INTRODUCTION

The grass carp (Ctenopharyngodon idella) is one of the largest species of the Cyprinidae family. It is the only member of this genus and there are no known subspecies. Since the grass carp C. idella was introduced to Mexico at the end of the 19th century from China, it was widely distributed in northern and central Mexico, and it was later introduced in the rivers of southern Mexico. This species has outstanding qualities due to its high biological potential (high reproduction rates and adaptation to a variety of habitats and climates), resistance to handling and diseases. Ctenopharyngodon idella along with Cyprinus carpio and Carassius auratus are among the 25 exotic freshwater fish species for the central region of Mexico and together represent 12 % of dominant exotic species, being introduced to the country for aquaculture and weed control purposes (^{Baruah et al., 2014}; ^{Contreras-MacBeath et al., 2014}; ^{Silva et al., 2014}; ^{Ahmad et al., 2018}).

In Mexico, it is cultivated in Aguascalientes, Chiapas, Coahuila, Durango, Guanajuato, Hidalgo, Jalisco, México, Michoacán, Puebla, Querétaro, San Luis Potosí, Sinaloa and Zacatecas states (^{INAPESCA, 2021}). For the southeast of Mexico, and specifically for Tabasco and Chiapas states, this species has fishing importance (^{Mendoza-Carranza et al., 2013}; ^{Mendoza-Carranza et al., 2018}), reaching in Tabasco a fishery production of 795 tons in live weight (^{CONAPESCA, 2021}). Despite its fishery importance, grass carp represents a threat to the ecosystems where it occurs as its herbivory habits decrease habitat complexity by reducing plant structure (^{Amador-del ángel, 2014}a; ^2014b; ^{Castillo-Domínguez, 2015}).

Recent studies in C. idella are focused on cadmium toxicity effects, evaluation of hematological response after exposure to endosulfan, effects of copper sulfate on gill histopathology, structural changes in gills and musculature by exposure to chlorpyrifos and mercury. The effect of dietary alginate on growth performance and non-specific immunity of juvenile carp (^{Dahmardeh et al., 2012}; ^{Atabati et al., 2015}; ^{Bala, 2016}; ^{Kaur & Jindal 2016}; ^{Vajargah & Hedayati, 2017}; ^{Hu et al., 2021}). On the other hand, studies on genetic diversity and phylogenetic relationships have been carried out in China, using SSR markers (^{Yu, 2014}); as well as the variability of populations in China estimated using EST-SNP markers (^{Muhammad et al., 2022}) and the analysis on the chemical composition and fatty acid profile of fillets (^{Hoseini, 2013}). Likewise, evaluation of hematological and plasma indices in grass carp with reference to age, sex and hormone treatment (^{Ejraei et al., 2015}). Other studies evaluate the weight-length ratio of the species fed with balanced food and comparative studies of the retina of the eye with other fish species (^{Bhosale & Bhilave, 2014}; ^{She et al., 2014}) and pathologies caused by cestodes (^{Ahmad et al., 2018}). As seen in Mexico, basic and applied research on this species is

very limited. The objective of this research is to determine some aspects of the reproductive biology, age and growth of the grass carp Ctenopharyngodon idella in the basin of the Usumacinta River, Tenosique, Tabasco, that will serve as base information for the implementation of ecological-fisheries strategies for a sustainable use and control of this introduced species.

MATERIAL AND METHODS

RESULTS

Immature specimens presented a TL 27.50 to 37.5 cm (56.18 ± 16.15 cm). Males presented a TL 61.53 to 77.54 cm (68.5 ± 3.78 cm) with the 60 cm class being the most frequent. In females the TL was 40.00 to 81.5 cm (72.1 ± 7.29), with the 70 cm class being the most frequent. Males were significantly smaller in length and weight (medians (M) = 68.5 cm TL 3439.0 g TW, than females with M =72.0 cm TL 3986.0 g TW (Mann-Whitney, W = 2121.0 and 1094.5, p < 0.001). The relationship for females was TW= 0.0457(TL)2.6617 and for males TW= 0.1182(TL)2.4290. For both sexes the model obtained was TW= 0.0526(TL)2.6244, and the percentage of variability of the data explained by the model (R2) was 88 % for females, 72 % for males and 85 % for both sexes. The observed value of b for the TL-TW equation for both sexes is less than three, indicating that the species presents a negative isometric growth type (t2 =1.00, p<0.005) (Figure 1). The length- weight relationship of female and males were significantly different (ANCOVA, F1.106 = 268.54, p < 0.001).

Figure 1 Length-weight relationship in females (a), males (b) and both sexes (c) of C. idella (N = 100) from the Usumacinta River, Tabasco, Mexico. TW = Total weight, TL = Total length, R2 = Coefficient of determination 

Males accounted for 53 % of the organisms analyzed, while females accounted for 47 %, resulting in a male: female relationship of 1.1:1. The proportion of males was higher in February (88 %) and April (80 %), while females presented maximum values in May (89 %) and August (80 %). The relationship between males and females was statistically different in February (X²11= 4.5, p = 0.034) and May (X²11= 5.4, p = 0.020). The overall sex relationship showed no difference (X²11= 16.88, p = 0.111). In October and November, it was not possible to capture specimens, due to the increase in river level.

The maximum GSI values in females occurred during April (15.52) and August (9.12). In January, June and December the GSI was less than 2.8. In males, the maximum GSI values were observed in July (2.17) and September (2.41), in the months of January, June and December the GSI was below 0.68 (Figure 2).

Figura 2 Monthly variation of the gonadosomatic index (GSI) and hepatosomatic index (HSI) in females (a) and males (b) of C. idella from the Usumacinta River, Tabasco, Mexico (N = 100) 

The hepatosomatic index (HSI) in females showed its maximum values in June (2.91) and December (2.3) while the minimum was recorded in April (1.17). For males, the maximum values were recorded in June (3.18) and August (2.33) and the minimum in May (1.17). K values for both sexes had little variability throughout the year, showing a slight increase for females in March, June and September, with maxima in March for females (1.69) and December for males (1.59). The minimum values for females were 1.29 during April and 1.14 for males in August. The macroscopic description of the maturity stage of C. Idella gonads is described in Table 1 and Figure 3.

Absolute fecundity in C. idella (n = 26) was in females weighing 2.318 - 5.845 g (X = 4.091g ± SD 771.34 g). This fecundity was 36.736 - 607.780 oocytes (X = 320.887 ± SD = 133.549.38). Relative fecundity was 14 - 125 oocytes/g (X = 78 oocytes/g ± SD=28.63 oocytes/g).

Figure 3 Images of gonad maturity stages in females (a) and males (b) of C. idella captured in the Usumacinta River, Tenosique, Tabasco. I = Immature, II = Inactive, III = Maturing, IV = Mature, V = Spawning and VI = Worn 

The studied population of Ctenopharyngodon idella from the Usumacinta River consisted of eight age groups between 1, 3 and 9 years (Figure 4). For both sexes, ages 4, 5 and 6 were the most frequent (28 %, 25 % and 22 %, respectively). It is important to mention that no specimens belonging to age group 2 were obtained. The average error rate among the three readers was 8.26 % with a coefficient of variation of 8.45 %.

Figure 4 Images of vertebrae of C. idella showing the age of organisms captured in the Usumacinta River, Tabasco, Mexico. Black dots represent age: one-year (a), three years (b), four years (c), five years (d), seven years (e) and eight years (f) 

The von Bertalanffy growth equation for both sexes was TL∞= 72.03(1-e0.46(t-0.553)), for females was TL∞= 74.26(1-e0.55(t-0.5568)) and for males was TL∞= 51.02 (1-e0.289(t-0.280)).

Water temperature ranged from 23°C in December to 30°C in May. Precipitation ranged from 1.9 mm in March to 22 mm in November. The Usumacinta River level reached its lowest value in April, at 11 m a.s.l., obtaining the greatest depth (19.11 m) in October. Rainfall was high throughout the second half of the year, beginning in June with 10.7 mm and ending in December with 14 mm.

DISCUSSION

This research is the first to be conducted on the reproductive biology of grass carp in the hydrological accounts of Mexico, so it was not possible to compare our data with previous studies, since most studies are focused on its fisheries importance (^{INAPESCA, 2021}; ^{Mendoza-Carranza et al., 2018}). Despite this lack of studies related to biological-fishery data, it is observed that the TL (cm) and weight (g) recorded were similar to growth in captivity (^{Sherrat, 2020}). The frequency in TL and weight recorded was lower than that reported for this same species in Western Europe, but were similar to those recorded in the fishery resources of the Usumacinta River in Mexico (^{Milardi et al., 2015}; ^{Mendoza- Carranza et al., 2018}). The size structure of C. idella depends on the environment in which they live, mainly in terms of food availability, population density and ecological factors. Therefore, the recording of these lengths in this study may be conditioned by a migratory behavior of the species, as is the case of other species, such as Labeo rohita, Barbus graellsii, Chondrostoma miegii (^{Miñano et al., 2000}; ^{Mir et al., 2013}).

Analysis of length-weight relationship for females and males indicates that these are statistically different, similar data to those recorded by ^{Hailu, (2013)} and ^{Khalid & Naeem, (2017}) in a tropical reservoir (Amerti: Ethiopia) and Southeastern Pakistan, respectively. The male: female ratio in the present study was similar, the records by ^{Hailu, (2013)} for common carp (Cyprinus carpio). However, in the present study there was difference in this ratio in the month of February that was favorable to males and on May was favorable to females. It is relating it to the reproductive indices for these months; it can be observed that males mature first than females, with the purpose of preparing to spawn in the month of April, where the highest gonadosomatic index was recorded.

The GSI in C. idella indicates an activity starting in February with a maximum peak in April and August in females, behavior that is related to the reproductive peaks of males during the annual cycle studied. These records are similar to those reported in the Nile River at a temperature of 20 °C. As well as with specimens from a reservoir in Sri Lanka, where reproductive peaks occur in the month of October. However, in the present study, no specimens were captured in this month due to the increase in the level of the Usumacinta River (^{Abd-Elhakim et al., 2019}; ^{Nathanael & Edirisinghe, 2021}; ^{Sheha et al., 2021}). In carp, final maturation and spawning could occur within a 24-h period following environmental cues (water temperature, dissolved oxygen) and stimulating factors (specific climatic conditions, the presence of herbaceous vegetation, opposite sex and rainfall or flooding) for spawning to be present, and this likely accounts for increased GSI during the reproductive period. If these signals do not appear within a certain period, at the gonadal level, atresia or reabsorption of a portion of the vitellogenic oocytes occurs (^{Nathanael & Edirisinghe, 2021}). On the other hand, C. idella has high reserves of essential fatty acids such as Ω-3 and Ω-6, which contributes to the reproductive success of the species (^{Bibi & Muhammad, 2021}).

The hepatosomatic index for C. idella in the present study shows similarity to that recorded for the species in the Nile River of Egypt (^{Abd-Elhakim et al., 2019}).

In the present study the length distributions were relatively wide, ranging from 55 to 110 cm, which, are within the age of first sexual maturity in males of 53 cm in length reported by ^{Sheha et al., (2021)} and those reported by ^{Abd-Elhakim et al., (2019)} of 62 cm for females and 53 cm for males.

The fecundity of the species in this study resulted similar to that reported by ^{Maiztegui, (2015)}; ^{Khalid & Naeem, (2017}) and ^{Jones et al., (2017)} for C. idella and C. carpio, respectively.

One of the important environmental parameters for the growth and reproduction of grass carp is water temperature. In this research resembles those reported by other authors on the biological aspects of the species, mentioning tolerances from 0 to 33 °C. It, and that temperatures above 38 °C, that are lethal for adults, and the water temperature in which they are stimulated to sexual maturity is between 20 to 30 °C, but generally between 20 and 22 °C. These parameters are similar to those recorded for the species Cyprinus carpius (^{Laverde & Hernando, 2012}, ^{Tessema et al., 2020}).

The most frequent ages of C. idella in the present study for both sexes were 4, 5 and 6 years, being these ages different from those reported in Eastern Europe (from 7 to 17 years) (^{Milardi et al., 2015}), these differences may indicate the impact of the fishery to which the species is subjected in the Usumacinta River. In addition, they are within the age recorded in this same species in two reservoirs: Patterson and Bowman-Haley in North Dakota in the U.S. State, which ranged between 2 and 24 years through the study with fin rays and between 2 and 27 years with dorsal fin spines (^{Weber et al., 2011}). Other species studied in the same family present this variability; such is the case of the species Labeo rohita where the highest age recorded was 8 years with a TL of 86.22 to 90. 45 cm; also in the species Barbus graellsii and Chondrostoma miegii recording specimens of 10 and 8 years of age, and of Gobio lozanoi with ages of 7 and 8 years; Luciobarbus callensis of 4 and 7 years. To some extent, these variations are the product of the plasticity of the species to adapt to different environments (^{Miñano et al., 2000}; Amat-Trigo et al., 2013; Mir et al., 2013; ^{Mimeche et al., 2013}).

In this study, the adaptability of Ctenopharyngodon idella to the environmental and ecological conditions of the Usumacinta River in southeastern Mexico is confirmed. However, being an exotic species, it is among the most important, least controlled and irreversible impacts that occur in ecosystems and that affect their biodiversity in a very important way; as well as, they can strongly modify the hydrology, the biogeochemical cycle and the biotic composition of invaded ecosystems (^{Strayer, 2010}; ^{Traveset, 2015}). On the other hand, the large volumes with which species are caught have positively impacted the economy of fishermen, since, although they do not have a high commercial value, they represent a good income for their families. Likewise, these species have modified the dietary patterns of the surrounding communities, a source of affordable animal protein for these communities due to the economic value at which they are marketed (^{Mendoza-Carranza et al., 2018}).

CONCLUSION

The biological-fishing aspects demonstrate the adaptive capacity of the species in southeastern Mexico, specifically in the Usumacinta River basin. It is a species with two maximum peaks of sexual maturity, in July and September for males, and in April and August for females. The most frequently captured ages of C. idella for both sexes were 4, 5 and 6 years old. This indicates that, according to the data obtained in this research, fishing exploitation is mainly of young organisms. It is important to continue with these studies to provide biological, ecological and commercial information in different geographic and temporal areas with the objective of establishing a fishing management of this species that is being subjected to strong fishing pressure.