Research Article |
Corresponding author: Carolina Salas-Moya ( carosalasm@gmail.com ) Academic editor: Raymond Bauer
© 2014 Carolina Salas-Moya, Sebastián Mena, Ingo Wehrtmann.
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:
Salas-Moya C, Mena S, Wehrtmann IS (2014) Reproductive traits of the symbiotic pea crab Austinotheres angelicus (Crustacea, Pinnotheridae) living in Saccostrea palmula (Bivalvia, Ostreidae), Pacific coast of Costa Rica. 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: 239-252. https://doi.org/10.3897/zookeys.457.7851
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Pea crabs of the family Pinnotheridae exhibit a symbiotic life style and live associated with a variety of different marine organisms, especially bivalves. Despite the fact that pea crabs can cause serious problems in bivalve aquaculture, the available information about the ecology of these crabs from Central America is extremely limited. Therefore, the present study aimed to describe different reproductive features of the pinnotherid crab Austinotheres angelicus associated with the oyster Saccostrea palmula in the Golfo de Nicoya, Pacific coast of Costa Rica. Monthly sampling was conducted from April to December 2012. Average carapace width (CW) of the 47 analyzed ovigerous females was 7.62 mm. The species produced on average 2677 ± 1754 recently -extruded embryos with an average volume of 0.020 ± 0.003 mm3; embryo volume increased during embryogenesis by 21%, but did not vary significantly between developmental stages. Brood mass volume varied greatly (between 11.7 and 236.7 mm3), and increased significantly with female CW. Females invested on average 76.7% (minimum: 21.7%; maximum: 162.8%) of their body weight in brood production, which confirms a substantially higher energy allocation for embryo production in pinnotherid crabs compared to free-living decapods.
Central America, fecundity, reproductive output, symbiosis
Symbiotic relationships in marine organisms are a well-documented phenomenon (
The Pinnotheridae is a highly diverse family, currently with 52 genera and more than 300 described species (
The pinnotherid crab Austinotheres angelicus Lockington, 1877 (Fig.
The study site was Punta Morales, Golfo de Nicoya (Fig.
Morphometric measurements of oysters (height, length, and thickness) were obtained with a digital caliper (± 0.01 mm); the three morphometric variables were multiplied in order to calculate the approximate volume of each oyster (OV). Each individual of S. palmula was carefully opened and inspected for associated pea crabs. The carapace length (CL: distance between distal part of the eye socket to the posterior margin of the carapace), carapace width (CW: distance between lateral margins of the carapace), abdomen length (AL: distance between posterior margin of the carapace to the distal part of the abdomen) and abdomen width (AW: distance between lateral margins of the abdomen) were measured with the aid of a Leica MS5 stereoscopic microscope equipped with a calibrated ocular micrometer.
The entire brood mass was detached from ovigerous females (n = 47), evenly distributed on a Petri dish, and photographed (Benq GH650). These images were analyzed subsequently with the program ImageJ® versión 1.46r to count the total number of embryos carried by each ovigerous female. Embryos were staged according to the following criteria (
EV = (b / 2)2 × a × b × π (1)
where a is the major diameter, and b is the perpendicular diameter. A total of 15 embryos were measured from each female, and the average embryo volume was multiplied by the total number of embryos per female to calculate brood mass volume.
Females and their separated brood masses were dried at 60 °C for 48 hours, and dry weights were measured to calculate the reproductive output (RO): dry weight of total brood mass per female / dry weight of females without brood mass (
The Kruskal-Wallis test was applied to detect possible differences in both brood numbers between the three embryonic stages, and embryo volume during embryogenesis. Simple linear regressions and the Pearson correlation coefficient were calculated to determine the relation between both host morphometry (OV: volume of the oyster) and CW of A. angelicus (considering exclusively females with recently -produced embryos), fecundity (exclusively embryos in Stage I) and the following morphometric variables of the female: CW, CL, AW, and AL; and finally brood mass volume and CW of ovigerous females. All statistical analyses were carried out with JMP® version 7.0.
The CW of the ovigerous female crabs averaged 7.62 mm, and ranged in size from 5.02 to 14.25 mm (Table
Fecundity, embryo volume during embryogenesis (Stage I–III) and carapace width of corresponding ovigerous females of Austinotheres angelicus (n = 47), Golfo de Nicoya, Pacific coast of Costa Rica.
Stage | N | Fecundity | Embryo volume (mm3) | Carapace width (mm) | |||||||||
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Av | SD | Min | Max | Av | SD | Min | Max | Av | SD | Min | Max | ||
I | 35 | 2677 | 1764 | 550 | 7527 | 0.020 | 0.003 | 0.013 | 0.027 | 7.60 | 1.18 | 5.02 | 10.87 |
II | 6 | 3029 | 2599 | 955 | 7900 | 0.023 | 0.005 | 0.017 | 0.031 | 7.27 | 1.21 | 5.70 | 9.00 |
III | 6 | 4890 | 3176 | 830 | 8509 | 0.024 | 0.005 | 0.017 | 0.031 | 8.10 | 3.10 | 6.07 | 14.25 |
This is the first published report on reproductive aspects of A. angelicus.
Brood size increases with female body size have been well documented for pinnotherids (
Comparison of female size (CL and CW), fecundity, embryo volume during early embryogenesis, and reproductive output of different pinnotherids; host species and study sites are indicated. NA: no data available.
Species | CL (mm) | CL range (mm) | CW (mm) | CW range (mm) | Average fecundity | Fecundity range | Embryo volume (mm3) | RO (%) | Host | Study site | Reference |
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Austinixa gorei | NA | NA | 6.80 | 6.30–8.90 | NA | 195–525 | NA | NA | Gilvossius setimanus (Malacostraca, Callianassidae) | United States of America, northwest Point on Key Biscayne in Bear Cut |
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Austinotheres
angelicus
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5.60 | 4.00–7.60 | 6.87 | 4.90–9.40 | 2032 |
680–3300 | NA | NA | Saccostrea palmula (Bivalvia, Ostreidae) | Costa Rica, mangroves at Punta Morales, Pacific coast |
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Austinotheres angelicus | 5.43 | 3.82–9.37 | 7.60 | 5.03–10.87 | 2677 | 550–8509 | 0.020 | 77 | Saccostrea palmula (Bivalvia, Ostreidae) | Costa Rica, Punta Morales, Pacific coast | Present study |
Fabia subquadrata | NA | NA | NA | NA | 7560 | NA | 0.037 | 97 | Mytilus californianus (Bivalvia, Mytilidae) | United States of America, Bodega Head, CA |
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Pinnaxodes chilensis | 12.22 | 8.20–15.50 | NA | NA | 4553 | 2134–9456 | 0.048 | 70 | Loxechinus albus (Echinoidea, Parechinidae) | Chile, Caleta Coloso |
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Pinnaxodes chilensis | 16.39 | 10.75–20.00 | NA | NA | 8358 | 2376–15898 | 0.070 | 80 | Loxechinus albus (Echinoidea, Parechinidae) | Chile, El Quisco |
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Pinnaxodes chilensis | 18.59 | 17.40–20.30 | NA | NA | 8082 | 5045–15432 | 0.072 | 81 | Loxechinus albus (Echinoidea, Parechinidae) | Chile, Mehuín |
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Zaops ostreus | NA | NA | NA | NA | 5680 | NA | 0.092 | 66 | Crassostrea virginica (Bivalvia, Ostreidae) | United States of America, Indian River, FL |
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Brood loss is a well described phenomenon in decapods (for review:
The embryo volume of A. angelicus increased during the incubation period by 21%. This increase is relatively low when compared to other marine decapods living in association with other invertebrates: Synalpheus yano (Ríos & Duffy, 2007) in the sponge Lissodendoryx colombiensis Zea & van Soest, 1986; 118% (
Embryo size has been considered as an indicator for energy content provided by the female (
The size of A. angelicus increased significantly with the volume of its host, S. palmula. This finding concurs with results reported by
Representatives of the family Pinnotheridae have evolved a series of adaptations to cope with their symbiotic life style (
We would like to acknowledge the logistic support provided by the Estación de Ciencias Marino Costeras (ECMAR). A special thanks goes to Raymond T. Bauer for his support and suggestions. Rita Vargas and Ernesto Campos helped us with the identification of Austinotheres angelicus, Julian Schneider took the photographs of the species, Fiorella Vásquez and Gustavo Arias assisted during some sampling trips; thanks goes to Juan José Alvarado for his interest in this study, and Raquel Romero Chaves prepared the map with the sampling locations; to all of them: muchas gracias!