Environmental characterization of the reproductive season of migratory fish of the Sinú river ( Córdoba , Colombia ) Caracterización ambiental de la temporada reproductiva de los peces migradores del río Sinú ( Córdoba , Colombia )

Objective. To characterize some abiotic factors during the reproductive season of migratory fish (bocachico Prochilodus magdalenae, dorada Brycon sinuensis, bagre blanco Sorubim cuspicaudus and barbul Pimelodus blochii) in the Sinú River. Materials and methods. From April to October, 2008, in Carrizola (Tierralta, 36.31 km from the Urrá hydroelectric plant) factors such as flow=Qriver, daily flow difference =ΔQriver, velocity=Vriver, temperature=Triver, electrical conductivity=CE, total dissolved solids=STD, turbidity=Turb, cloudiness=Nub, rainfall=Pluv and solar brightness=Bs were measured daily three times/day (07:00 h, 12:00 h, 17:00 h). Also, on the same schedule, ichthyoplankton was collected as an indicator of reproductive activity, assessed by reproductive frequency (Fr=number of days with presence of ichthyoplankton/number of days in the period evaluated X 100) and larval density (Dl=larval/m3). Results. The daily values of Qriver ranged between 278.7 and 838.5 m3/s, ΔQriver between 0.0 and 100.7 m3/s, Vriver between 1.40 and 1.53 m/s, Pluv between 0.0 and 88.2 mm, Triver between 27.0 and 28.7°C, STD between 73.0 and 302.3 mg/L, Turb between 9.7 and 679.7 NTU, CE between 81.0 and 361.7 mS/cm, Bs between 0.0 and 11.2 hours, Nub between 2.0 and 7.3 octaves. The Fr was 30.4%, with April (40.0%) and May (74.2%) as the higher activity reproductive months, while the Dl in the season was 4.9 larvae/m3, with the larvae group other species (2.9 larvae/m3) and bocachico (1.8 larvae/m3) as the most abundant. Conclusions. Most reproductive activity was recorded early in the season (April and May) and parameters such as Qriver, Triver, Vriver, Pluv, STD and Nub may be considered final factors associated with migratory fish reproduction.


INTRODUCTION
In fish, reproduction is a process controlled by external and internal factors; the external factors, which are of biotic type (predation, competition, sex ratio, population density, among other) and abiotic (flow, photoperiod, temperature, pH, dissolved oxygen, electrical conductivity, among others) act in different moments and spaces of the reproductive cycle (1).
The abiotic factors can trigger and extend spawning and generate favorable conditions for the development of larva (2).Such conditions are considered environmental factors that stimulate spawning of migratory fish.In rivers that have been intervened by hydroelectric constructions, these incentives could be altered and thus, could affect the reproduction of fish (3).
In tropical atmospheres, the increase in water level, precipitation and electrical conductivity are considered key factors in fish reproduction (4).Jimenez-Segura et al (4) found that in the Magdalena river, the initial and proximate stimuli, which determine the start of the gonad maturity, were high solar illumination and high water temperatures during shallow water periods; while final or last factors, which determined the courtship and mating, were the reduction of solar illumination, as a result of the increase in cloudiness and the reduction of the temperature during high and rising water periods.
In the Sinu river basin there is little information about the abiotic factor characteristics during the reproductive season of migratory fish and which of these can be considered as final factors for reproduction incentives (mating and spawning); therefore, the objective of this study was to characterize some environmental abiotic factors and which are associated to the final stimuli for the reproduction of migratory fish such as the bocachico, dorada, bagre blanco and barbul in the Sinu river.

MATERIALS AND METHODS
Study location.The Sinu river begins in the town of Ituango, Antioch (Paramillo Massif), crosses the towns of Tierralta, Valencia, Montería, Cereté, San Pelayo, Cotorra, Lorica and San Bernardo del Viento, in the department of Cordoba, and ends at the Caribbean Sea, in the Tinajones delta area.The total length of the river is 437.97 km, from its source until its mouth.At 267 km from its mouth, the Urra (HU) hydroelectric power plant was built, and therefore, the river is regulated by the operation of the hydroelectric plant.
In order to verify the presence of reophilic fish spawning, ichthyoplankton was collected daily between April 15 and October 15, 2008 (184 days), in the upper part of the Sinu river, at 36.3 km (North latitude 8°09´40.8"and West longitude 76°05´44.8")downstream from the HU (Carrizola, Tierralta, Cordoba).The period evaluated corresponded to the rainy season in the Sinu river basin.The ichthyoplankton was collected three times per day at 7:00, 12:00 and 17:00 hours, at a distance between 5 and 10 m from the right margin of the river, with superficial samples of 1 minute, using a simple conical plankton net with a mouth diameter of 50 cm and a 0.5 mm mesh opening; the samples were fixed in formalin 1% (v/v) neutralized with monobasic and dibasic sodium phosphate and labeled in 50 ml plastic jars.The ichthyoplankton were separated by species (bocachico, liseta, bagre blanco, barbul, and other species) at the Fish Research Center of the University of Cordoba (CINPIC) and their state of development was determined (blastomeration, blastulation, gastrulation, segmentation, pharyngulation).The identification was made based on embryonic and larva characteristics of the fish (5).To the embryos that were not identified, a development stage was determined, and they were counted and registered as other species (other spp.)

Larval density and reproductive frequency.
The estimation of the amount of larva collected from each sample was expressed as larval density per day (Dl, larvae/m 3 ) using the following equation:
The amount of days with reproductive activity of the migratory fish in the Sinu river during the reproductive season was called reproductive frequency (Rf), which was calculated by dividing the number of days with ichthyoplankton presence over the total number of days analyzed x 100.Rf was estimated per month and for the whole evaluated period.
Hydraulic characteristics of the river during the reproductive period.The daily estimation of the river flow was conducted (Q river ), flow difference (ΔQ river ) and river velocity (V river ).The Q river and the V rio were estimated three times per day (07: 00; 12:00 and 17:00 hours) based on the reading of the water level of the river, obtained at the IDEAM water level gauging Station in Carrizola (Tierralta, Cordoba); the river flow and an average velocity per day were calculated as well.The ΔQ river was estimated from the river flow differences from one day to the next.The Q river, V river and water level gauging readings were adjusted through eight hydraulic gauging (two times per month during six months) which considered the measure of V river and the Q river at different depths (superficial, 20% and 80% depth) every eight meters in a section of the river at Carrizola (Tierralta) with the aid of flowmeters (A.OTT Kempten, C31-00, Germany) with propeller (2-38798, Germany), flow meter (A.OTT Kemptem, Typ 12,400, Germany) and winch (65645PKS, Germany).

Physicochemical characteristics of the river.
The temperatures of the river (T river ), the turbidity (Turb), the total dissolved solids (STD) and the electrical conductivity (CE), were measured during each collection of ichthyoplankton.The T river was measured with a mercury thermometer with a precision of ±0.5°C (BRIXCO, United Kingdom).Turb was measured with a portable digital turbidimeter (Orbeco-Hellige, the USA); whereas CE and STD were measured using a digital conductimeter (WTW, LF538, the USA).An average value per day for each one of these parameters was estimated from the three daily readings.

Characterization of rainfall (Pluv), solar brightness (Bs) and cloudiness (Nub).
The daily records of Pluv, Bs and Nub, were obtained from the URRA I Weather Center Station, located at the dam (Tierralta, Córdoba).

Statistical analysis.
No environmental variable studied (Q river , ΔQ river , V river , T river , Turb, EC, STD, Pluv, Bs and Nub) or Dl met the assumptions of normality (Shapiro-Wilk test) and homogeneity (Levene test).A descriptive statistic (average±standard deviation) of all environmental variables considered during every day of the study (184 days) and the days in which spawning presence (ichthyoplankton) was detected, was carried out.During the studied period, Dl of the different species was compared though a non-parametric ANOVA (Kruskal-Wallis test) and when differences were observed, Dunnett's multiple comparison per pairs test was used (p<0.05).To determine the association between the studied environmental variables and the reproduction of the fish (presence of ichthyoplankton), a correlation analysis (Spearman Coefficient) and a Main Component Analysis (ACP) was conducted.The data was transformed through Log (Xi+1) before their analysis.The statistical analysis was conducted with using of the Statgraphic Centurion (6) and XLSTAT (vs.2011) programs.
Reproductive frequency and larval density.In 30.4% of the days of the evaluated period (184  3).
Environmental characteristic of the reproductive season of migratory fish.The daily Q river during the study's period presented values that ranged between 278.7 and 838.5 m 3 /s, with averages of 651.0 m 3 /s.But when fish spawning appeared, the maximum values were 792.7 m 3 /s for the bocachico, dorada, bagre blanco and barbul species; and minimums values of 543.1 3 m 3 /s for the group other species (Figure 1).La ΔQ río , durante el período osciló entre 0.0 y 100.7 m 3 /s.Cuando se presentaron desoves de especies como bocachico y bagre blanco, oscilaron entre 1.0 y 88.3 m 3 /s; mientras que los desoves de dorada sucedieron con valores que oscilaron entre 1.0 y 92.1 m 3 /s.Los desoves de barbul sucedieron con valores que oscilaron entre 1.0 y 100.7 m 3 /s (Figura 1).
La V río durante el período, mostró valores que oscilaron entre 1.40 y 1.53 m/s y en ese intervalo se presentaron los desoves de los peces (Figura 1).ΔQ river during the period ranged between 0.0 and 100.7 m 3 /s.When spawning of species like bocachico and bagre blanco appeared, the values ranged between 1.0 and 88.3 m 3 /s; while the dorada spawning occurred with values that ranged between 1.0 and 92.1 m 3 /s.Barbul spawning appeared with values that ranged between 1.0 and 100.7 m 3 /s (Figure 1).
V river during the period showed values that ranged between 1.40 and 1.53 m/s and fish spawning appeared during this period (Figure 1).
Pluv during the period of the study showed values that ranged between 0.0 and 1.53 and 88.2 mm; during this same interval, migratory fish spawning appeared.
T river during the reproductive season showed values that ranged between 26.7 and 29.0°C; while spawning appeared in the interval between 27.0 and 28.7°C (Figure 1).
STD values during the period ranged between 73.0 and 302.3 mg/L; dorada, bagre blanco and bocachico spawning appeared in this interval; while barbul spawning appeared in the interval between 99.3 and 119.0 mg/L (Figure 1).
Bs values during the reproductive period ranged between 0.0 and 11.2 hours.The values were similar to those values of the period where the bocachico, dorada, bagre blanco and other species were recorded.Barbul spawning occurred with minimum values of 1.6 and maximum values of 7.5 hours (Figure 1).

Correlation between environmental variables and migratory fish spawning.
Q river , V river , T river and Pluv, were the variables that showed the highest number of significant relations.Bocachico spawning is related to Q river , V river and T river , as well as STD and Pluv (p<0.05).Bagre blanco spawning, as well as bocachico spawning, were directly correlated to Q river , V river and T river , and inversely correlated to Bs. Dorada and barbul spawning were associated with Pluv and Nub, respectively.The other species group had a similar behavior to the bocachico species correlating with Q river , V river , T river and Pluv (Table 4).Analysis of Main Components.In figure 2, the formation of two big groups can be observed: the first group is composed by the environmental variables Q river , V river , T river , STD, Nub and Pluv, that showed a high relation with spawning of all type of reophilic species of the Sinu river; while the second group was composed by the environmental variables ΔQ river , CE, Turb and BS, which are not related with the main species of reophilic spawning in this river.

DISCUSSION
The collection of ichthyoplankton was composed, mainly, by migratory fish embryos of the Characiformes order (Prochilodus magdalenae and Brycon sinuensis) and the Siluriformes order (Sorubim cuspicaudus and Pimelodus blochii).
According to Maldonado-Ocampo et al (7) of the 1435 fish species that live in Colombia's fresh water systems, the orders that make up the most species of the continent's ichthyofauna are Characiformes, with 637 species (44%) Análisis de Componentes Principales.En la figura 2, se observa la formación de dos grandes grupos: el primero conformado por las variables ambientales Q río , V río , T río , STD, Nub y Pluv, que evidenciaron una alta asociación con los desoves de todas las especies reofílicas en el río Sinú; mientras que el segundo grupo estuvo conformado por las variables ambientales ΔQ río , CE, Turb y Bs, las cuales no están asociadas con los desoves de las principales especies reofílicas en este río.
and Siluriformes, with 524 species (37%).Jimenez-Segura et al (4), also reported that 64% of the ichthyoplankton of the Magdalena river belong to the migratory fish group of the Characiformes order (P.magdalenae, Leporinus muyscorum, Curimata mivartii, Salminus affinis and Brycon sp.) and Siluriformes (Pimelodus spp., Pseudoplatystoma magdaleniatum, S. cuspicaudus).Also, in other South American rivers, such as the Uruguay river, it was found that the largest abundance of larva collected belongs to the Characiformes order (3).
When analyzing the results by species, it was observed that the highest Dl in the Sinu river was shown by Prochilodus magdalenae, which is the most important species of the Colombian continental fisheries and the Prochilodus genus, which is the most abundant in species in the South American continental waters (7).Pimelodids S. cuspicaudus and P. blochii, showed the lowest larval abundance during the studies reproductive season.
Fr during the study's period indicated that the presence of ichthyoplankton was observed (reproductive activity) in only in 30.4% of the days .The months of April and May were the months with the most reproductive activity while in terms of frequency, like the Dl (which suggests that despite spawning appearing during the studied period (April-October), the first two months (April-May) are the months of highest reproductive activity and of highest larval density when compared to the rest of the period.These results suggest that in the Sinu river basin the highest reproductive activity of migratory fish occurs at the beginning of the rainy season, stimulated by the variations of abiotic factors caused by the start of the first rainy period of the year.
The Dl average of the estimated ichthyoplankton in Carrizola (Tierralta) as an indicator of the abundance of larval was 4.9 larvae/m 3 , which is higher than the records reported in the Magdalena river (2.5 larvae/m 3 ) (4).It's possible that the difference between these numbers is due to the sampling structure; in this study, an estimated average for the entire reproductive season is presented (184 days), considering only the days with spawning presence; while in the Magdalena rive, the amount of days evaluated was 72 days in two years of study.Salete-Daga et al (8) reported larval densities of 2.9 individuals/ m 3 in to floodable plains with different degrees of connection with the Parana river, Brazil; while Reynalte-Tatage et al (9) reported densities of 0.1 larvae/m 3 in the Ivinhema river, Brazil.
El río Sinú, a pesar de ser un río intervenido por la construcción de la HU, presentó una fuerte variabilidad en los valores de los parámetros que describen la masa de agua, generado por la estacionalidad pluviométrica, que se caracteriza por desórdenes cíclicos y temporales durante la transición de aguas bajas a altas y viceversa.Las alteraciones ocasionadas por el aumento de los niveles de las aguas, se caracterizaron por incremento en el caudal del río, velocidad, conductividad eléctrica, turbidez y sólidos totales disueltos y reducción en la temperatura.Iguales The Sinu river, despite being a river intervened by the construction of the HU, presented a strong variation in the values of the parameters that describe water mass caused by rainfall season, which is characterized by cyclical and temporary disorders during the transition between shallow and high waters and vice versa.The alterations caused by the increase in water levels are characterized by the increase in the river's flow, velocity, electric conductivity, turbidity and total dissolved solids and by the reduction of temperature.Similar conditions were reported for the Magdalena river with the difference that this river showed stronger daily fluctuations (4).
In this study, it was observed that spawning appeared when the river flows were above 790 ms 3 /s; agreeing with Baumgartner et al's proposal (2), who considered that this condition was the only way for these species' larva to reach floodable plains that are not connected to the rivers during dry season.Both in the upper part of the Parana river as well as in the floodable plains, a higher Dl of Pimelodus, Auchenipterus osteomystax and Iheringichthys labrosus was reported when the water level was high (2,10).
In the Sinu river, the results suggest that the variables associated to the spawning of reophilic fish were the river's flow, velocity, temperature, rainfall, total dissolved solids, cloudiness and solar brilliance.Jiménez-Safe et al (4) suggest that in the Magdalena river during both annual hydrologic cycles (2004)(2005), Dl increased when a reduction in solar brilliant, an increase in cloudiness, an increase in rainfall and a fluctuation of synchronized water appeared with specific moments of low lunar brightness (4).In the upper part of the Uruguay river (Brazil), the abundance of eggs and larva showed a strong seasonal variation related to the higher flow values and water temperature as well as lower dissolved oxygen values, pH and transparency (3).
In the Sinu river, spawning of P. magdalenae, S. cuspicaudus and other species are related to more than three parameters, being the river's flow, velocity, temperature, and rainfall common factors in these species; while B. sinuensis and P. blochii were only correlated to rainfall and cloudiness, respectively.In the Magdalena river, Dl of S. cuspicaudus, Pimelodus spp.and P. magdalenae was increased before the start of the currents when some reduction in solar brilliance was evident and the stability index began to decrease due to changes in the increase of rainfall and total dissolved solids (4).
In the high plains of the Portuguesa river (Venezuela), the presence of eggs between three condiciones fueron reportadas para el río Magdalena con la diferencia que este río presenta fluctuaciones diarias más marcadas (4).
En este estudio se observó que los desoves se presentaron cuando los caudales del río estuvieron por encima de 790 m En los llanos altos del río Portuguesa (Venezuela), se registró la presencia de huevos entre tres y cinco veces por año, sólo cuando se observó aumento del nivel del río, con velocidades de las aguas entre 0.59 a 1.06 m/s y generalmente luego del máximo nivel de inundación (11).En el alto río Uruguay (Brasil), se observaron huevos y larvas vitelínicas en los rápidos y desembocadura del río, con velocidades promedios entre 0.84 y 0.50 m/s and five times per year was recorded only when an increase in the river's level was observed with water speeds between 0.59 to 1.06 m/s and generally, after the maximum flood level (11).In the upper Uruguay river (Brazil), eggs and yolk-sac larvae in the river rapids and mouth, with average speeds between 0.84 and 0.50 m/s were observed (3).In the Sinu river, these events were observed with average speeds above 1.41 m/s.
In the Sinu river, the electric conductivity was not related to spawning of migratory fish, but they were related to the temperature.In the Cuiba, Mato Gross river (Brazil), the higher densities of embryos and larvae are related to the places with low concentrations of dissolved oxygen, electric conductivity and transparency, larger width of the river and intermediate depths (12).In the flood plain of the upper Parana river, the electric conductivity was positively correlated with the ichthyoplankton density (8); likewise, a positive linear ratio was observed between the abundance of total larvae and the environmental conditions; which suggests that the higher abundance of larvae was related to higher values of electric conductivity and temperature (near 30ºC) (8).
In this study, the highest spawning of reophilic fish in the Sinu river appeared between April and May, when the temperature showed values between 27.0 and 28.7°C.The highest reproductive intensity of many species of the Upper Parana river occurs between October and January (13), when the water temperatures are higher.Bialetzki et al (10) found strong relations between the ichthyoplankton community and the environmental variables in the Bahia river, mainly related with the temperature, the dissolved oxygen, the rainfall and the velocity.According to Jimenez-Segura (4) the photoperiod and the temperature are related to physicochemical processes associated with rainfall, such as the reduction in the intensity of solar brilliance, the increase in clouds and the increase in the water level, causing the reduction of the temperature.
In the Sinu river, the total dissolved solids were only correlated with P. magdalenae dissolves.In the Magdalena rive, the migratory fish spawning were related to total dissolved solids and the turbulence that characterizes the river currents period (4).
In the Sinu river, solar brilliance was only correlated inversely to S. cuspicaudus, spawning; whereas, in the river Magdalena, the change in maximum number of hours of solar brilliance between the months with higher and lower precipitation (about 2 hours), defined by temporary cloudiness patters, seem to define the chronology in the reproduction of reophilic fish (4).
Los resultados del presente trabajo permiten concluir que la mayor actividad reproductiva, en términos de Fr y Dl, se presentó al inicio de la temporada de lluvias (abril y mayo).
Where: Dl = larval Density by sampling (larvae/m 3 ) n = Number of ichthyoplankton collected by sampling V river = Speed of the river (m 3 /s) t = collection Time (60 s) Ared = Area of the net (m 2 ).

Figure 1 .
Figure 1.Variation of environmental factors in the Sinu river at Carrizola (Tierralta) during the 2008 reproductive season.a) River flow, b) river flow difference, c) river flow velocity, d) rainfall, e) temperature, f) total dissolved solids, g) turbidity, h) electric conductivity, i) solar brilliance and j) cloudiness.Black dots indicate days with spawning of migratory fish.

Figure 2 .
Figure 2. Biplot of the analysis of the main components for environmental variables and spawning in the Sinu river, Carrizola (Tierralta), during the 2008 reproductive season (April-October).

Table 1 .
Composition and stage of development of ichthyoplankton in the Sinu river in Carrizola (Tierralta) during April-October of 2008.April and May were the months with more Fr.June and July showed a reduction in FR; while a slight increase of Fr was observed in August (22.6%), La mayor Dl m se registró en abril (19.8 larvas/ m 3 ), la cual disminuyó con el transcurrir de los meses, alcanzando valores mínimos al final de la days), a presence of ichthyoplankton was observed; fourth month of the study; while the bagre blanco was observed during the first four months of the study.Barbul was only registered in May (Table

Table 2 .
Monthly reproductive frequency of spawning of migratory fish in the Sinu river in Carrizola (Tierralta) during April-October of 2008 (184 days).

Table 3 .
Monthly larval density of spawning of migratory fish in the Sinu river in Carrizola (Tierralta) during April-October of 2008 (184 days).

Table 4 .
Correlation between the environmental factors and the reproductive activity of the rheophilic fish in the Sinu river in Carrizola, Tierralta (April-October 2008).