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Brazilian Journal of Oceanography

Print version ISSN 1679-8759On-line version ISSN 1982-436X

Braz. j. oceanogr. vol.63 no.3 São Paulo July/Sept. 2015

http://dx.doi.org/10.1590/S1679-87592015085806303 

Original Article

The reproductive performance of the Red-Algae shrimp Leander paulensis (Ortmann, 1897) (Decapoda, Palaemonidae) and the effect of post-spawning female weight gain on weight-dependent parameters

Uwe Zimmermann1  2 

Fabrício Lopes Carvalho2  3 

Fernando L. Mantelatto2  * 

1Eberhard Karls-University Tübingen, Faculty of Science, Department of Biology (Auf der Morgenstelle 28, 72076 Tübingen, Germany)

2Universidade de São Paulo (USP), Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP), Departamento de Biologia, Laboratório de Bioecologia e Sistemática de Crustáceos (LBSC) (Av. Bandeirantes, 3900, Ribeirão Preto, 14040-901, São Paulo, Brazil)

3Universidade Federal do Sul da Bahia (UFSB), Instituto de Humanidades, Artes e Ciências Jorge Amado (IHAC-JA) (Rod. Ilhéus-Vitória da Conquista, km 39, BR 415, 45613-204, Ferradas, Itabuna, Bahia, Brazil)

Abstract

Decapod species have evolved with a variety of reproductive strategies. In this study reproductive features of the palaemonid shrimp Leander paulensiswere investigated. Individuals were collected in the coastal region of Ubatuba, São Paulo, Brazil. In all, 46 ovigerous females were examined in terms of the following reproductive traits: fecundity, reproductive output, brood loss and egg volume. Leander paulensis produces a large number of small eggs with an average fecundity of 635 ± 246 eggs. Egg volume increased significantly from early (0.034 ± 0.008 mm3) to late development stage (0.05 ± 0.012 mm3). The reproductive output did not correlate with female size. The weight of females bearing stage 2 eggs was significantly higher than that of females carrying stage 1 eggs. We assume that the reason for this weight gain is the recovery of female reserves that have been depleted for egg production. Moreover, we emphasize that this weight gain must be considered when evaluating weight-dependent variables such as reproductive output or brood loss in relation to female weight. Otherwise, an overestimation of these variables might lead to inaccurate results.

Descriptors: Brood loss; Caridea; Egg volume; Fecundity; Reproductive output

Resumo

Decápodes desenvolveram uma ampla variedade de estratégias reprodutivas. Neste estudo foram investigadas características reprodutivas da espécie de PalaemonidaeLeander paulensis. Os indivíduos foram coletados na região costeira de Ubatuba, São Paulo, Brasil. Foram examinadas 46 fêmeas ovígeras quanto aos seguintes aspectos reprodutivos: fecundidade, investimento reprodutivo, perda de ovos e volume dos ovos. Leander paulensis produz uma grande quantidade de pequenos ovos, com fecundidade média de 635 ± 246 ovos. O volume dos ovos aumentou significativamente quando comparado o estágio inicial (0.034 ± 0.008 mm3) com o estágio final de desenvolvimento (0.05 ± correlação com o tamanho das fêmeas. Fêmeas com ovos no estágio 2 apresentaram massa corpórea seca significativamente maior que aquelas carregando ovos no estágio inicial. Esse aumento de massa parece ser decorrente da recuperação de reservas energéticas das fêmeas, que teriam sido utilizadas durante a produção de ovos. Além disso, deve-se considerar neste tipo de avaliação o aumento da massa corpórea em relação ao investimento reprodutivo, assim como da perda de ovos relacionada à massa das fêmeas ou qualquer outra variável dependente do peso.

Descritores: Fecundidade; Caridea; Perda de ovos; Volume de ovos; Investimento reprodutivo

INTRODUCTION

There are many reproductive strategies among decapods, and these manifest as differences in parameters such as fecundity and breeding frequency, which are directly related to the species’life strategy (OH; HARTNOLL, 2004). Caridean shrimps are not an exception to this scenario, with some species, such as Macrobrachium potiuna (NAZARI et al., 2003) and Synalpheus pectiniger (COREY; REID, 1991), producing few but larger eggs, and others, such as Macrobrachium olfersii and Pontonia margarita, carrying a great number of relatively small eggs (COREY; REID, 1991). Differences in reproductive strategies can also occur intraspecifically, depending on environmental factors such as salinity (JANAS; MAŃKUCKA, 2010) or temperature and season (BODDEKE, 1982; OH; HARTNOLL, 2004). Other examples and variations among these genera and congeners are discussed in PAVANELLI et al. (2008) and TAMBURUS et al. (2012).

The genus Leander DESMAREST, 1849, is composed of five species distributed in different regions (DE GRAVE; FRANSEN, 2011). Leander paulensis ORTMANN, 1897, is a small shrimp that occurs in shallow marine waters of the western Atlantic from Florida, USA to Paraná, Brazil (CARVALHO et al., 2014). It inhabits sand and rock bottoms with algae up to a depth of 16 m (RAMOS-PORTO, 1986). Studies regarding L. paulensishave focused on the composition of crustacean fauna of certain areas (COSTA et al., 2000; COELHO et al., 2006; ALMEIDA et al., 2006, 2007a, b; MCCARTHY et al., 2012), taxonomy and geographical distribution (MANNING, 1961; RAMOS PORTO, 1986; ABELE; KIM, 1989; RAMOS-PORTO; COELHO, 1998; CARVALHO et al., 2014). Some ecological features, such as reproductive period, fecundity, egg volume and brood volume (BAUER, 1989, 1991; COREY; REID, 1991), have been addressed in the congeneric species Leander tenuicornis. However, Leander paulensis remains completely unknown in terms of its reproductive strategy. Considering that fecundity is an expressive measure of reproductive potential and contributes to the understanding of reproductive performance, the aim of the present paper is to analyze female weight gain during egg incubation, fecundity and investment per reproductive event in Leander paulensis.

MATERIAL AND METHODS

All specimens were collected in April 2013 at Lamberto beach (23º29′56″S, 45º07′04″W), a protected area that lies in the sheltered Flamengo bay, south of Ubatuba, São Paulo State, Brazil (Figure 1). In total, 46 ovigerous females were captured using a hand push net at a depth of 0.5 to 1 m and were identified according to Ramos-Porto (1986). All specimens were kept in 80% ethanol for the duration of the study.

Figure 1 Location of the sampling site in the Flamengo Bay in the southern region of Ubatuba, State of São Paulo, Brazil. 

Eggs of all females were gently removed, using fine forceps under a Leica® stereomicroscope M205C. The measurement of eggs and females, and the counting and classification of eggs, were performed under the stereomicroscope with the aid of the Leica Application Suite® (v 3.8.0). Female carapace length was measured from the post-orbital margin to the posterior border of the carapace. Eggs were counted and classified into two stages: stage 1 (early development) without eyespots and stage 2 (late development) with visible eyespots (COREY; REID, 1991). Ten eggs from each female were randomly chosen for measurement of their major and minor axis and the volume of each egg was quantified using the volume formula of oblate spheroids (cf. TURNER; LAWRENCE, 1979): EV = 4/3 * π * EL/2 * (EW/2)2, where EV = egg volume, EL = egg length and EW = egg width. For fecundity estimation, an ANCOVA was performed to check whether there is a loss of eggs from stage 1 to stage 2. As the results showed no significant difference (see results section), eggs of all 46 females were considered, regardless of their stage. Fecundity was thus determined as the total number of eggs attached to the abdomen of each female.

Egg samples and females were weighed separately. Female weight was quantified after removing all the eggs from the female’s abdomen. All weight measures were dry weight values and were quantified after 48 hours of oven drying at 50º C (Fanem oven model 315 SE). Brood weight was determined as the total weight of the entire egg batch. The reproductive output (RO) was estimated for one single spawning event (one brood) and is therefore defined herein as investment per reproductive event. To determine the reproductive output of each female, brood dry weight was divided by the females’ dry weight. An ANCOVA was performed to check whether reproductive output differed between females of stage 1 and females of stage 2 eggs. As the reproductive output was significantly lower for females carrying stage 2 eggs (see results section), only females carrying stage 1 eggs were used to determine the reproductive investment. Additionally, differences in female weight between individuals of stage 1 and 2 were tested by performing ANCOVA.

The Akaike Information Criterion (AIC) was used to choose the simplest model of ANCOVA that could be used (with or without interaction). All ANCOVA were performed with sum of squares type III, having carapace length as the covariate. The variables were linearized (ln) for all ANCOVA. A Student’s t-test was performed to verify whether there is any difference between the volume of eggs in stage 1 and stage 2. A linear regression analysis was conducted to check for a relationship between the reproductive output and carapace length of females. Power regression and the coefficient of determination were obtained and displayed whenever a significant correlation was observed.

The significance level of 0.05 was adopted for all analyses. The results are displayed as the mean ± standard deviation. All statistical analyses were performed using the R program version 3.0.1 (car package) (FOX; WEISBERG, 2011).

RESULTS

Female size and weight

Carapace length varied from 4.27 mm to 6.92 mm (mean 5.50 ± 0.63 mm). Female weight varied from 16.3 mg to 67.6 mg (39.55 ± 13.06 mg) for stage 1 and from 21.3 mg to 81.8 mg (50.99 ± 18.70 mg) for stage 2. The mean female weight of both stages combined was 42.96 mg (± 15.66). Females of stage 2 eggs were significantly heavier than females of stage 1 eggs (F = 36.4, d.f. = 1, 43, p < 0.01). The carapace length vs. weight relationship was described by a power function (Figure 2). The equation for stage 1 was FW = 0.2178 * CL3.0407(R2 = 0.859) and FW = 0.3986 * CL2.8062 (R2 = 0.945) for stage 2, where FW = female weight and CL = carapace length.

Figure 2 Power function of female weight and carapace length. The weight of females with stage 2 eggs is significantly higher than the weight of females with stage 1 eggs (F = 36.4, d.f. = 1, 43, p > 0.01). Female weight does not include egg weight. FW = female weight; CL = carapace length. 

Fecundity

Of the 46 females examined, 32 females carried eggs of stage 1 and 14 carried eggs of stage 2. Fecundity showed a strong correlation with carapace length which could be described by a power function (Figure 3). There was no significant difference in the number of eggs between stages 1 and 2 (F = 0.32, d.f. = 1, 43, p = 0.58). The number of eggs ranged from 227 (smallest female, CL = 4.27 mm) to 1360 (largest female, CL = 6.92 mm) averaging 635 ± 246 eggs. The power regression equation representing the data of both egg stages is FW = 2.5857 * CL3.1997 (R2 = 0.8922), where F = fecundity (number of eggs) and CL = carapace length (mm).

Figure 3 Fecundity in relation to carapace length. A power regression is applied to the individuals of both egg stages combined. The number of eggs does not vary significantly from stage 1 to 2 (F = 0.32, d.f. = 1, 43, p = 0.58). F = fecundity; CL = carapace length. 

Egg volume

The mean egg volumes of stages 1 and 2 were 0.034 mm3 (± 0.008) and 0.050 mm3 (± 0.012), respectively, with volume values ranging from 0.013 to 0.055 mm3 for stage 1 and from 0.018 to 0.076 mm3 for stage 2. There was a significant increase in egg volume from stage 1 to stage 2 (t = 16.3, d.f. = 458, p < 0.01) (Figure 4). The outlier in stage 2 is from a female whose eggs were poorly developed and small, although eyespots were visible.

Figure 4 Boxplot of egg volume at stage 1 and 2. The egg volume of stage 2 eggs is significantly higher than that of stage 1 eggs (t = 16.3, d.f. = 458, p > 0.01). 

Reproductive output

As the reproductive output was significantly lower for females bearing stage 2 eggs (F = 7.28, d.f. = 1, 43, p < 0.01), only females carrying stage 1 eggs were used to calculate the reproductive investment. The values of reproductive output per reproductive event ranged from 4.8% (CL = 4.94 mm) to 28.5% (CL = 4.86 mm) of egg weight relative to female weight (Figure 5). The mean value was 14.2 ± 5.4%. A linear regression test showed no significant relationship between the reproductive output and carapace length (F = 1.75, d.f = 44, p = 0.19), which indicates that the reproductive output does not depend on female size in this species.

Figure 5 Reproductive output and carapace length of females carrying eggs at stage 1. No significant relationship could be detected (F = 1.75, d.f. = 44, p = 0.19). 

DISCUSSION

Female weight gain during incubation

Females carrying stage 2 eggs exhibit a significantly higher weight than those carrying stage 1 eggs. To the best of our knowledge, this aspect has never been shown in caridean species. In terms of energy (i.e. nutritional resources), spawning is very costly and uses up accumulated reserves. At the beginning of the incubation period, females have a lower weight as nutritional reserves were invested into egg production. During egg incubation and maturation weight is regained as food intake is used to build up new reserves. Moreover, females may rebuild their gonads after spawning, which additionally increases female weight. However, gonad recovery has not been analyzed in this study.

The weight gain of females during egg incubation must be considered when evaluating weight-specific variables, such as the reproductive output or egg loss. According to ANGER; MOREIRA (1998), egg loss can be estimated measuring both size and weight-specific fecundity. However, our data reveal that a weight-specific estimation of fecundity might give inaccurate results. An increase in female weight might lead to an overestimation of brood loss when regressing fecundity on female weight. Female size is less likely to change during the incubation period. Therefore, our recommendation is to analyze brood loss rather by size-specific than weight-specific fecundity.

Similar consideration is needed for the analysis of the reproductive output, since it is calculated by measuring the weight of eggs and females. Therefore, one should either rule out a weight change for females during the incubation period or consider only females of an early developmental egg stage. In our study the reproductive output was significantly lower for females bearing eggs of stage 2. This reduction, however, cannot be explained by egg loss but is due to an increase of female weight. Thus, our results strongly recommend an estimation of reproductive output at an early stage of egg development. With proceeding, egg maturation females are more likely to have gained weight. This weight increase could give lower results for the reproductive output than if it was measured at early egg stage. If and how much female weight increases during egg incubation depends on the amount of food uptake. Variation in the degree of weight gain therefore underlies variation in the extent of feeding during egg incubation. If a female weight increase cannot be ruled out, we suggest quantifying exclusively the reproductive output of females with eggs of early developmental stages. To our knowledge, no further information on the effect of post-spawning female weight gain is available in the literature. Therefore, we strongly recommend this approach in future studies with other members of this group.

Fecundity

Fecundity and carapace length show a strong positive correlation as has been recorded for many decapod crustacean species (REID; COREY, 1991a, b). The same relationship is found in the congener Leander tenuicornis (COREY; REID, 1991) and other palaemonid shrimps (ALBERTONI et al., 2002; DA SILVA et al., 2004; BILGIN; SAMSUN, 2006; TAMBURUS et al., 2012). Although female size is likely to be the principal factor determining the fecundity of a species, other factors, such as latitudinal distribution, adaptation to habitat and season may influence fecundity as well (BODDEKE, 1982; MANTELATTO; FRANSOZO, 1997). Additionally, various biological variables, such as pleopod size in relation to body size, the number of spawns in a single reproductive period, egg mortality, and food availability may also affect fecundity (ANNALA, 1991; OH et al., 2002).

Fecundity data on a member of the genus Leander has been published by BAUER (1991) and COREY and REID (1991) for Leander tenuicornis. The mean fecundity of L. tenuicornis found by COREY and REID (1991) in East Florida/USA (28º31’N, 80º45’W) amounts to 452 eggs per female, ranging from 181 to 640 eggs. BAUER (1991) obtained a somewhat higher fecundity on the north coast of Puerto Rico (18º29’N, 66º15’W) averaging 593 ± 311 eggs. Compared to these results, Leander paulensis from Ubatuba (23º29′S, 45º07′W) achieves a slightly higher fecundity than its congener (635 ± 246 eggs ranging from 227 to 1360). Carapace length by both authors is very similar (BAUER, 1991: 6.7 mm; COREY; REID, 1991: 6.42 mm) and is therefore slightly higher than the mean carapace length of L. paulensis in this study (5.50 ± 0.63 mm, ranging from 4.27 to 6.92 mm), which still permits a fecundity comparison of both species. Other palaemonids of similar size, such as Palaemonetes pugio (110 eggs ranging from 53 to 189) and Palaemon mundusnovus (former Palaemonetes intermedius) (105 eggs ranging from 52 to 168) also laid fewer eggs than L. paulensis (COREY; REID, 1991).

Brood loss is a life-history parameter playing an important role when determining fecundity per spawning event (ANGER; MOREIRA, 1998). In this study, no significant loss of eggs was observed during the spawning period examined. Similar results were found for Macrobrachium acanthurus and Palaemon carinicauda (former Exopalaemon carinicauda) (OH; KIM, 2008; TAMBURUS et al., 2012). Tamburus et al. (2012) conjectured an efficient parental care strategy to reduce the most common causes of egg loss. Contrary to these findings, many other studies have found a significant reduction of fecundity in other palaemonid species. ANGER and MOREIRA (1998) calculated a maximum loss of eggs of 23% in Palaemon pandaliformis and Macrobrachium acanthurus. A brood loss of 38% was estimated for Palaemon serratus by REEVE (1969) and 15-33% for Palaemon modestus(former Exopalaemon modestus) by OH et al. (2002). NAZARI et al. (2003)studied two freshwater prawns, Macrobrachium potiuna and M. olfersii, and stated that the egg loss could result in a better accommodation of the eggs in the brood pouch and, therefore, a greater circulation and better supply of oxygen. Other factors causing this loss may be mechanical stress, increase in egg volume during incubation, abrasion by the ventilatory movements of the pleopods or any intrinsic or extrinsic change during incubation period (BALASUNDARAM; PANDIAN, 1982; KURIS, 1991). Parasites can also affect brood mortality as shown by KURIS and WICKHAM (1987)for some brachyuran crabs. It is possible that disturbances such as mechanical stress are lower for the area or time period where L. paulensis females were collected since the sampling site was inside a sheltered bay. However, mechanical stress could not be controlled for in this study since collecting took place at one single sampling site and during one single spawning event. Likewise, the absence of egg loss in this study could be explained by more intensive brood care as was suggested for Macrobrachium acanthurus by TAMBURUS et al. (2012).

Egg volume

Egg volume increases significantly during egg development from stage 1 to stage 2. An increase in size during egg development is a common feature among crustaceans (DAVIS, 1965, 1966; PANDIAN, 1970; WEAR, 1974; MORAIS et al., 2002; NAZARI et al., 2003; ZHAO et al., 2007). Most authors relate this increase mainly to osmotic water uptake through the egg membrane (DAVIS, 1965; 1966; PANDIAN, 1970; WEHRTMANN; KATTNER, 1998; NAZARI et al., 2003; ZHAO et al., 2007). Moreover, AMSLER and GEORGE (1984) discussed metabolic water as a by-product of respiration as an additional factor.

Data on egg size of a species of the genus Leander has been published by COREY and REID (1991) and BAUER (1991) for Leander tenuicornis. For calculation of egg volume, Corey and Reid (1991) applied the formula EV = EL * π * (EW/2)2 differing from the formula of oblate spheroids used by BAUER (1991) and in this study: EV = 4/3 * π * EL/2 * (EW/2)2 with EV = egg volume, EL = egg length and EW = egg width. The results of the two formulas differ by the factor 1.5. To compare the egg volume data of the present study to both studies on Leander tenuicornis, egg volume values of L. tenuicornispublished by COREY and REID (1991) were transformed by dividing them by 1.5.

Results on Leander tenuicornis by BAUER (1991) and COREY and REID (1991) differ to some extent. The mean egg volume obtained by Bauer (1991) (0.028 and 0.033 mm3 for first and second egg stage, respectively; both stages without visible eyespots) on the north coast of Puerto Rico (18º29’N, 66º15’W) is about a third of that found by COREY and REID (1991) (0.109 mm3) in East Florida/USA (28º31’N, 80º45’W). An overview of egg volume, fecundity and carapace length of L. tenuicornis and L. paulensis is given in Table 1. Eggs of Leander paulensis (0.034 mm3) are much smaller than those of L. tenuicornis from a mangrove ecosystem in Florida. However, they are about the same size as eggs of L. tenuicornis from seagrass meadows in Puerto Rico. This not only implicates ecological and latitudinal factors accounting for differences between the species, but also reveals strong intraspecific variation in egg size of L. tenuicornis, changing with latitude and habitat. Fecundity of L. paulensis also resembles that of L. tenuicornis from Puerto Rico, however it differs from that found in Florida.

Table 1 Comparison of fecundity, egg volume (mm3) and female size (carapace length in mm) of Leander tenuicornis and L. paulensis. The values of egg volume by Bauer (1991) are means of first and second egg stage, both without visible eyespot. The egg volume data of Corey and Reid (1991) was adjusted by the factor 1.5 to the volume formula applied by Bauer (1991) and in this study. For the egg volume of L. paulensis only stage 1 eggs were used in this comparison. 

Species Mean fecundity ± SD (min. - max.) Mean egg volume (mm3) ± SD (min. - max.) Carapace length (mm) ± SD (min. - max.) Reference
L. tenuicornis 452 (181-640) 0.109 6.42 (5.20-7.52) Corey and Reid (1991)
593 ± 311 0.028 - 0.033 6.7 ± 1.0 Bauer (1991)
L. paulensis 635 ± 246 0.034 ± 0.008 5.50 ± 0.63 present study
(227-1360) (0.013-0.055) (4.27-6.92)

These results indicate that Leander tenuicornis may pursue different reproductive strategies in different localities. Moreover, L. paulensis and L. tenuicornis from Florida differ strongly in their reproductive traits. L. paulensis produces more but smaller eggs, whereas fecundity of L. tenuicornis is lower but egg volume is comparatively high. However, compared to L. tenuicornis from Puerto Rico, reproductive traits are very similar, implying a similar reproductive strategy, i.e. many small instead of few larger eggs.

Studies comparing different species of marine invertebrates have revealed that egg size represents an energy investment on the part of females, as larger eggs contain a higher amount of yolk (SHAKUNTALA; REDDY, 1982; MCCLINTOCK; PEARSE, 1986; CLARKE; GORE, 1993; MCEDWARD; MORGAN, 2001). This model is strongly confirmed and accounts for interspecific variation in egg size (CLARKE, 1993a). Egg size strongly influences the developing rate and the hatching size of larvae or juveniles. Larger eggs generally produce larger offspring, which may be better prepared for competition (SASTRY, 1983). Egg size is an adaptive factor for different habitat conditions, such as temperature, salinity, food supply or predation (SASTRY, 1983; MASHIKO, 1990; CLARKE, 1993b). In this context, latitudinal differences also play an important role. Several of the mentioned features presumably account for differences in fecundity and egg size of L. tenuicornis from Florida and L. paulensis. The little data available on the fecundity of the genus, however, do not permit a consistent evaluation of this trait for this taxon; populations of these species in other areas should be studied to construct a more comprehensive scenario regarding reproductive performance.

Reproductive output

The reproductive output of Leander paulensis shows no significant correlation with female carapace length. The absence of a significant relationship between size and reproductive output has been reported for other species of palaemonids (ANGER; MOREIRA, 1998; MANTEL; DUDGEON, 2005; LARA; WEHRTMANN, 2009), which suggests that this feature may be common in the family. CLARKE et al. (1991)found site-to-site variation for Pandalus borealis showing no significant relationships of reproductive output to female body size in four of six sample localities. Another intraspecific study of two populations of Macrobrachium amazonicum, depicted a higher reproductive output in an inland compared to a coastal population (MEIRELES et al., 2013).

Seasonal variation of reproductive output was shown for Crangon crangon by OH and HARTNOLL (2004)and two amphipods, Gammarus oceanicus and Echinogammarus marinus, by CLARKE et al. (1985). In the latter study, egg size of both species decreased, whereas overall investment increased as the breeding season proceeded. These results point to a great variety of factors influencing the reproductive output of caridean species. For species with a reproductive output independent of female size we suggest other variables, such as the nutritional condition of a female, the number of broods per reproductive station, population structure and density, temperature or mortality to modulate the energetic investment and thus the reproductive output of a female (SASTRY, 1983; CLARKE et al., 1991).

Brood weight of L. paulensis averages 14.2 ± 5.4% of female body weight. This value lies at the low end of the range of previously published data of palaemonids (10.5 -26.9%, Table 2) and within the range of other pandalid, crangonid and alpheid shrimp species (9 - 24%) (see OH et al., 2002 for references). The reproductive output of L. paulensis is very similar to that of Palaemon northropi(14.4 ± 2.7%), a sympatric tropical marine shrimp species also abundant in Brazilian shallow waters (ANGER; MOREIRA, 1998).

Table 2 Comparison of reproductive output (RO) and fecundity in different species of Palaemonidae 

Species RO (%) Fecundity Reference
Mean ± SD Mean ± SD min - max
Macrobrachium hainanense 10.5 ± 3.8 39.1 20-75 Mantel and Dudgeon (2005)
M. carcinus 12.0 ± 4.0 98,749 14,420-242,437 Lara and Wehrtmann (2009)
Palaemon gravieri 12.7 ± 6.6 n.a. 212-3,989 Oh and Park (2000)
M. amazonicum (inland) 14 ± 6 271 ± 54 n.a. Meireles et al. (2013)
(coastal) 10 ± 2 2,237 ± 586 n.a.  
P. carinicauda 14 ± 9 n.a. 107-1216 Oh and Kim (2008)
Leander paulensis 14.2 ± 5.4 635 ± 245.95 227-1360 Present study
P. northropi 14.4 ± 2.7 n.a. 172-418 Anger and Moreira (1998)
P. modestus 17.4 ± 4.6 182 ± 68 60-353 Oh et al. (2002)
  17.5 ± 8.6 n.a. 254-1,702 Oh and Park (2000)
P. pandaliformis 18.6 ± 3.0 n.a. 102-375 Anger and Moreira (1998)
M. acanthurus 19.1 ± 4.5 n.a. 440-3,042 Anger and Moreira (1998)
M. olfersii 21.7 ± 6.6 n.a. 170-8,960 Anger and Moreira (1998)
P. paucidens 27 241 ± 33 195-328 Kim et al. (2008)

RO values are dry weight estimates; n.a.: no information available.

Reproductive output underlies a trade-off with growth.

This tradeoff has been suggested for some sympatric congeneric species of brachyuran crabs (CARVALHO et al., 2010). However, the lack of comparative studies for many ecological traits and for many groups makes a general statement for Palaemonidae unfeasible. Since brood weight is a combined measure of fecundity and single egg weight (i.e. egg volume) the reproductive output (a measure of brood weight relative to female weight) underlies the ecological factors determining fecundity and egg volume. Over evolutionary time-scales, selection acts on egg size through factors such as food availability or predation risk, whereas overall reproductive investment is determined by feeding conditions for the adult females as ovaries mature (CLARKE et al., 1985). In any given situation, proximate local factors may modulate the extent to which the optimal level of reproductive investment is realized (CLARKE et al., 1991). This makes it very difficult to identify rules and relationships of specific factors. Although necessary to analyze different reproductive strategies and their ecological and phylogenetic relationships, comparative studies of marine, estuarine and freshwater palaemonid species will be challenging since there is strong biological variation among reproductive traits.

CONCLUSION

Comparison of fecundity and egg size of Leander paulensis with other palaemonids reveals that this species produces a large number of relatively small eggs, with no correlation of investment per reproductive event to female body size. We suggest several extrinsic and intrinsic variables to modulate the reproductive output, such as nutritional condition, temperature or the number of broods per reproductive station. Size and number of eggs of L. paulensis may suggest an extended larval development, as found in many species of Palaemonidae. We showed that females gain weight during egg incubation, which may be a result of a restoration of depleted energy reserves after reproduction. This weight gain must be taken into account when estimating the reproductive output, brood loss in relation to female weight or any other weight-dependent variables of reproduction. The evaluation of several reproductive traits of marine, estuarine and freshwater palaemonids is necessary to generate a comparative analysis of strategies as well as their ecological and phylogenetic relationships.

Financial Support: FAPESP (Temático Biota 2010/50188-8) CAPES (Ciências do Mar II Proc. 2005/2014 - 23038.004308/201414) CNPq (DR 140199/2011-0 and PQ 302748/2010-5; 304968/2014-5)

ACKNOWLEDGEMENTS

The authors express their deep gratitude to the Faculty of Philosophy, Science and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), to FAPESP (Temático Biota 2010/50188-8) and CAPES (Ciências do Mar II Proc. 2005/2014 -23038.004308/2014-14) for grant support enabling us to travel to the northern coast of São Paulo and for facilities during the development of the course: Methodologies on Fauna Studies - Invertebrates. We express our thanks to all participants for their help during field activities. FLC and FLM were supported by PhD and Research fellowships from CNPq (140199/2011-0 and 302748/2010-5; 304968/2014-5, respectively). The collection of specimens conducted in this study complied with current applicable state and federal laws of Brazil (DIFAP/IBAMA/126/05; permanent license to FLM for collection of Zoological Material Nº 11777-1 MMA/IBAMA/SISBIO).

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* Corresponding author: flmantel@usp.br

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