Research Article |
Corresponding author: Adriana Rebolledo ( adriprn@gmail.com ) Academic editor: Raymond Bauer
© 2014 Adriana Rebolledo, Ingo Wehrtmann, Darryl Felder, Fernando Mantelatto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Rebolledo AP, Wehrtmann IS, Felder DL, Mantelatto FL (2014) Embryo production in the sponge-dwelling snapping shrimp Synalpheus apioceros (Decapoda, Alpheidae) from Bocas del Toro, Panama. In: Wehrtmann IS, Bauer RT (Eds) Proceedings of the Summer Meeting of the Crustacean Society and the Latin American Association of Carcinology, Costa Rica, July 2013. ZooKeys 457: 227-238. https://doi.org/10.3897/zookeys.457.6403
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Caridean shrimps of the genus Synalpheus are abundant and widely distributed in tropical and subtropical regions, but knowledge of their reproductive biology remains scarce. We report reproductive traits of Synalpheus apioceros from Bocas del Toro, Panama, based on collections in August 2011. The 46 ovigerous females that were analyzed ranged in size from 3.8 to 7.4 mm in carapace length. Fecundity varied between 8 and 310 embryos and increased with female size. Females invested 18.6 ± 10.3% of their body weight in Embryo production. Embryo volume increased considerably (77.2%) during embryogenesis, likely representing water uptake near the end of incubation period. Compared to Synalpheus species with abbreviated or direct development, S. apioceros produced substantially smaller embryos; however, S. apioceros seems to have a prolonged larval phase with at least five zoeal stages, which may explain the combination of relatively small and numerous embryos. We did not find nonviable, minute, chalky embryos, previously reported for S. apioceros specimens obtained from the northwestern Gulf of Mexico, which supports the hypothesis that the production of this type of embryos may be a physiological response of this warm-water species to the temperature decrease near to its latitudinal range limit.
Aunque los camarones carídeos del genero Synalpheus son muy abundantes y se encuentran ampliamente distribuidos en regiones tropicales y subtropicales, el conocimiento sobre su biología reproductiva es escaso. En este estudio reportamos algunas características reproductivas de especímenes de Synalpheus apioceros de Bocas del Toro, Panamá, colectados en Agosto del 2011. El largo del caparazón de las 46 hembras ovígeras analizadas se encuentra en un rango de 3.8 y 7.4 mm. La fecundidad varió entre 8 y 310 huevos, aumentando con el tamaño de la hembra. Las hembras invirtieron 18.6 ± 10.3% de su peso corporal en la producción de huevos. El tamaño de los huevos aumentó considerablemente (77.2%) durante la embriogénesis, probablemente por la absorción de agua al final del periodo de incubación. Comparado con especies de Synalpheus que presentan desarrollo abreviado o directo, S. apioceros produce huevos considerablemente más pequeños; sin embargo S. apioceros parece tener una fase larval prolongada, con al menos cinco estadios larvales, lo que podría explicar que los huevos sean relativamente pequeños y numerosos. No encontramos los huevos anómalos, no viables, que previamente se habían reportado para especímenes obtenidos en el Golfo de México, lo cual apoya la hipótesis de que la producción de este tipo de huevos puede ser una respuesta fisiológica a la disminución de temperatura cerca del límite latitudinal de esta especie habitante de aguas cálidas.
Central America, embryo volume, fecundity, incubation period, reproductive output, water uptake
Reproductive traits of crustacean species offer relevant information about their life history strategies (
Caridean shrimps of the genus Synalpheus are distributed worldwide with estimates of about 150 valid species (
Most studies on this genus have focused on geographical distribution (
Synalpheus apioceros is widely distributed in the western Atlantic (Gulf of Mexico; Florida; Bahamas), throughout the Caribbean Sea (e.g., Panama, Puerto Rico, Mexico, Venezuela etc.), Suriname, and Brazil (Amapá to Santa Catarina). Assuming that we are dealing with a single species, it can be found in association with different hosts (see
Ovigerous females of Synalpheus apioceros were collected by hand (August 2011) from an area near the Smithsonian Tropical Research Institute (STRI) marine station (09°20'N, 82°14'W), at Bocas del Toro, on the Caribbean coast of Panama. Shrimps were found in the red-orange sponge Lissodendoryx colombiensis Zea & van Soest, growing on jetty pilings and mangrove roots. In the laboratory, ovigerous females were extracted from the sponge canals and stored individually to avoid mixing and loss of the embryos and then preserved in ethanol (70%). Voucher specimens were deposited in the Crustacean Collection of the Museo de Zoología - Universidad de Costa Rica (MZUCR) under catalog number MZUCR 3128-01.
Carapace length (CL) of ovigerous females was measured (± 0.1 mm) under a stereomicroscope with an ocular micrometer, from the tip of the rostrum to the posterior margin of the carapace. The entire embryo mass from each female was detached from the pleopods and embryos were classified into three stages (I–III) according to the shape and development of the abdomen and eyes (
Ten embryos of each female were randomly selected to measure the length (a) and width (b) under a stereomicroscope equipped with an ocular micrometer; these data were used to determined the embryo volume (EV) with the formula EV = 1/6×a×b2×π (
Due to possible embryo loss during the incubation period (
Data were analyzed with the statistical software SPSS v.20.0. The assumption of normality on the size distribution of the individuals was tested using the Kolmogorov-Smirnov test. Linear regressions and Pearson’s correlation analyses were applied to determine the relation between CL and fecundity, and CL and RO. One-way Analyses of Variance (ANOVA) were used to compare embryo volume and water content among the three stages of development.
A total of 46 ovigerous females were analyzed; the majority of them (21 total or 45.7%) carried embryos at Stage I, 10 (21.7%) in Stage II and 15 females (32.6%) in Stage III. The size frequency distribution was normal (Kolmogorov-Smirnov test, KS = 0.11, p > 0.05). The mean CL of the individuals was 5.4 ± 0.8 mm, ranging from 3.8 to 7.4 mm, and 43.5% of the ovigerous females were in the intermediate size class of 5.0–5.9 mm (Fig.
Fecundity in Stage I ranged from 8 to 310, and increased with female size (Pearson’s correlation, r = 0.68, p < 0.05) (Fig.
Fecundity by size class in females carrying recently-produced embryos (Stage I) for Synalpheus apioceros, Bocas del Toro, Panama.
Size class (mm) | Mean embryos number |
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4.0–4.9 (N = 6) | 34.8 ± 28.5 |
5.0–5.9 (N = 10) | 88.6 ± 49.6 |
6.0–6.9 (N = 4) | 184.8 ± 103.8 |
7.0–7.9 (N = 1) | 220 |
Embryos were slightly oval with mean diameters ranging from 0.63 ± 0.04 mm (Stage I) to 0.77 ± 0.06 mm (Stage III). Embryo volume differed significantly (ANOVA, F = 369.25, p < 0.05) between the stages of development, with an overall volume increase during the incubation period of 77.2% (Table
Embryo volume, weight, and water content of different embryonic development stages of Synalpheus apioceros, Bocas del Toro, Panama.
Embryo features | Stage I (N = 20) | Stage II (N = 8) | Stage III (N = 9) |
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Embryo volume (mm3) | 0.101 ± 0.015 | 0.136 ± 0.018 | 0.179 ± 0.034 |
Wet weight (µg) | 74.0 ± 12.5 | 128.2 ±10.5 | 173.9 ± 19.8 |
Dry weight (µg) | 30.1 ± 5.3 | 29.8 ± 1.5 | 29.3 ± 5.2 |
Water content (µg) | 43.9 ± 10.0 | 98.4 ± 9.4 | 144.6± 21.0 |
% Water content | 59.0 ± 5.9 | 76.6 ± 2.0 | 82.9 ± 3.6 |
The size of ovigerous females of Synalpheus apioceros from Bocas del Toro is within the range for congeneric species (Table
Mean carapace length, embryo number, and embryo volume for ten species of sponge-dwelling Synalpheus.
Species | N | Carapace length (mm) | Embryo number | Embryo volume (mm3) | Reference |
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Synalpheus agelas | 5 | 5.0 (4.2–5.6) |
42.4 (16–65) |
0.23 |
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S. brooksi | 10 | 3.9 (3.4–4.5) |
5.8 (3-11) |
0.50 | |
S. fritzmuelleri | 13 | 4.9 (3.8–6.5) |
173.4 (39–484) |
0.09 | |
S. herricki | 4 | 4.5 (3.5–5.12) |
45.8 (11–81) |
0.22 | |
S. longicarpus | 21 | 6.9 (5.5–8.0) |
195.4 (27–349) |
0.17 | |
S. pectiniger | 31 | 4.2 (3.5–4.6) |
9.9 (4–17) |
0.75 | |
S. chacei | 2 | 3.7 | 16 | 0.15 |
|
S. idios | 4 | 3.9 ± 0.2 (3.7–4.2) |
12.0 ± 4.3 (9–18) |
1.04 ± 0.23 (0.70–1.20) |
|
S. yano | 84 | 5.6 ± 1.2 (3.7–9.6) |
98.0 ± 64.6 (6–246) |
0.15 ± 0.08 (0.06–0.51) |
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S. apioceros | 46 | 5.4 ± 0.8 (3.8–7.4) |
97.8 ± 80.1 (8–310) N = 21 (Stage I) |
0.13 ± 0.04 (0.07–0.24) N = 37 |
Present study |
Fecundity variation within the same size class is a well-known phenomenon in decapods, including alpheid shrimps (
The energy invested in embryo production, estimated by reproductive output (RO), was not related to their size in S. apioceros. Average RO in alpheid shrimp is highly variable, ranging from 7 to 35% (
The embryo volume in S. apioceros is within the range reported for other alpheid shrimp (
Embryo volume of S. apioceros increased considerably (77.2%) during the incubation period. This is a common phenomenon in decapod species and is probably related to water uptake over the course of embryogenesis (
While we here provide novel information on reproduction in the sponge-dwelling alpheid shrimp S. apioceros, it is based on a limited sampling period and a single locality. We thus regard our work to date as a starting point from which we and others might build comparative studies. Conspecific populations can be readily sampled across latitudes and temperature regimes, as well as over varied seasons, applying the methods we have used and enabling comparative analyses. Such work can both reveal life history strategies that have evolved in these host-dependent shrimp species and shed light on what ranges of reproductive variability might be expected due to environmental interactions in this era of global coastal ocean change.
The authors acknowledge the Smithsonian Tropical Research Institute (STRI), Panama for support to APR, DLF, and FLM covering their travel to Panamá and use of facilities during a workshop on crustacean biology and taxonomy. Special thanks are due to Rachel Collin (Director of the Bocas del Toro Laboratory, STRI), who assisted with logistics, and Jenny Felder for her enthusiastic help during both field and laboratory activities, and all other participating students, assistants, and STRI staff involved in the course hosted at the Bocas del Toro Research Station from July 31 to August 15, 2011. Partial support was provided by research grants NSF/RAPID DEB 1045690 and GoMRI-112-8 to DLF. This is contribution number 166 of the University of Louisiana’s Laboratory for Crustacean Research.