Open Journal of Ecology
Vol.3 No.2(2013), Article ID:31250,3 pages DOI:10.4236/oje.2013.32019

Parental care in the freshwater crab Sylviocarcinus pictus (Milne-Edwards, 1853)*

Bruno Sampaio Sant’Anna, Erico Luis Hoshiba Takahashi, Gustavo Yomar Hattori

Federal University of Amazonas (Amazonas University), Institute of Exact Science and Technology (ICET), Itacoatiara, Brazil; *Corresponding Author: brunusant@hotmail.com, ericolht@yahoo.com.br, ghattori@yahoo.com

Copyright © 2013 Bruno Sampaio Sant’Anna et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received 16 January 2013; revised 17 February 2013; accepted 15 March 2013

Keywords: Freshwater Crab; Parental Care; Reproduction; Trichodactylidae

ABSTRACT

Parental care is a common strategy in many animal groups, to increase survival of the offspring. Here, we report parental care in the freshwater crab Sylviocarcinus pictus. A female caught in the Amazon River, Brazil, bore juvenile crabs rather than eggs on her abdomen. Kept in the laboratory, the female retained the juveniles on the abdomen for 17 days, after which the juveniles left the abdomen. A total of 341 juvenile crabs measuring 3.45 ± 0.12 mm were recorded. This pattern of parental care is very important for the maintenance of local populations of S. pictus, because if the larvae were released, as occurs in many marine species, they would drift downstream.

1. INTRODUCTION

In many animal species, parental care is a common reproductive strategy [1-3]. The many patterns of parental care include biparental, or uniparental by either males or females [1]; that may show manipulation of sex differences in parental care [4] and is energetically costly [5]. Many groups of invertebrates show some form of parental care. For instance, in insects the most rudimenttary form of maternal care is provided by females that incorporate toxins into their eggs, oviposit them in protected places, or cover their eggs with a hard wax-like shell before abandoning them [3]. In arachnids, females of Bourguyia albiornata Mello-Leitão 1923 oviposit almost exclusively inside the tube formed by the curled leaves of the bromeliad Aechmea nudicaulis (Linnaeus) Grisebach, 1864 [6]. Jawed Hirudinidae deposit desiccationresistant cocoons on land and many species brood the eggs and young [7].

In decapod crustaceans, parental care is usually restricted to females that carry the eggs in the brood compartment, and care is terminated when the larvae are released into the plankton [8,9]. However, among other examples in crustaceans, [10] presented evidence of a direct link between active brood care and provision of oxygen to the young. For amphipods, [11,12] studied active maternal brooding and juvenile care. The preparation of a nest structure to defend and feed its young in the crab Metopaulias depressus Rathbun, 1918 was recorded [9,13].

For freshwater crustaceans, available information about parental care is sparse in comparison with marine species. The species that has been most studied is the crab M. depressus, in several aspects, i.e., parental care in an unusual environment [13], protection of larvae from predation by damselfly nymphs [9], maintaining oxygen, pH and calcium levels optimal for the larvae [14] and evolution theory [15]. In freshwater crabs, 15 species have been reported to bear juvenile crabs attached to the female abdomen [16]. The extended brood care was reported in species of all five families of primary freshwater crabs [17]. Here, we record a female of the freshwater crab Sylviocarcinus pictus (Milne-Edwards, 1853) with juvenile crabs attached on the abdomen, indicating the existence of parental care in this species.

2. MATERIAL AND METHODS

The female of S. pictus was collected by hand, on a bank of the Amazon River (03˚08'13.7''S; 58˚27'46.8''W) in October 2011 (Figure 1). The specimen was placed in a plastic box with aerated water and transported to the laboratory. In the laboratory, the carapace width was measured with a caliper (0.05 mm), and the crab was maintained in an aquarium for 17 days.

3. RESULTS AND DISCUSSIONS

This female had a carapace width of 41.5 mm, with 341 juvenile crabs attached to the abdomen (Figure 2). The mean size of the juveniles was 3.45 ± 0.12 mm, ranging from 3.10 to 3.66 mm. The juveniles remained on the female’s abdomen for 17 days; during this period, they would occasionally leave the female’s abdomen for

Figure 1. Location of the study area, Itacoatiara (arrow) on the Amazon River, Brazil.

Figure 2. Dorsal view of Sylviocarcinus pictus (A), ventral view of S. pictus (B), detail of juvenile crabs attached on the female abdomen (C) and juvenile crab (D). Scale bar of the figures A, B and C = 10 mm, and of figure D = 1 mm.

several minutes. After 17 days, all the juveniles permanently left the female’s abdomen. Sylviocarcinus pictus shows gregarious behavior, and the juveniles can cling to their mother, as also observed in the freshwater crab Potamon edulis (P. fluviatile) (Latreille, 1818) by [18], this kind of behavior is common for freshwater crabs. According to [20], the juveniles of the potamid crab Candidiopotamon rathbunae (de Man, 1914) are essentially independent after their first day of life, but often return to the mother for shelter during the following 2 weeks. The same pattern was observed for the juveniles of S. pictus.

In a recent study [16] observed two size groups of juvenile crabs with different carapace morphology, attached on the abdomen of females of the crab Kingsleya ytupora Magalhães, 1986, suggesting that the juveniles are attached to females for a prolonged period. In the present study, all juveniles had the same morphology and similar size, and remained on the female’s abdomen for 17 days in the laboratory. However, as recorded by [16], we did not observe the hatching process and cannot accurately report the full period of juvenile incubation by females.

According to [11], brood care is called “active” if specific parental activities are directed toward the brood, and “passive” if such specific behavior is lacking. Females of S. pictus could be considered “active” in parenmtal activities, since in this freshwater crab the embryonic and larval periods are completed entirely in the egg stage, resulting in hatching of miniature adults [20]; these are considered juveniles, and remain on the abdomen.

Abbreviated larval development is often accompanied by increased parental care. According to [21], in its broadest sense, parental care includes preparation of nests and burrows, production of heavily yoked eggs, care of the eggs, provisioning of the young, and care of the offspring after they reach nutritional independence. Parental care significantly affects the ecological success and evolutionary potential of species by enhancing the survival and fitness of the offspring. In the freshwater caridean shrimp Dugastella valentina, [22] observed both the abbreviated development and parental safeguarding until the decapodid stage obviously reduce the risk of being washed away or of being predated upon. Simultaneously, this type of parental care could mean a limited gene flow and hence a high degree of genetic divergence between populations, because of the low dispersal ability of the larvae [22]. In populations of S. pictus, the epimorphic development and parental care could produce a similar situation.

This pattern is common in primary freshwater crabs, because in freshwater habitats there are strong selective pressures toward reduction in egg number and increase in egg size, abolishment of free larvae, and extension of brood care until the juvenile stage, resulting in a marked reduction in dispersal and gene flow, and leading to the high degree of endemism and speciation seen in these crustaceans [17]. However, under conditions of rapid habitat destruction, environmental pollution and global warming, slow dispersal of direct developers may become a severe disadvantage, impairing replacement of lost populations and placing the directly developing taxa at a greater risk of extinction than the indirectly developping taxa [17].

4. CONCLUSIONS

The present study records extended parental care in the crab S. pictus, contributing to knowledge of the reproduction of freshwater crabs. This pattern of parental care is very important for the maintenance of local populations of S. pictus, because if the larvae were released, as occurs in many marine species, they would drift downstream.

REFERENCES

  1. Webb, J.N., Houston, A.I., McNamara, J.M. and Székely, T. (1999) Multiple patterns of parental care. Animal Behaviour, 58, 983-993. doi:10.1006/anbe.1999.1215
  2. Cockburn, A. (2006) Prevalence of different modes of parental care in birds. Proceedings of the Royal Society B, 273, 1375-1383. doi:10.1098/rspb.2005.3458
  3. Scott, M.P. (2009) Parental care. In: Resh, V.H. and Cardé, R.T., Eds., Encyclopedia of Insects, 2nd Edition, Academic Press, New York, 751-753. doi:10.1016/B978-0-12-374144-8.00200-9
  4. Wring, J. and Cuthill, I. (1989) Manipulation of sex differences in parental care. Behavioral Ecology and Sociobiology, 25, 171-181. doi:10.1007/BF00302916
  5. Lardies, M.A., Cotoras, I.S. and Bozinovic, F. (2004) The energetics of reproduction and parental care in the terrestrial isopod Porcellio laevis. Journal of Insect Physiology, 50, 1127-1135. doi:10.1016/j.jinsphys.2004.10.005
  6. Machado. G. and Oliveira, P. (2002) Maternal care in the neotropical harvestman Bourguyia albiornata (Arachnida; Opiliones): Oviposition site selection and egg protection. Behaviour, 139, 1509-1524. doi:10.1163/15685390260514744
  7. Kutschera, U. and Wirtz, P. (2001) The evolution of parental care in freshwater leeches. Theory in Bioscience, 120, 115-137.
  8. Hazlett, B.A. (1983) Parental behaviour in decapod Crustacea. In: Rebach, S. and Dunham, D.W., Eds., Studies in Adaptation. The Behaviour of Higher Crustacea, John Wiley, New York, 171-193.
  9. Diesel, R. (1992) Maternal care in the bromeliad crab, Metopaulias depvessus: Protection of larvae from predation by damselfly nymphs. Animal Behaviour, 43, 803- 812. doi:10.1016/S0003-3472(05)80203-9
  10. Baeza, J.A. and Fernández, M. (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): The relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Functional Ecology, 16, 241-251. doi:10.1046/j.1365-2435.2002.00616.x
  11. Dick, J.A., Faloon, S.E. and Elwood, R.W. (1998) Active brood care in an amphipod: Influences of embryonic development, temperature and oxygen. Animal Behaviour, 56, 663-672. doi:10.1006/anbe.1998.0797
  12. Thiel, M. (1998) Extended parental care in marine amphipods. I. Juvenile survival without parents. Journal of Experimental Marine Biology and Ecology, 227, 187- 201. doi:10.1016/S0022-0981(97)00268-2
  13. Diesel, R. (1989) Parental care in an unusual environment: Metopaulias depressus (Decapoda: Grapsidae), a crab that lives in epiphytic bromeliads. Animal Behaviour, 38, 561- 575. doi:10.1016/S0003-3472(89)80001-6
  14. Diesel, R. and Schuh, M. (1993) Maternal care in the bromeliad crab Metopaulias depressus (Decapoda): Maintaining oxygen, pH and calcium levels optimal for the larvae. Behaviour Ecology and Sociobiology, 32, 11-15. doi:10.1007/BF00172218
  15. Schubart, C. D, Diesel, R. and Hedges, S. B. (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature, 393, 363-365. doi:10.1038/30724
  16. Wehrtmann, I.S., Magalhães, C., Hernáez, P. and Mantelatto, F.L. (2010) Offspring production in three freshwater crab species (Brachyura: Pseudothelphusidae) from the Amazon region and Central America. Zoologia, 27, 965- 972. doi:10.1590/S1984-46702010000600019
  17. Vogt, G. (2013) Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biological Reviews, 88, 81-116. doi:10.1111/j.1469-185X.2012.00241.x
  18. Pace, F., Harris, R.R. and Jaccarini, V. (1976) The embryonic development of the Mediterranean freshwater crab, Potamon edulis (P. fluviatile) (Crustacea, Decapoda, Potamonidae). Journal of Zoology, 180, 93-106. doi:10.1111/j.1469-7998.1976.tb04666.x
  19. Liu, H.C. and Li, C.W. (2000) Reproduction in the freshwater crab Candidiopotamon rathbunae (Brachyura: Potamidae) in Taiwan. Journal of Crustacean Biology, 20, 89-99. doi:10.1651/0278-0372(2000)020[0089:RITFWC]2.0.CO;2
  20. Von Sternberg, R., Cumberlidge, N. and Rodriguez, G. (1999) On the marine sister groups of the freshwater crabs (Crustacea: Decapoda: Brachyura). Journal of Zoological Systematics and Evolutionary Research, 37, 19-38. doi:10.1046/j.1439-0469.1999.95092.x
  21. Clutton-Brock, T.H. (1991) The evolution of parental care. Princeton University Press, Princeton, 1-352,
  22. Cuesta, J.A., Palacios-Theil, E., Drake, P. and Rodríguez, A. (2006) A new rare case of parental care in decapods. Crustaceana, 79, 1401-1405.

NOTES

*Research Group on Biology and Production of Amazonic Aquatic Organisms