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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.46 no.3 Valparaíso July 2018

http://dx.doi.org/10.3856/vol46-issue3-fulltext-2 

Research Article

Fecundity, egg volume and reproductive output of Macrobrachium tenellum (Crustacea: Palaemonidae) from the northern coast of Jalisco, Mexico

Manuel Alejandro Vargas-Ceballos1  2 

Ernesto López-Uriarte2 

Marcelo Ulises García-Guerrero3 

Ingo S. Wehrtmann4  5 

Eduardo Ríos-Jara3 

Fernando Vega-Villasante1 

1Laboratorio de Calidad de Agua y Acuicultura Experimental, Universidad de Guadalajara Puerto Vallarta, Jalisco, México

2Departamento de Ecología, Centro Universitario de Ciencias Biológicas y Agropecuarias Universidad de Guadalajara, Jalisco, México

3Instituto Politécnico Nacional CIIDIR-IPN, Oaxaca, Oaxaca, México

4Unidad de Investigación Pesquera y Acuicultura (UNIP), Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San José, Costa Rica

5Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica

ABSTRACT

Our knowledge of the reproductive biology of palaemonid shrimps is an important tool to assess potential candidates for aquaculture as well as being useful to develop adequate strategies for the conservation of the biodiversity. Here we analyzed the fecundity, volume and water content of the eggs, and the reproductive output (RO) of Macrobrachium tenellum in the Ameca River, Jalisco-Nayarit, Mexico. The total length of the females ranged from 26.6 to 67.0 mm (average 44.2 ± 8.8 mm) and fecundity (considering all stages) fluctuated between 253 and 10,384 eggs (average 2,418 ± 2,089 eggs). Females lost on average 26% of the initially produced eggs. The average egg length increased from 0.55 (recently produced eggs) to 0.66 mm (eggs close to hatching). The water content of eggs increased significantly during embryogenesis by 11.4%. The RO was not related to female length and fluctuated between 4.1 and 16.0%, which are values within the range reported for other decapods. The results of the current research contribute to laying the foundations for future studies that help to define strategies for the conservation and sustainable use of this crustacean.

Keywords: egg production; embryogenesis; freshwater shrimp; reproductive biology; egg loss; water content; Ameca River

INTRODUCTION

Aquaculture is an economic activity with great potential for food production under a sustainable scheme. A species with high potential for aquaculture should combine the following features: fast-growing, easy reproduction in captivity, high fecundity, low aggressiveness, and diseases resistance (Da Silva et al., 2004). One of such species combining these characteristics is Macrobrachium tenellum, locally known in Mexico as "manopalito", "chacal", "brazo largo", "popotillo," "langostino", among other names, depending on the region. This shrimp is of economic importance, and is target of the artisanal fishery in coastal cities and lagoons of Mexico, El Salvador and Guatemala (Cabrera-Peña, 1983). Information of the reproductive biology of palaemonid shrimps is an important tool to identify potential candidates for aquaculture; moreover, such information is required for the development of adequate management strategies of these decapods (Mossolin & Bueno, 2002). Therefore, fecundity studies are fundamental to assess the capacity of the use of (freshwater) shrimps as a sustainable living resource. Fecundity refers to the number of eggs produced in each spawning (Bertini & Baeza, 2014) or to the number of eggs carried by the female under the abdomen (Bond & Buckup, 1982; Valenti et al., 1989). Information about egg production permits not only to recognize the potential of each species to be cultivated on a commercial scale, but also allows to estimate the minimum number of adults needed to maintain wild populations (Valenti et al., 1989; Barros-Alves et al., 2012; Aya-Baquero & Velasco-Santamaría, 2013).

The estimation of the egg volume is important to understand the mechanisms of adaptation to the environment used by the different species (Hernáez & Palma, 2003). Macrobrachium species have different adaptations to the freshwater environment (Lara & Wehrtmann, 2009; Bauer, 2013): some species complete their entire life cycle in freshwater, producing a small number of eggs but of relatively large volume (Melo & Brossi-Garcia, 1999). Other species are dependent on brackish water and larvae require coastal waters to complete their life cycle (Gamba, 1982; Bauer, 2013). These species produce smaller eggs but in large quantity (Jalihal et al., 1993; Pereira & Garcia, 1995). The energy that the females allocated for reproduction can be estimated through the reproductive output (RO) (Hines, 1988, 1991, 1992). The common formula to measure reproductive output is: dry weight of the ovigerous mass divided by the dry weight of the female without eggs (López et al., 1997). In crustaceans, the energy investment made by the female may be affected by the loss of eggs during incubation caused by ecological, allometric and/or mechanical factors (Kuris, 1991; Oh & Hartnoll, 1999; Oyarzún et al., 2010).

In Mexico, the egg production of M. tenellum has been studied by Román-Contreras (1979) and Guzmán-Arroyo (1987); however, these studies did not assess the female energy investment per egg clutch. Therefore, the objective of the present investigation was to analyze aspects of the reproductive biology previous not studied (fecundity, egg volume, reproductive output) in M. tenellum in the Ameca River, Jalisco-Nayarit, Mexico.

MATERIALS AND METHODS

Shrimps were captured between February 2015 and January 2016 in four different collecting sites in the Ameca River: Boca, Las Juntas and San Juan (Fig. 1). Boca and Las Juntas sites are located closer to the river mouth (0 and 3 km from the river mouth, respectively), San Juan are situated upstream (23 km from the coast) (Fig. 1). In each locality, shrimps were collected on the riverbank, between the vegetation and roots of trees using an electrofishing equipment (Samus 725G) for 30 min. at each sampling point. After the sampling, organisms were placed individually in plastic bags and kept at a temperature of 0-5°C during the transportation to the Laboratory of Water Quality and Experimental Aquaculture (LACUIC) located in the University Centre of the Coast of the Guadalajara University. Once in the laboratory, the organisms were kept frozen until further analysis.

Figure 1 Location of the Ameca River sampling sites. The kilometer values refer to the distance from the river mouth. 

Collected organisms were identified according to Holthuis (1952) and Hendrickx (1995). Ovigerous females were selected and the following parameters were measured: 1) female overall length (from the posterior margin of the eye orbit until the distal extreme of the telson: TL; mm) with a digital vernier caliper (±0.01 mm), 2) female total weight (TW; g) using a digital balance Ohaus® (0.001 g), 3) total number of eggs present on the pleopods, 4) size, volume, water content of the egg, and 5) the reproductive output (RO).

To determine fecundity, the total egg mass of the female was detached carefully with the aid of dissection tweezers. Three subsamples (between 250 to 1000 eggs each) were taken, and eggs were counted in each of the subsamples with a stereomicroscope (AmScope®). The three subsamples along with the remaining eggs were dried in an oven at 60°C for 48 h. A digital balance (Ohaus®, 0.001g) was used to estimate dry weight. The average weight of each egg, and fecundity were calculated according to the following equations proposed by Hernáez & Wehrtmann (2011): (1) E = S/100 and (2) NE = WEM/E where E = egg weight, S = average weight of the subsamples; NE = total number of eggs; WEM = weight of the total egg mass. In this case, an adaptation was made since the utilized number of eggs was different. Thus the following formula was applied: E = S/N in which S = sample weight and N = number of eggs in the sample, in agreement with I. Wehrtmann (pers. comm.).

The developmental stage of the egg was determined according to the criteria proposed by Wehrtmann (1990): Stage I: rounded egg, uniform yolk and without visible eye pigments; Stage II: ovoid egg, elongated and barely visible eye pigment; and Stage III: ovoid egg, well-developed and intensely pigmented eyes; embryo with free abdomen. An analysis of covariance was applied (ANCOVA, P < 0.05) to the relationship between the number of eggs and the total length in Stage I and Stage III to rule out the possible influence of the stage of development in the number of eggs carried by female. Subsequently, a regression analysis was used to analyze the relationship between the number of eggs, TL and TW.

To determine the egg size, 20 eggs of each female were separated and digital photographs were taken; the length and width was measured with the software Image Tool version 3.0 (University of Texas, Health Science Center, San Antonio, Texas (http://compdent.uthscsa.edu/dig/itdesc.html). The egg volume was calculated with the formula V=1/6(a×b×π) proposed by Corey & Reid (1991), where a is the length and b the egg width in mm; π = 3.14. Average volume and standard deviation was calculated for each of the three stages. An ANOVA was applied (P < 0.05) to determine possible differences between stages. A linear regression model was used to represent the relationship between fecundity and female size (TL) for Stage I and III.

The estimation of the egg water content was obtained from the difference between wet and dry weight of the ovigerous mass. An ANOVA (P < 0.05) was applied to analyze differences between developmental stages. The RO was obtained by dividing the dry weight of the ovigerous mass by the dry weight of the female without eggs (López et al., 1997), taking into account all development stages. A linear regression was performed to determine the relationship between the RO and TL of the females.

RESULTS

A total of 92 M. tenellum ovigerous females were selected from the Ameca River (San Juan [18], Las Juntas [39] and Boca [35]) for the fecundity analysis. Taking into account all the localities, the size of females varied between 26.6 and 67.0 mm TL with an average of 44.2 ± 8.8 mm TL (Boca 42.0 ± 3.8 mm, Puente 41.7 ± 7.4, San Juan 48.8 ± 10.2 mm). The average weight was 2.1 ± 1.6 g and fluctuated between 0.4 and 6.5 g. The ANCOVA analysis showed no significant effect of the locality over the fecundity (F = 2.7, d.f. = 2, number of eggs P = 0.07) (Fig. 2); however, fecundity increased significantly with female TL (F = 101.2, d.f. = 1, P = < 0.0001). Considering all the localities, fecundity ranged from 253 to 10,384 eggs with an average of 2,418 ± 2,089 eggs.

Figure 2 Average fecundity (with standard deviation) of Macrobrachium tenellum between different sampling locations in the Ameca River, Jalisco-Nayarit, Mexico. 

The relationship between fecundity and female size showed a linear positive relationship in Stage I and II (Fig. 3). The number of eggs per ovigerous female decreased significantly with egg stage (ANCOVA, F = 7.63, d.f. = 1, P = 0.007). The Stage I and Stage III slopes were not significantly different (F = 0.24, d.f. = 1, P > 0.6). Calculations of estimated egg numbers in early and late stage of development suggest that the percentage of egg loss in M. tenellum is 26%.

The average egg length increased during the incubation period from of 0.55 (Stage I) to 0.66 mm (Stage III). Similarly, the egg volume showed significant differences (F = 4.04, d.f. = 2, P = 0.04) during embryonic development: 0.054 (Stage I) to 0.074 mm3 (Stage III), which represents a total increase of 37.9%. The water content of eggs (Table 1) increased significantly by 11.4% during embryogenesis (F = 7.66, d.f. = 2, P = 0.001). The RO was not related to female length (R = 0.00008). Females invested on average 8.5 ± 2.5% of their body weight in egg production, and this value varied between 4.1 and 16% (Fig. 4).

Table 1 Macrobrachium tenellum: water content percentage, volume and size of the different egg development stages (average, maximum and minimum as well as standard deviation values). 

Stage n Average ± SD Maximum Minimum
Water content %
I 6 78.1 ± 5.1 86.7 71.9
II 12 78.7 ± 3.7 83.8 70.5
III 35 82.8 ± 3.6 92.0 73.0
Volume (mm3)
I 18 0.054 ± 0.010 0.059 0.037
II 39 0.059 ± 0.009 0.068 0.049
III 35 0.074 ± 0.012 0.087 0.056
Length (mm)
I 18 0.553 ± 0.034 0.585 0.500
II 39 0.590 ± 0.033 0.640 0.531
III 35 0.667 ± 0.050 0.707 0.610

Figure 3 Macrobrachium tenellum: relationship between a) total length and b) total weight versus number of eggs (black circles indicate Stage I and white circles refer to Stage III). 

Figure 4 Relationship between total length (mm) and females reproductive outputs of Macrobrachium tenellum, considering all stages of development. 

DISCUSSION

Numerous studies revealed that fecundity in decapods is closely related to female size (e.g., Antezana et al., 1965; Corey & Reid, 1991; Echeverría-Sáenz & Wehrtmann, 2011). This pattern is related to the fact that large-sized females have larger ovaries than smaller individuals of the same species, which allows them to produce and carry more eggs. Our results are in accordance with this general trend: larger and heavier M. tenellum females produced significantly more eggs than smaller ones (Fig. 2). Similar results have been obtained from other Macrobrachium species: M. acanthurus (Anger & Moreira, 1998; Tamburus et al., 2012), M. amazonicum (Da Silva et al., 2004; Parra-Medina et al., 2008; Aya-Baquero & VelascoSantamaría, 2013), M. carcinus (Graziani et al., 1993; Lara & Wehrtmann, 2009), M. heterochirus (Ching & Velez, 1985) and M. olfersii (Anger & Moreira, 1998).

The relationship between female size and fecundity has been described usually by linear regressions, although in some cases an exponential or potential function was used to describe this relationship (Sutcliffe, 1993; Hernáez & Palma, 2003). In the present study, M. tenellum fecundity increased linearly with female size, corroborating similar results reported by Gutiérrez-Jara (2010) for the same species. Similarly, such a positive linear relationship has been described also for M. acanthurus (Valenti et al., 1989; Albertoni et al., 2002; Tamburus et al., 2012), M. amazonicum (Da Silva et al., 2004; Aya-Baquero & Velasco-Santamaría, 2013; Lima et al., 2014), M. carcinus (Lobão et al., 1985; Lara & Wehrtmann, 2009), M. heterochirus (Ching & Velez, 1985), and M. olfersii (Ammar et al., 2001; Mossolin & Bueno, 2002). However, an exponential model was used to describe the relationship between the number of eggs and females size of the following Macrobrachium species: M. rosenbergii (Rajyalakshmi, 1961), M. carcinus (Pérez & Segura, 1981; Mejía-Ortiz et al., 2001), M. acanthurus (Pérez & Segura, 1981; Mejía-Ortiz et al., 2001), and M. heterochirus (Mejía-Ortiz et al., 2001). Finally, other authors mentioned that a potential model provided the best fit for this relation in M. acanthurus (Anger & Moreira, 1998), M. amazonicum (Hayd & Anger, 2013), and M. olfersii (Anger & Moreira, 1998). According to Lara & Wehrtmann (2009), the relationship between fecundity and female size in species of the genus Macrobrachium should be analyzed and described separately for each species to assess which model described best this relation.

The fecundity range estimated in this study for M. tenellum is comparable to that reported for the same species by Román-Contreras (1979) and Guzmán-Arroyo (1987) (Table 2). Nevertheless, the range of fecundity in the present study were higher than those mentioned by Signoret & Brailovsky (2002) for M. tenellum collected in the Coyuca de Benitez Lagoon in Guerrero, Mexico. Moreover, Gutiérrez-Jara (2010) reported a higher fecundity of M. tenellum in Costa Rica compared to the present data; this difference may be due to the fact that the study by Gutiérrez-Jara (2010) included larger females when compared to our study. The number of eggs obtained in the present study for M. tenellum was lower than in other larger species of the same genus, such as M. americanum (Smitherman et al., 1974; Gutiérrez-Jara, 2010), M. carcinus (Lara & Wehrtmann, 2009), or M. rosenbergii (Habashy, 2010) (Table 2). These results reveal that fecundity in Macrobrachium species is highly variable and strongly related to female size.

Table 2 Fecundity (number of eggs per female) of different Macrobrachium species (n: number of females, TL: total length; maximum and minimum values are indicated in parenthesis). 

Species n TL mm
Mean (max-min)
Fecundity
Mean (max-min)
Reference
M. acanthurus 87 (60.0 - 135.9) 8,929 (740 - 17,769) Valenti et al. (1989)
29 10.7 - 53.5) (440 - 3042) Anger & Moreira (1998)
36 71.1 (42.9 - 110.4) 1,886 (113 - 5568) Mejía-Ortiz et al. (2001)
M. amazonicum 46 (38 - 67) (178 - 1344) Lobão et al. (1986)
32 (7 - 21)* (150 - 2165) Odinetz Collart (1991)
60 (50 - 100) (480 - 2128) Da Silva et al. (2004)
246 (7.6 - 19.5)* 211 (16 - 1630) Hattori et al. (2009)
19 17.2* 2,237 (1341 - 2956) Meireles et al. (2013)
M. americanum 34.1 (33.9 - 60.8)* 76,900 (17942 - 124057) Gutiérrez-Jara (2010)
M. carcinus 41 (100 - 220) 53,764 (6350 - 194,350) Lobão et al. (1985)
16 90.9 (46.4 - 127.7) 7,892 (502 - 23,852) Mejía-Ortiz et al. (2001)
35 161.2 (120.0 - 190.0) 98,749 (14,420 - 242,437) Lara & Wehrtmann (2009)
M. heterochirus 34 71.8 (51.7 - 153.1) 3659 (293 - 28,512) Mejía-Ortiz et al. (2001)
50 (18 - 61) 1788 (184 - 5031) Ching & Velez (1985)
M. rosenbergii 20 25, 083 Graziani et al. (2003)
M. tenellum (68 - 7) (2,288 - 11,102) Guzmán-Arroyo (1987)
43 (56 - 101) (900 - 10,800) Román-Contreras (1979)
38.0 (67 - 80) 984 (900 - 1,200) Signoret & Brailovsky (2002)
15 32* 15,315 Gutiérrez-Jara (2010)
92 44.2 (26.6 - 67.0) 2,418 (253 - 10,384) Present study

*Carapace length

Inter- and intraspecific differences in the egg production of decapods are not only influenced by size differences (Ching & Velez, 1985; Da Silva et al., 2004), but also by temperature, quality and quantity of food, which may vary within the latitudinal range of the species´ distribution (Odinetz-Collart & Rabelo, 1996; Fransozo et al., 2004). Similarly, Mashiko (1990, 1992) indicated that the egg number could vary within a river system with the distance from the coast.

Some studies estimated the production of eggs, considering all embryonic stages (e.g., Walker & Ferreira, 1985; Mejía-Ortiz et al., 2001; Albertoni et al., 2002; Antunes & Oshiro, 2004). Other studies reported only the number of recently extruded eggs to exclude possible egg loss during embryonic development, caused by infections, parasites, poor water quality, predation or constant friction with the bottom (e.g., Lara & Wehrtmann, 2009; Tamburus et al., 2012; Meireles et al., 2013; Bertini & Baeza, 2014). Our results revealed an egg loss of 26% during the embryogenesis of M. tenellum, which is within the range reported for other Macrobrachium species (10-46%): M. rosenbergii 30% (Wickins & Beard, 1974), M. nobilii 46% (Balasundaram & Pandian, 1982), M. acanthurus 23% (Anger & Moreira, 1998; Bertini & Baeza, 2014), and M. lanchesteri 20% (Phone et al., 2005). Egg loss in M. tenellum may be explained by the egg volume increase during the incubation period (Bertini & Baeza, 2014), thus probably outgrowing the available physical space of the abdominal chamber. The increase of the egg volume is a common pattern in crustaceans (Zhao et al., 2007) and is the result of a gradual water intake during the incubation period (Lardies & Wehrtmann, 1997; Müller et al., 2004) and/or the retention of metabolic water product of respiration (Anger et al., 2002). In the present study, the eggs of M. tenellum showed an average egg volume increase of 37.0% during embryogenesis, similar to the results of Gutiérrez-Jara (2010) working with the same species. Likewise, similar results have been reported for other species of the same genus (Table 3). The increase in the egg volume in the Macrobrachium species seems to be independent to the size of the females (Lara & Wehrtmann, 2009; Tamburus et al., 2012).

Table 3 Increase egg volume and reproductive output (RO) of different Macrobrachium species. 

Species Increase egg volume (%) RO (%) mean (min-max) Reference
M. acanthurus 38.0 Tamburus et al. (2012)
19.0 (14.0 - 30.0) Anger & Moreira (1998)
M. amazonicum 33.4 Odinetz-Collart & Rabelo (1996)
11.7 (4.8 - 21.8) Lima et al. (2014)
M. carcinus 35.4 12.0 (4.0 - 21.0) Lara & Wehrtmann (2009)
M. hainananse 10.0 (4.0 - 17.0) Mantel & Dudgeon (2005)
M. olfersii 30.7 Mossolin & Bueno (2002)
22.0 (7.0 - 38.0) Anger & Moreira (1998)
M. potiuna 28.0 Nazari et al. (2003)
M. vollenhovenii 58.5 Oben et al. (2015)
M. surinamicum 4.3 - 35.5 Lima et al. (2015)
36.0 18.5 (3.1 - 49.4) Gutiérrez-Jara (2010)
M. tenellum 37.0 8.5 (4.1 - 16) Present study

The size (length) of the egg in M. tenellum increased from 0.55 to 0.66 (Table 1), and these values are in the range reported for other Macrobrachium species, which require estuarine environments to complete its reproductive cycle (M. carcinus, M. olfersii, M acanthurus, and M. ohione (Lara & Wehrtmann, 2009).

The water content of M. tenellum eggs increased during the embryogenesis on average by 11.4% (from 78.1% in Stage I to 82.8% in Stage III), a value similar to that reported by Lara & Wehrtmann (2009) for M. carcinus (15.8%). According to Pandian (1970), the egg water content of marine benthic decapods with planktonic larval development increases from 50-60% in recently extruded eggs to 70-80% at the end of the incubation period (Pandian, 1970). Lara & Wehrtmann (2009), studying M. carcinus, suggested that the pattern proposed by Pandian (1970) might be also valid for freshwater shrimps with planktonic larval development. This assumption is further supported by similar values of water content in eggs of Atya scabra (60.0-82.6%; Herrera-Correal et al., 2013).

The energy that females invest in reproductive processes is one of the most interesting factors on the reproductive biology of crustaceans (Hernáez & Palma, 2003). Females of M. tenellum allocate between 4.1 to 16% (average 8.5 ± 2.5%) of the body weight in egg production. For the same species, Gutiérrez-Jara (2010) mentioned values ranging from 3.1 to 49.4% (average 18.5%). These results are in the range reported for other species of the same genus (Table 3). Just as in other Macrobrachium species (e.g., Mantel & Dudgeon, 2005; Lara & Wehrtmann, 2009; Lima et al., 2014, 2015), the RO of M. tenellum was not size-related.

The results of the current research contribute to laying the foundations for future studies that help to define strategies for the conservation and sustainable use of this crustacean with ecological as well as economic and social importance.

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Received: April 07, 2017; Accepted: October 17, 2017

Corresponding author: Marcelo Ulises García Guerrero (mgarciagu@ipn.mx)

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