Reproduction of the fish gracilis (: ) in Coatetelco, a tropical shallow lake in Mexico

José Luis Gómez-Márquez1, Bertha Peña-Mendoza1, Isaías H. Salgado-Ugarte2, Abby K. Sánchez-Herrera1 & Leonardo Sastré-Baez1 1. Laboratorio de Limnología, F.E.S. Zaragoza, U.N.A.M. Batalla 5 de Mayo esq. Fuerte de Loreto, Ejército de Oriente, C.P. 09230 Iztapalapa, México, D.F.; [email protected] 2. Laboratorio de Biometría y Biología Pesquera, F.E.S. Zaragoza, U.N.A.M. Batalla 5 de Mayo esq. Fuerte de Loreto, Ejército de Oriente, C.P. 09230 Iztapalapa, México, D.F.; [email protected]

Received 19-vi-2007. Corrected 21-v-2008. Accepted 31-vii-2008.

Abstract: A reproductive analysis of 1 225 specimens of Poeciliopsis gracilis obtained through monthly samples from Coatetelco, a tropical shallow lake in Central Mexico, was made. There was an evident sexual dimorphism, including a difference in body size at the onset of reproduction. Sex ratio deviated significantly from unity. Monthly variations in gonadosomatic (GSI), hepatosomatic (HSI) indexes and ovarian development stages showed that the spawning season was from July to October, coinciding with the rainy season and phyto- plankton biomass increase. The largest sizes were 50 mm for females and 43 mm for males. Rev. Biol. Trop. 56 (4): 1801-1812. Epub 2008 December 12.

Key words: chloropyll “a”, gonadosomatic index, hepatosomatic index, Poeciliopsis gracilis, reproduction, sex ratio, Mexico.

The members of the fish order Nicaragua Lake (Miller 1966, Miller et al. Cyprinodontiformes are cosmopolitan in 2005). P. gracilis has been recently recorded to tropical and temperate latitudes. The the North of its previously known distribution Poeciliopsis belongs to the Heterandrini Tribe zone at the Balsas River basin in Morelos and and comprise 44 . The poeciliids are Puebla, Mexico (Mejia 1992). small fishes, none attains an overall length of Poeciliids live in a broad array of habitats, 50 mm and most are less than half of that size occupying temperate to tropical zones, desert, (Rosen and Bailey 1963, Rauchenberger 1989, rivers, lakes springs, fresh and brackish marsh- Huidobro 2000). Only a small proportion of the es, seacoasts, and saline mangrove swamps. nearly 200 poeciliids species has been studied However, basic ecology of most poeciliids is in an ecological context (Meffe and Snelson unknown. Considering the economic impor- 1989). The porthole livebearer Poeciliopsis tance of poeciliids (aquarium trade, biological gracilis (Heckel 1848) is of Central American control, conservation) few species have been origin (Meffe 1989, Miller et al. 2005). studied in the field as P. gracilis (Huidobro The species is a member of the live-bear- 2000) and P. infans (Galindo-Villegas and ing teleost poeciliids and can be found in the Sosa-Lima 2002); the majority of the available Pacific slope from the Río Verde in Mexico, information comes from laboratory studies to the Eastern tributaries of the Fonseca Gulf (Meffe and Snelson 1989). in Honduras (Choluteca River) and, possibly Martínez et al. (2004) and Maya et al. Nicaragua. On the Atlantic slope it is found (2006) mentioned that ornamental fish culture from the Coatzacoalcos River in Mexico to is one of the main economic activities at the

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 1801 Morelos State, being the Poeciliidae family between 24°C and 26°C. The highest air tem- the most cultivated at the fish farms, with an peratures were recorded in May (32°C) and the annual production of 16.5 millions of fry that lowest in December and January (20 - 21°C). represent US$2.59 millions. The observed water temperature fluctuation P. gracilis is a species which is caught at in this study was similar to that reported by several aquatic systems in Mexico. It’s ecologi- Granados (1990), in that low temperatures pre- cally very tolerant, inhabiting in quiet water vailed in January and February, whereas high of streams, flood-water ponds, lagoons, micro temperatures prevailed during the rest of the reservoirs, lakes and dams, in water clear to year. Water level decreased between January turbid or very muddy (Meffe and Snelson Jr. and September. 1989, Miller et al. 2005). This species starts to be reared in laboratory in order to obtain Monitoring: The samples were taken results about to how the environmental con- approximately at monthly periods from May dition affects its survival and how the food 2002 to April 2003. Fish were caught with a amount and quality, affects its growth rate and seine 10 m long and 1.0 m deep, with 5 mm fecundity. mesh and fixed in 10 percent formaldehyde. In spite of the high demand of P. gracilis Specimens were then transported to the labora- as a forage species in Mexico, its commercial tory where they were measured to the nearest value is very low, as from the ecological point 0.1 cm and weighed to the nearest 0.01 g. of view there are few investigations about Maturation stages for females were established the impact that this introduced species causes by gonadal inspection following Mendoza’s on the native fauna and habitats in different technique (1962) and Contreras-MacBeath countries. and Ramírez-Espinoza (1996) description. The To date, no studies in relation with P. ovaries were removed, weighed and the ovules, gracilis reproduction has been carried out at eggs and embryos from each female caught Coatetelco, a tropical shallow lake at Morelos, throughout the study were counted. Mexico. The purpose of this study was to ana- The gonadosomatic and hepatosomatic lyze the relationships between the reproductive indexes (GSI and HSI respectively) were esti- cycle (fecundity-length, fertility-length, size of mated by: first reproduction, sex ratio, maturity develop- ment stages, etc.) of P gracilis and the environ- Wg Wg mental conditions. GSI = 100 We We MATERIALS and METHODS Wh HSI = Wh 100 Lake Coatetelco (18°45’ N; HSI = 100 Study site: We 99°20’ W) is located at an altitude of 1100 m in e Morelos State (Anonymous 1981, Anonymous 5 Wt 1998). It has a surface area of approximately where W is gonadK = wet10 5 weightWt (g), W is liver g K =10 3 h Lt 3 120 ha, a mean depth of 0.49 m and a maxi- wet weight and, We is evisceratedLt wet weight mum depth of 1.5 m. Gómez-Márquez (2002) (g). This can be considered as a measurement cited that the conductivity varies between of reproductive cost. To establish the size of 574 and 1 110 µsiems/cm, pH values were first reproduction for females, the ovaries were considered as lightly alkaline (8.9 average), examined following the criteria employed by even that at a global way the tendency was Reznick and Miles (1989) and using the logis- to increase from June to December. Lake tic equation (King 1995). For males, we con- Coatetelco is characterized by a sub humid sidered the smallest sample with completely warm climate, with annual mean temperature formed gonopodial structures.

1802 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 The total length (Lt)-total weight (Wt) rela- to 0.72 g (males) and 0.1 to 5.0 g (females). tionship was calculates by regression between The females were larger than males (t-student these variables for each sex using the formula: = 13.98; p<0.05). There was an evident sexual dimorphism in the morphological features of P. Wt = aLt b gracilis, being the modification of the anal fin in males to form a gonopodium the main sexual A covariance analysisWg made it possible to distinctive characteristic. determine whetherGSI or= not there100 were significant W differences at p<0.05, fore the length-weight Sex ratio: Of the 1 143 adults specimens relationship between both sexes. dissected, 345 (30.2%) were males and 798 W Condition (K)HSI was= calculatedh 100 for males and (69.8%) were females. The sex ratio of the females using the Fulton’s formula (Nikolsky catch as a whole was 2.3:1 (female:male), sig- We 1963): nificantly different from a 1:1 ratio (χ²= 89.76, p<0.05). The females dominated significantly Wt K =105 throughout the year, except February when Lt3 more adult specimens were males (Fig. 1).

Where Wt = total wet weight (g) and Lt = total Length-weight relationship: This rela- length (mm). The Kruskal-Wallis test (p<0.05) tion was evaluated for all individuals, and for was used to test whether condition differed each sex separately (females and males), due to between males and females. the significant difference between the male and Fecundity was estimated by calculating the female slopes of Wt-Lt regressions (ANCOVA; regression of the ovules number on the total F = 19.03, p<0.05). These equations are given length, using logarithms. The sex ratio was below: analyzed for the whole population by month. The statistical significance of the monthly ratio Females: results was established by a goodness of fit Wt = 0.0134 Lt 2.94, R² = 0.9431, p<0.05 Chi-squared test (χ²). Some environmental factors were also Males: investigated to determinate if they are associ- Wt = 0.0155 Lt 2.73, R² = 0.7426, p<0.05 ated with the breeding cycle of the fish. Surface temperature was measured using a thermom- All fishes: eter around 12:00 h during each sampling occa- Wt = 0.0132 Lt 2.94, R² = 0.9319, p<0.05 sion. In addition, previously measured month water temperature data for the period between Weight increased allometrically with size 2002 and 2003 were considered. A photosyn- (Fig. 2), since b value had a significant differ- thetic pigment (chlorophyll”a”) was measured ence from 3 (t = -2.027, p<0.05 for females, by means of the spectrophotometric method and t = -8.530, p<0.05 for males). For the same (Wetzel and Likens 1991). length, females were heavier. The catalogue number of voucher speci- mens is IBUNAM 12725. Maturation stages and reproduction: The size of first reproduction for females was RESULTS 28 mm total length. In males, the smallest specimen identified with completely formed Biometry: The total sample size was 1 225 gonopodial structure measured 22 mm total P. gracilis individuals. Standard body length length. ranged from 19 to 43 mm (males) and from 20 Percentage of each gonadic develop- to 50 mm (females) with weights between 0.08 ment stage is illustrated in Fig. 3. Monthly

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 1803 140

120

100

80

60 Number of fish 40

20

0 M-02 J J A S O N D J-03 F M A

Females Males

Fig. 1. Sex ratio at monthly periods for P. gracilis.

1.6

2.9432 1.4 Wt = 0.0132 Lt R2 = 0.9319 1.2

1

0.8

0.6 Total weight (g) weight Total

0.4

0.2

0 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 Total length (cm)

Fig. 2. Length-weight relationship of P. gracilis.

occurrences in the ovarian maturation stages of We found a broad breeding activity as inter- P. gracilis were used to establish the breeding preted by the presence of development stages period of the species. According with female’s IV and V, which were present all the year. Fig. gonadic maturation stages, 14.6 percent of the 3 shows that for females, the highest propor- total fishes were first reproduction (II), 15.4 tion of the average gonadal ripe stage (V) was percent were maturing (III), 4.6 percent were present in October. However, from January to mature (IV), 46.9 percent were ripe (V) and, April another reproduction peak was registered. 2.8 percent were spent (VI). Therefore, 54.2 On the other hand, the fishes in spent stage (VI) percent of the fish were in the reproductive were observed in June and in December. process. In the males all gonads analyzed were For females (Fig. 4A), the highest gona- mature all the time. dosomatic index (GSI) values occurred in

1804 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 100

80

60

Percent 40

20

0 M-02 J J A S O N D J-03 F M A

I II III IV V VI

Fig. 3. Seasonal variation of development maturity ovary stages for P. gracilis.

20 18 A 16 14 12 10 8 6

Gonadosomatic index 4 2 0 M-02 J J A S O N D J-03 F M A

14 B 12 10 8 6 4

Gonadosomatic index 2 0 M-02 J J A S O N D J-03 F M A

Fig. 4. Seasonal variation of the gonadosomatic index (GSI) of P. gracilis females (A) and males (B).

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 1805 October and decreased during November, fecundity and body length (r=0.46, p>0.05). reaching another peak in March. The GSI Moreover, embryos from each female caught of males (Fig. 4B) varied over the year and throughout the study were counted (fertility). significant differences between months were Brood size was variable too, ranging from one found (Kruskal-Wallis, H = 82.29, p<0.05), to 12, with a mean fertility of four. We calcu- with March and December showing the high- lated a regression between fertility and total est values. A similar pattern of gonad and liver length, which resulted in a significant (p<0.05) weight means for females was detected. The determination coefficient (r²) of 5.04%, indicat- value of hepatosomatic index (HSI) of females, ing that the number of embryos is not influ- reached its maximum in September (Fig. 5). enced by female size. With regard to condition, there were not significant differences between sexes (Kruskal- Environmental factors: Data on water Wallis, H = 3.20, p>0.05), with females (Fig. temperature and chlorophyll “a” are presented 6A) always in better condition than males (Fig. in figure 7. During the present study, the area 6B), and showing similar pattern. The condi- was characterized by a dry (November to May) tion values of males calculated with total or and a rainy (June to October) season. The lake eviscerated weight were similar. Condition water level increased from July to October in decreased from February to June, especially in response to the “heavy rains”. The water tem- the females, maybe due to prevailing adverse perature ranged from 24.1°C to 32.3°C, and was environmental conditions. When the repro- relatively high from March to October. Low ductive cycle began in July, the condition of temperatures were recorded from December both sexes improved, although it can be con- to January. Respect to chlorophyll “a”, the sidered that in the females the energetic cost data showed that phytoplankton biomass peaks of embryo formation is higher. In October the occurred during October and April. maximum condition values were achieved, as a consequence of weight increase due to embryo Discussion growth and to the favorable environmental conditions. Due to the limited information about The fecundity (number of oocytes + reproduction biology of P. gracilis in different number of embryos) was estimated from 455 journals, the discussion here was elaborated con- females and ranged from 1 to 74, with a mean sidering papers on biological and reproductive value of 44. There were no correlation between aspects occurring with other species or genera.

10 9 8 7 6 5 4 3

Hepatosomatic index Hepatosomatic 2 1 0 M-02 J J A S O N D J-03 F M A

Fig. 5. Seasonal variation of the hepatosomatic index (HSI) of P. gracilis females.

1806 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 4.5 A 4 3.5 3 2.5 2 1.5 Condition (%) Condition 1 0.5 0 M-02 J J A S O N D J-03 F M A

3.5 B 3 2.5 2 1.5

Condition (%) Condition 1 0.5 0 M-02 J J A S O N D J-03 F M A

Fig. 6. Seasonal variation of condition index of P. gracilis females (A) and males (B).

160 140 120 100 80 60 40 20 0 M-02 J J A S O N D J-03 F M A

Chlorophyll “a” (µg/m3) Water Temperature (ºC)

Fig. 7. Seasonal variation of chlorophyll a concentration (µg/m³) and water temperature (°C) at Coatetelco lake, Morelos.

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 1807 During the present study we confirmed that environmental conditions. Rosenthal et al. P. gracilis is a dimorphic species with marked (2001) cited that the brightly colored appears secondary sexual differences in size and the detrimental for survival and involves a higher presence of a gonopodium in males, a char- risk of predation for males. Moreover, Maya acteristic shared by all poeciliids (Rodriguez and Marañon (2001) under experimental con- 1977). Porthole livebearer females live longer ditions concluded that the highest tempera- and reach larges sizes than males, possibly ture alters the sex ratios, being 31°C the one because in general, females take a longer time that induced most proportion of males in the to mature and continue growing throughout native population of P. reticulata. In this study, their life. Males stop growing, or grow very monthly variations in the sex ratios could be little after the gonopodium has been completely explained too by the effect of the mesh size formed and they do not live as long after reach- and the shallowness of the lake, which make ing maturity (Snelson 1984, 1989). Reznick difficult the fish capture. (1983) point out that high growth rates favors Respect to the relationship between length the survival of young fishes because, if they and weight, Ricker (1975) mentioned that are bigger, then they can feed on a large range when the fishes have a coefficient b value of prey and successfully avoid predation, so significantly different from 3, growth is allo- decreasing their mortality rate. metric. This is the case of the present study Another aspect that could also have and therefore, it suggests that body parts do not some influence on survival is the size at first grow at a similar rate and then the fish grow reproduction, because males are precocious in length more than in weight. Similar results compared to females, which have a shorter have been found for others species such as P. growth period prior to maturation and there- sphenops (Martinez-Trujillo 1983), P. gracilis fore lower growth rates. Contreras-MacBeath (Contreras-MacBeath and Ramírez-Espinoza and Ramírez-Espinoza (1996) mentioned that 1996), bimaculata (Gómez- males take advantage of being precocious Márquez et al. 1999) and, reticulata and also prolong their reproductive life, while (Urriola Hernández et al. 2004a). females delay maturation but they are able to The porthole livebearer reaches sexual bear and nourish a greater number of larger maturity at a small size within its first year of embryos. life and is therefore able to begin to reproduce The sex ratio significantly female biased in October. Urriola et al. (2004a) found similar (1:2.3) was in accordance with what has results of sexual maturity for P. reticulata. The been found in other poeciliids species such reproductive cycle analysis showed that this as (1:5) (Martínez-Trujillo type of activity is present throughout the year. 1983) and holbrooki (1:4) and this With the gonadosomatic index and develop- is a well known feature occurring in sexually ment stages together, it is evident that peak dimorphic fishes, particularly those belonging reproduction occurs from July to October, to the Poeciliid family (Vargas and de Sostoa during the rainy season. Contreras-MacBeath 1996). Contrary to this, Urriola et al. (2004a) and Ramírez-Espinoza (1996) cited similar cited that the sex ratio for Poecilia reticula was information for the same species in Morelos significantly male biased. State, but at a different location. Burns (1985) Snelson (1989) mentioned that the pre- found that when P. gracilis was subject to long ponderance of females might be attributed to photoperiods, gonadosomatic index was high- the differential mortality of the sexes. Females est and therefore, reproduction occurred during have higher survivorship rates due to their summer and autumn months, when photope- larger sizes, longer lifespan, less conspicuous riod is longer. colors, and that they are more resistant to the The maximum condition value occurred rigors of reproductive effort and unfavorable in October coincides with rainy season when

1808 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 the reproductive period was highest. Condition of the spawning season. Schoenherr (1977) then diminished to December during a reduc- for P. occidentalis, Contreras-MacBeath and tion in the water temperature. Moreover, is Ramírez-Espinoza (1996) for P. gracilis and, possible than the combination of a lower con- Vargas and de Sostoa (1996) for Gambusia dition and a greater reproductive effort resulted holbrooki, obtained similar results. in a reduction of the individuals as is observed Schoenherr (1977) cited that temperature during this period. Furthermore, the decrease and day length both influence reproduction in in condition has been ascribed to a depletion of P. occidentalis and that probably is true that body reserves during gonad maturation. many parameters exert an influence, with one The relationship between fecundity with or other dominating in different populations or body size does not demonstrate a signifi- under differing circumstances. Perhaps, water cant correlation. Burns (1985) and Contreras- temperature does not vary and therefore, the MacBeath and Ramírez-Espinoza (1996) found fishes are responding to an increase in photope- similar results for superfetating poeciliids, in riod and that both factors show their influence which an increment in size is not necessarily not only in terms of the proportion of fishes associated with an increased embryos number. that carry broods, but also in brood size. Reznick and Miles (1989) mentioned that in Moreover, Burns (1985) mentioned that non-superfetating poeciliids there is an asso- slight photoperiod differences could affect the ciation between body size and fecundity as in reproductive capabilities of native fish from Poecilia reticulata (Thibault and Schultz 1977), tropical latitudes. Seasonal day length varia- P. turrubarensis (Cabrera and Solano, 1995), tions have been implicated in affecting the Heterandria bimaculata (Gómez-Márquez et observed annual fluctuations in brood size in a al. 1999) and, P. reticulata (Urriola Hernández number of poeciliids species studied (for exam- et al. 2004b). Miller (1975; cited in Burnes, ple, Poeciliopsis gracilis and Poecilia sphe- 1985) point out that superfetation is common in nops) in their natural environments, because Poeciliopsis and therefore, the embryos includ- each population may be able to express differ- ed in the fecundity estimate for a given female ent life history traits resulting in adaptations to were often in different development stages. In a particular environment. this study, 25 percent of females had several The breeding activity for most of poeciliid broods in the same reproductive season, which species increases during periods of intense means that porthole livebearer is one of the sunshine and/or rainfall. In this study, a major poeciliids that exhibit superfetation. Likewise, breeding peak of porthole livebearer is associ- Burns (1985) cited that for P. gracilis, approxi- ated with warm temperature, high rainfall and mately 25 percent of the females in each water level rising. The period with high values group showed superfetation and no significant of GSI for the fish is also the time of increase correlation between standard length and egg/ in phytoplankton biomass (chlorophyll a) at embryos number was seen for each group. In Coatetelco Lake. Phytoplankton biomass in this addition, Bagenal (1978) cited that fish species aquatic system increases following high nutri- exhibit wide fluctuations in fecundity among ent concentrations resulting from water mixing fish of the same species, size and age. and rainfall associated changes in the lake’s Probably, the reproductive cycle in the hydrology. This increase in phytoplankton bio- lake was primarily determinate by the tem- mass may play as one of the environmental cues perature, the seasonal fluctuations of photo- indicating an approaching season favorable for period, the rainy season (when the water is better growth and offspring survival, while the not totally transparent and the productivity is other environmental factors may have indirect high) and, the increased water level between effects. A similar conclusion can be drawn July and September, when nutrients for devel- also for O. niloticus in Lake Awassa studied opment are available, which affect the timing by Admassu (1996) and, for O. niloticus from

Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (4): 1801-1812, December 2008 1809 Emiliano Zapata dam (Peña-Mendoza et al., Palabras clave: clorofila “a”, índice gonadosomático, 2005). Nevertheless, a more detailed research índice hepatosomático, Poeciliopsis gracilis, reproducción, is required to investigate the effect of phyto- proporción sexual, México plankton at the time of breeding of P. gracilis in the lake or in other tropical aquatic systems. REFERENCE The information obtained suggests that a combination of life history traits, early matu- Admassu, D. 1996. The breeding season of tilapia, Oreochromis niloticus L. in Lake Awassa (Ethiopian rity, fast growth and reduced longevity enable rift valley). Hydrobiologia 337: 77-83. porthole livebearer to inhabit different areas and exploit favorable environmental condi- Anonymous. 1981. Síntesis Geográfica de Morelos. tions, as in Morelos State and other places. This Coordinación General de los Servicios Nacionales de Estadística, Geografía e Informática, S.P.P. D.F., explains why the Poeciliidae family is the most México. cultivated at the fish farms of the state mainly with Poecilia reticulata and P. sphenops as the Anonymous. 1998. Anuario Estadístico del Estado de most representative species. Morelos. Instituto Nacional de Estadística, Geografía e Informática. Aguascalientes, Ags. México.

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