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The Reproductive Performance of the Red-Algae Shrimp Leander Paulensis

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The Reproductive Performance of the Red-Algae Shrimp Leander Paulensis Zimmermann et al.: The reproductive performance of Leander paulensis ORIGINAL ARTICLE / ARTIGO ORIGINAL BJOCE 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,* 1 Eberhard Karls-University Tübingen, Faculty of Science, Department of Biology (Auf der Morgenstelle 28, 72076 Tübingen, Germany) 2 Universidade 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) 3 Universidade 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) *Corresponding author: [email protected] 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) ABSTRACT RESUMO Decapod species have evolved with a variety of Decápodes desenvolveram uma ampla variedade reproductive strategies. In this study reproductive de estratégias reprodutivas. Neste estudo foram features of the palaemonid shrimp Leander paulensis investigadas características reprodutivas da espécie de were investigated. Individuals were collected in the Palaemonidae Leander paulensis. Os indivíduos foram coastal region of Ubatuba, São Paulo, Brazil. In coletados na região costeira de Ubatuba, São Paulo, all, 46 ovigerous females were examined in terms Brasil. Foram examinadas 46 fêmeas ovígeras quanto of the following reproductive traits: fecundity, aos seguintes aspectos reprodutivos: fecundidade, reproductive output, brood loss and egg volume. investimento reprodutivo, perda de ovos e volume dos Leander paulensis produces a large number of ovos. Leander paulensis produz uma grande quantidade small eggs with an average fecundity of 635 ± 246 de pequenos ovos, com fecundidade média de 635 ± 246 eggs. Egg volume increased significantly from early ovos. O volume dos ovos aumentou significativamente (0.034 ± 0.008 mm3) to late development stage quando comparado o estágio inicial (0.034 ± 0.008 mm3) com o estágio final de desenvolvimento (0.05 ± (0.05 ± 0.012 mm3). The reproductive output did not 0.012 mm3). O investimento reprodutivo não apresentou correlate with female size. The weight of females correlação com o tamanho das fêmeas. Fêmeas com bearing stage 2 eggs was significantly higher than ovos no estágio 2 apresentaram massa corpórea seca that of females carrying stage 1 eggs. We assume significativamente maior que aquelas carregando ovos that the reason for this weight gain is the recovery no estágio inicial. Esse aumento de massa parece ser of female reserves that have been depleted for decorrente da recuperação de reservas energéticas das egg production. Moreover, we emphasize that this fêmeas, que teriam sido utilizadas durante a produção weight gain must be considered when evaluating de ovos. Além disso, deve-se considerar neste tipo de weight-dependent variables such as reproductive avaliação o aumento da massa corpórea em relação output or brood loss in relation to female weight. ao investimento reprodutivo, assim como da perda de Otherwise, an overestimation of these variables ovos relacionada à massa das fêmeas ou qualquer outra might lead to inaccurate results. variável dependente do peso. Descriptors: Brood loss, Caridea, Egg volume, Descritores: Fecundidade, Caridea, Perda de ovos, Fecundity, Reproductive output. Volume de ovos, Investimento reprodutivo. http://dx.doi.org/10.1590/S1679-87592015085806303 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 63(3):207-216;2015 207 Zimmermann et al.: The reproductive performance of Leander paulensis INTRODUCTION Ubatuba, São Paulo State, Brazil (Figure 1). In total, 46 ovigerous females were captured using a hand push net There are many reproductive strategies among at a depth of 0.5 to 1 m and were identified according to decapods, and these manifest as differences in parameters Ramos-Porto (1986). All specimens were kept in 80% such as fecundity and breeding frequency, which are directly ethanol for the duration of the study. 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 Figure 1. Location of the sampling site in the Flamengo Bay in the southern region of Ubatuba, State of São Paulo, Brazil. congeners are discussed in PAVANELLI et al. (2008) and TAMBURUS et al. (2012). Eggs of all females were gently removed, using The genus Leander DESMAREST, 1849, is composed fine forceps under a Leica® stereomicroscope M205C. of five species distributed in different regions (DE GRAVE; The measurement of eggs and females, and the counting FRANSEN, 2011). Leander paulensis ORTMANN, 1897, and classification of eggs, were performed under the is a small shrimp that occurs in shallow marine waters of stereomicroscope with the aid of the Leica Application the western Atlantic from Florida, USA to Paraná, Brazil Suite® (v 3.8.0). Female carapace length was measured (CARVALHO et al., 2014). It inhabits sand and rock from the post-orbital margin to the posterior border of bottoms with algae up to a depth of 16 m (RAMOS-PORTO, the carapace. Eggs were counted and classified into two 1986). Studies regarding L. paulensis have focused on the stages: stage 1 (early development) without eyespots and composition of crustacean fauna of certain areas (COSTA stage 2 (late development) with visible eyespots (COREY; et al., 2000; COELHO et al., 2006; ALMEIDA et al., REID, 1991). Ten eggs from each female were randomly 2006, 2007a, b; MCCARTHY et al., 2012), taxonomy and chosen for measurement of their major and minor axis and geographical distribution (MANNING, 1961; RAMOS- the volume of each egg was quantified using the volume PORTO, 1986; ABELE; KIM, 1989; RAMOS-PORTO; formula of oblate spheroids (cf. TURNER; LAWRENCE, COELHO, 1998; CARVALHO et al., 2014). Some ecological 1979): EV = 4/3 * π * EL/2 * (EW/2)2, where EV = egg features, such as reproductive period, fecundity, egg volume volume, EL = egg length and EW = egg width. For fecundity and brood volume (BAUER, 1989, 1991; COREY; REID, estimation, an ANCOVA was performed to check whether 1991), have been addressed in the congeneric species there is a loss of eggs from stage 1 to stage 2. As the results Leander tenuicornis. However, Leander paulensis remains showed no significant difference (see results section), eggs completely unknown in terms of its reproductive strategy. of all 46 females were considered, regardless of their stage. Considering that fecundity is an expressive measure of Fecundity was thus determined as the total number of eggs reproductive potential and contributes to the understanding of attached to the abdomen of each female. reproductive performance, the aim of the present paper is to Egg samples and females were weighed separately. analyze female weight gain during egg incubation, fecundity Female weight was quantified after removing all the eggs and investment per reproductive event in Leander paulensis. from the female’s abdomen. All weight measures were dry weight values and were quantified after 48 hours of MATERIAL AND METHODS oven drying at 50º C (Fanem oven model 315 SE). Brood weight was determined as the total weight of the entire All specimens were collected in April 2013 at egg batch. The reproductive output (RO) was estimated Lamberto beach (23º29′56″S, 45º07′04″W), a protected for one single spawning event (one brood) and is area that lies in the sheltered Flamengo bay, south of 208 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 63(3):207-216;2015 Zimmermann et al.: The reproductive performance of Leander paulensis 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 Figure 2. Power function of female weight and carapace length. The weight of females with stage 2 eggs is significantly higher than the ANCOVA. weight of females with stage 1 eggs (F = 36.4, d.f. = 1, 43, p < 0.01). The Akaike Information Criterion (AIC) was used Female weight does not include egg weight. FW = female weight; to choose the simplest model of ANCOVA that could be CL = carapace length. used (with or without interaction). All ANCOVA were FECUNDITY performed with sum of squares type III, having carapace length as the covariate. The variables were linearized Of the 46 females examined, 32 females carried (ln) for all ANCOVA. A Student’s t-test was performed eggs of stage 1 and 14 carried eggs of stage 2. Fecundity to verify whether there is any difference between the showed a strong correlation with carapace length which volume of eggs in stage 1 and stage 2. A linear regression could be described by a power function (Figure 3). There analysis was conducted to check for a relationship was no significant difference in the number of eggs between the reproductive output and carapace length between stages 1 and 2 (F = 0.32, d.f.
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