maximum depth (m) using a depth sounder and maximum amplitude. The precipitation and air temperature values were obtained from the Mexican National Weather Service (Servicio Meteorológico Nacional 2008).

A. aeneus were collected between the 8h and 16h range, with sweep nets 5 and 10m long by 5m deep (0.03m mesh size) and a 0.05m mesh size casting net. Nets were cast for 1hr at each site covering about 100m, in order to pro- vide a representative sample of fish fauna per site. All depths of the river were covered, and pools as well as riffles and areas with vegetation were considered. Each campaign collected an average of 80 specimens at each study site; ]]>

We analyzed a total of 1 286 specimens, all of them were measured (standard length=Ls in  mm)  with  a  digital  caliper  model  CD-8 and an Ohaus analytical balance Explorer (0.0001g), total (Wt), eviscerated weight (We), liver  weight  (Wh)  and  gonad  weight  (Wg) were measured.

Population structure was analyzed by size, based  on  the  relative  frequencies  of  standard length classes of each study site. Standard length varied from 13 to 95mm. Nine length  classes  were  established  according  to the methodology proposed from Vitule et al. (2008),  with  closed  intervals  of  10mm  and each interval with a code: ]]> 2 (p<0.05).

The  length-weight  relationship  for  each sex was derived using the equation: Wt=aLs^b. Significant    differences   ]]> b of females and males. The Kruskal-Wallis test was used to confirm the existence of significant differences with p set at p=0.05 (Samat et al. 2008).

The identification of gonadal developmental stages was made using the gonad characteristics: size, ]]>

The  reproductive  ]]>

To estimate the first sexual maturity (L₅₀) size of females and males, data were inserted in a logistical model as follows: P=1/(1+e-r(Ls- L₅₀)) according ]]> 50 is the mean size at first sexual maturity, which was taken to be the size at which 50% of individuals were mature (Vazzoler 1996).

Relative fecundity ]]> vs Ls and RF vs W. The sex ratio was determined as the proportion of females to males expressed as a percentage of the total sample. The chi-square C² ]]>

Gonadosomatic index (GSI), hepatosomatic index (HSI) and Fulton’s condition factor (K), were estimated in immature individuals, females and males using the following equations: GSI=(Wg/We)*100; HSI=(Wh/We)*100 and K=(We/Ls³). One-way analysis of variance (ANOVA) followed by Tukey’s test ]]>

Correlations between GSI values and mean water temperature, precipitation and between HSI and K values were evaluated with Spearman’s correlation using XLSTATPro 2010.2.03 software. A two-matrix discriminant analysis (DA) was used. One matrix included the physico-chemical parameters of water (dissolved oxygen, ]]> 5), and habitat characteristics (water depth, maximum width, altitude) as well as precipitation. The second matrix included the morphological indices (GSI, HSI, K), sex, standard length (Ls), size classes and gonadal stages. Data were all log (x+1) transformed. Biological indexes, sex, Ls, size classes and gonadal stages were square root-transformed. The analysis was performed with XLSTAT-Pro 2010.2.03.

Results

Rainfall records of the Mexican National Weather Service (Servicio Meteorológico Nacional 2008) showed that the annual mean precipitation in the area was 61.81mm during the study period, with a minimum mean value of 0.57mm in the dry season (March and May), and a maximum mean value of 161mm in the hurricane season (August and October) (Fig. 2). Overflowing of ]]> Table 1). Mean air temperature fluctuated: the maximum values were recorded in June and July during the summer period (28.3 and 28.2ºC, respectively) and the minimum value in January 2008 (22.8ºC) (Fig. 2).

Maximum temperature values were recorded in April and July (28.7 and 29.7ºC, respectively) and the minimum in November (24.3ºC). DO levels were highest in January and November (6.7mg/L both months) and lowest in July and February (5.7 and 5.3mg/L respectively), and pH values remained constant throughout the study period (range of 7.3 to 8). Salinity oscillated from 0.1 PSU in November at all study sites to 1.2 PSU in July at U. BOD5 attained minimum values in November and maximum values in April at all sites (Table 1).

Population structure by size: A spatial and seasonal pattern was noted in the size-class frequency distribution. The downstream site was the only one where all nine class sizes were detected, (Fig. 3 a, b and c); furthermore, classes 6 and 7 had the highest frequencies in April and July (Fig. 3c). At the upper and middle portion of the river only seven classes (1 to 7) were detected. Youngest organisms had a strong seasonal distributional pattern, class 1 was present only in April at the upper site, and in November at all study sites (Fig. 3b). Based on chi-square (x²) tests (p<0.05), significant differences were found between the size-class frequencies at the various study sites.

Length-weight relationship: The length- weight relationship is shown in Fig. 4, along with its mathematical expression: parameter b was 3.23 for females and 3.08 for males. The Kruskal-Wallis test found no significant differences between the sexes (p>0.05). ]]>
Reproduction:  From  the  1 286  specimens  collected,  818  (63.60%)  were  males, 438 (34.05%) were females and 30 (2.33%) immature. Sex ratio was 1.87:1 (males:females), differing significantly from the expected 1:1 (x² p<0.05). Males were significantly dominant during the whole period of study (Fig. 5).

Immature individuals were detected in the middle and downstream sites only in January and November (Figs. 6a and b). Females and males in maturity stage 1 were recorded during all sites and months studied, except for the downstream site in July, with the maximum abundance occurring in January at all three sites, and the minimum abundance in all study sites in April and July (Figs. 6a and b).

Females in maturity stage 2 were recorded in the middle and in the downstream sites in January and in April (respectively), and a peak was  detected  in  the  upper  river  site  during July. Males in stage 2 were present during all months and at all sites, except for the middle site in July and November (Figs. 6a and b). Mature females and males were found in the middle and downstream sites in April and July; females were most abundant at the downstream site in July (100%), while males were more abundant in the middle site in July (95.65%). Females with gonads in post-spawning stage were present at the downstream site in April, and showed low values in the middle site in July, while males with testes in post-spawning stage were found only in the middle site in July (Figs. 6a and b). These data suggest that the reproductive period is from early spring to midsummer (from April to July).

Size at first maturity was 45.7mm for females and 40.8mm for males (Figs. 7a and b).  AF  ranged  from  432  oocytes  to  11 890 oocytes  in  one  female  of  75.2mm  length. The lowest mean RF was at the middle site (RF=435.91±49.24 oocytes/g), while the highest was recorded at the downstream site during  July  and  April  (RF=652.68±29.69  and 394.8±29.11   oocytes/g,   respectively).   RF was significantly correlated with Ls (r=0.58 p<0.05)  and  W  (r=0.53,  p<0.05),  while  AF was significantly correlated with Ls (r=0.58, p<0.05) and W (r=0.53, p<0.05) (Figs. 8a y b).

Somatic indices: Immature individuals were only found at the downstream site in January and November, and at the middle site in November with low GSI values; while HSI values of fishes from the middle site showed a peak in November ]]> Fig. 9a).

GSI values of ]]> Fig. 9a). GSI values of females from the upper site ranged from 0.64±0.04 in January to 2.93±0.48 in  July,  while  males  showed  lower  values (0.06±0.006 in February to 1.77±0.15 in July). In the middle site both females ]]> Figs. 9b and c).

]]> HSI  scores  in  females  from  the  upper site  ranged  from  1.94±0.08  in  February  to 2.98±0.41 in November, while males showed their minimum value in January (1.75±0.06) and their maximum in November (3.24±0.13). At the middle section, females had their mini- mum HSI value in April (1.72±0.05) and males in January and April (1.82±0.08 both months); besides, females and males had higher values in July and November (females 3.4±0.14 and ]]> Figs. 9b and c).

The lowest K values for both sexes from the upper site occurred in July (1.73±0.03 and 1.71±0.02 in females and males, respectively), while the highest ]]> Figs. 9b and c).

The correlation test between GSI and abiotic (temperature and precipitation) and biotic factors (HSI and K) revealed no significant correlation  except  with  regard  to  temperature, which displayed a significant ]]>

Discriminant analysis revealed that standard length (Wilks’ Lambda 0.344, p=0.0001), somatic  indexes  (K  Wilks’  Lambda  0.692, p=0.0001), GSI (Wilks’ Lambda 0.296, p=0.0001); HSI (Wilks’ Lambda 0.541, p=0.0001),  gonadal  stages  (Wilks’  Lambda 0.402, p=0.0001); relative fecundity (Wilks’ Lambda 0.671, p=0.0001), size ]]> Figs. 10a and b).

In the biplot of the discriminant ]]> Figs. 10a and b).

Discussion

The genus Astyanax is made up of ]]> A.  aeneus (size range 13-95mm) is a large-size species within  this  genus,  like  A.  janeiroensis  (25- 115mm)  (Mazzoni  et  al.  2005),  as  opposed to smaller species from the Paraguaçu River, Brazil, with standard length ranges 13-42mm (Santos  &  Novaes  2008)  and  intermediate size species such as A. aurocaudatus from the Cauca River, Colombia (14-74mm) (Román- Valencia & Ruiz 2005).

Size-class frequency distribution of A. aeneus evidenced the differential use of spatial resources (sites) over time (study periods) in the longitudinal gradient of Champotón River.  This  may  be  the  ]]> A. janeiroensis were located downstream while adult organisms are located in the upper reaches of the Ubatiba river. Vitule et al. (2008) found that the size-class distribution of Deuterodon langei differs along the Paraná River basin: a higher number of large- size individuals ]]>

A positive  allometric  growth  was  found in A. aeneus, meaning a greater increment in weight than in length (Orsi et al. 2002), perhaps related in turn to the reproductive period. Carvalho et al. (2009) report allometric ]]> A. fasciatus, stating that the data may be skewed since most specimens were adults. A higher number of adult fish was also found in the present study.

Species with external fertilization and no parental care tend to have intermediate levels of fecundity, e.g. A. henseli (5 375 oocytes) (Dala-Corte & Azevedo 2010), and ]]> Bryconamericus iheringii (1 600 oocytes); Bryconamericus stramineus (1 100 oocytes) (Lampert et al. 2004, 2007). From this standpoint, A. aeneus has intermediate levels of fecundity.

]]> Sex differences in body size and length- weight relationship are the most frequent sexual dimorphism in fish (Nikolsky 1963). Females of A. aeneus were larger than males, this same trait was reported in other Characiformes (Agostinho & Júlio-Júnior 1999) e.g. Astyanax bimaculatus, A. schubarti (Nomura 1975), A. eigenmanniorum (Barlá et al. 1988), ]]> A. fasciatus (Mora et al. 1997, Nomura 1975), A. scabripinnis (Veloso-Júnior et al. 2009), as opposed to A. aurocaudatus in which males are larger than females (Román-Valencia & Ruiz 2005). Large females size is advantageous since fecundity is increased, while large males are at greater advantage during reproduction of producing potentially more, and larger, offspring (Nikolsky 1963). Sex ratio is an important trait in estimating reproductive biomass and total population fecundity and is also one of the factors determining ]]> A. aeneus the sex ratio was  skewed  towards  males.  This  same  trait has been reported in A. bimaculatus ]]> vittatus (Gurgel & Alves 2001); Characidium sp. n. (Mazzoni et al. 2002); Astyanax scabripinnis paranae (Louzada & Orsi 2003); Hemibrycon sp. (Román-Valencia & Botero 2006). Wootton (1998) found that some fish species with external fertilization had a higher male ratio during the reproductive cycle. However, most females have high levels of fecundity, which is advantageous since males are ]]>

The optimal first reproduction size depends on many factors, including the relative allocation of energy between gonadal and somatic growth (Mazzoni et al. 2005). In species of the genus Astyanax, size at first maturity varies from 41 to 78mm ]]> A. aeneus reaches sexual maturity at 45.7mm in females and 40.8mm in males, smaller sizes than those in A. janeiroensis (55mm Mazzoni et al. 2005) and A. bimaculatus (69mm Agostinho et al. 1984); these species attain a similar size (Ls) in the course of their life cycle. Interpretation of the selection forces acting on the genus Astyanax suggests that early ]]> Geophagus  brasiliensis  living in contrasting habitats (upper reaches and fluvial-lagunar conditions). The size at sexual maturity was smaller in ]]>

Environmental conditions permitting, extended reproductive periods are more common than short ones (Kramer 1978). However, tropical freshwater fishes (in particular cyprinids, characids and silurids, which comprise most  of  the  tropical  freshwater  forms)  are an interesting exception to this generalization since they have seasonal reproductive periods (Vazzoler & Menezes 1992). Characidae species have their reproductive period between April  and  September  (Vazzoler  &  Menezes 1992, Lampert et al. 2004, 2007, Gonçalves et al. 2005). Reproduction season of A. aeneus is from April to July (spring and summer sea- sons), with a reproductive peak in July, when water levels rise. In tropical regions, various species take this event as a signal to carry out reproduction, as stated previously for A. fasciatus (Mora et al. 1997); A. bimaculatus (Braga 2001); A. aurocaudatus (Román-Valencia & Ruiz 2005); A. scabrippinnis (Abilhoa 2007); A. henseli (Dala-Corte & Azevedo 2010). Like- wise, Lowe-McConnell (1987) found that in tropical  regions  spawning  is  stimulated  by local rainfall or a rise in water levels. Lampert et al. (2004, 2007) found no correlation between reproductive traits and abiotic factors in Characidae from Rio Grande do Sul, Brazil in a subtropical region. However, the same authors recognize that a temperature increase may unleash the beginning of gonadal maturation. A. aeneus reveals that the beginning of the reproductive period takes place when there is an increase in temperature values as was detected by the positive correlation between GSI and water temperature, lending added sup- port to the above-mentioned hypothesis.

A gradual increase in GSI values indicates the period of gonadal maturation while an abrupt fall signals the spawning season (Htun- Han 1978). A better reproductive condition based on GSI of A. aeneus was during July. GSI variability was higher in females than in males, due to existing differences between ovaries and testes in terms of volume, mass, and  energy  demands  for  gamete  production; this same trait was noted in A. fasciatus from Brazil (Carvalho et al. 2009).

HSI has been used to evidence the potential transfer of energy from the liver in order to maintain relevant biological events such as reproduction. During the reproductive period individuals allocate less effort to food procurement and consume reserves stored in the liver, eliciting a reduction in HSI values, particularly in females (Nikolsky 1963). In A. aeneus, higher HSI values were found during periods of reproductive inactivity. This is interpreted as an increase in the reserve materials stored in the liver for subsequent use in gamete production. In females low HSI values prior to and during reproduction may result from the transfer of energy materials stored in the liver toward gonadal maturation and the breeding event (Santos et al. 1996, Zimmerman 1997). A. henseli had higher HSI values before the breeding period and lower values at its reproductive peak, suggesting greater use of liver reserves for vitellogenesis and gonadal maturation (Dala-Corte & Azevedo 2010).
 
Acknowledgments

The study was supported by the National Science and Technology Council (CONACyT- México) and the government of the state Campeche (Project: 31173) and the Secretariat of Research and Posgraduate Studies (SIP) of the National Polytechnic Institute (IPN-México).

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*Correspondencia:
Patricia Trujillo-Jiménez: Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Av.  Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, Mexico. trujill@uaem.mx
Jacinto Elias Sedeño-Díaz: Programa Ambiental, Av. Wilfrido Massieu s/n. Esq. Av. Luis Enrique Erro. Col. Zacatenco, Mexico, D.F., Mexico. jsedeno@ipn.mx
Julio A. Camargo: Departamento de Ecología, Facultad de Biología, Universidad de Alcalá, Ctra. Madrid-Barcelona km. 33,6 28871 Alcalá de Henares, Madrid, Spain. julio.camargo@uah.es
Eugenia López-López: Laboratorio de Ictiología y Limnología, Escuela Nacional de Ciencias Biológicas, IPN, Prol. de Carpio y Plan de Ayala s/n, Col. Sto. Tomás, Mexico, D.F., 11340 Mexico. eulopez@ipn.mx
1. Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Av.  Universidad 1001, Col. Chamilpa, C.P. 62209, Cuernavaca, Morelos, Mexico; trujill@uaem.mx
2. Programa Ambiental, Av. Wilfrido Massieu s/n. Esq. Av. Luis Enrique Erro. Col. Zacatenco, Mexico, D.F., Mexico; jsedeno@ipn.mx
3. Departamento de Ecología, Facultad de Biología, Universidad de Alcalá, Ctra. Madrid-Barcelona km. 33,6 28871 Alcalá de Henares, Madrid, Spain; julio.camargo@uah.es
4. Laboratorio de Ictiología y Limnología, Escuela Nacional de Ciencias Biológicas, IPN, Prol. de Carpio y Plan de Ayala s/n, Col. Sto. Tomás, Mexico, D.F., 11340 Mexico; eulopez@ipn.mx