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New record and biological features of the commensal porcellanid crab  Polyonyx gibbesi (Crustacea: Anomura) from the north­eastern Brazilian  coast Gustavo Luis Hirose Marine Biodiversity Records / Volume 5 / October 2012 / e43 DOI: 10.1017/S1755267212000188, Published online: 27 April 2012

Link to this article: http://journals.cambridge.org/abstract_S1755267212000188 How to cite this article: Gustavo Luis Hirose (2012). New record and biological features of the commensal porcellanid crab Polyonyx gibbesi  (Crustacea: Anomura) from the north­eastern Brazilian coast. Marine Biodiversity Records, 5, e43 doi:10.1017/ S1755267212000188 Request Permissions : Click here

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Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2012 doi:10.1017/S1755267212000188; Vol. 5; e43; 2012 Published online

New record and biological features of the commensal porcellanid crab Polyonyx gibbesi (Crustacea: Anomura) from the north-eastern Brazilian coast gustavo luis hirose Laborato´rio de Carcinologia, Departamento de Biologia, Universidade Federal de Sergipe, Sa˜o Cristo´va˜o, Sergipe, Brazil

Polyonyx gibbesi—commonly known as the porcelain crab—lives commensally with an annelid that builds U-shaped tubes in shallow waters along the Atlantic coast. Polyonyx gibbesi is considered to have a mostly anti-tropical distribution, since it has been found only sporadically in tropical waters (e.g. the Caribbean). A total of 27 tubes of the polychaete host were collected from the estuarine mudflat of the Vaza-Barris River, State of Sergipe, Brazil; 23 of these tubes were inhabited by at least one individual of P. gibbesi. In the hosts examined, 42 crabs were found (21 males and 21 females). A total of four hosts harboured a single commensal crab. In all cases in which more than one crab was found per host, they were a male and female pair. A total of five females were recorded carrying eggs (1171.6 + 534.5). The frequency of P. gibbesi in the host was high (about 85%), suggesting that the occurrence of this porcelain crab was not accidental or sporadic at the study site. The presence of ovigerous females in the population further indicates the existence of mature and sexually active individuals, which are effectively reproducing. The expansion of the known distribution of P. gibbesi to the State of Sergipe in Brazil challenges the current idea of an anti-tropical distribution for P. gibbesi. Most probably, the current status of knowledge about this species’ distribution is the result of its commensal lifestyle, which makes it difficult to collect, and also the paucity of investigations along the north-eastern Brazilian coast.

Keywords: Polychaete, Chaetopterus, symbiosis Submitted 24 October 2011; accepted 6 February 2012

INTRODUCTION

The family Porcellanidae Haworth, 1825 is a group of crabshaped anomuran crustaceans, commonly known as porcelain crabs. These crabs occur worldwide in primarily intertidal and sublittoral zones of tropical and subtropical regions, and occupy habitats such as depressions under stones, algae, and corals (Haig, 1960; Gore & Abele, 1976; Baeza & Stotz, 1995). Porcelain crabs number about 280 species, partitioned among 30 genera (Rodrı´guez, 2005). Most species are freeliving but a few live commensally (Ross, 1983). Among the latter, Polyonyx gibbesi Haig, 1956 is the only species of the genus Polyonyx that occurs in the western Atlantic, and is a known commensal of the polychaete worm Chaetopterus variopedatus (Reiner, 1804). This annelid builds U-shaped tubes in shallow waters along the Atlantic coast. The tubes are buried upright, with only about 2.5 cm of narrow siphon at either end showing above the surface of substrate (Gray, 1961). The distribution of P. gibbesi is considered mostly antitropical, and it has been reported only sporadically in tropical

Corresponding author: G.L. Hirose Email: [email protected]

waters. According to Rodrı´guez et al. (2005), this species occurs in Massachusetts, Rhode Island, North Carolina, South Carolina, the east and west coasts of Florida, and Texas, USA. The crab has also been reported from Caledonia Bay in Panama, Papuy in Venezuela, Trinidad, Cuba, Puerto Rico, and from Rio de Janeiro to southern Brazil, and at La Paloma, Uruguay. More recently, Belleggia et al. (2010) extended the occurrence of P. gibbesi to the continental shelf of Argentina, with specimens found in the stomachs of the narrownose smoothhound shark Mustelus schmitti. This paper provides a new record for the commensal porcellanid crab Polyonyx gibbesi, and information about its biology as a commensal of the polychaete worm Chaetopterus sp., from the State of Sergipe, north-eastern Brazilian coast.

MATERIALS AND METHODS

The samples were obtained on an estuarine mudflat of the Vaza-Barris River, located in the State of Sergipe in northeastern Brazil (11808′ 20.77′′ S 37809′ 19.02′′ W) (Figure 1). The collections were made during diurnal spring tides in October and November 2010. The specimens of Polyonyx gibbesi (Figure 2) were obtained by manual capture of their 1

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gustavo luis hirose

Fig. 1. Study site on the north-eastern Brazilian coast (arrow points to the sample area in the estuary of the Vaza-Barris River).

host, a U-shaped polychaete identified as belonging to the genus Chaetopterus (Amaral & Nonato, 1996). The polychaetes were placed in individual plastic bags and transported to the laboratory, where they were dissected and analysed for the presence of P. gibbesi. The 17 polychaetes collected in November were measured for the total length and maximum diameter of the tube, and the diameter of the siphon opening. Unfortunately, during the first sampling conducted in October 2010, the methodology was not yet completely defined. The ten polychaetes collected during this month were stored together after they were checked for the presence of crabs, preventing any further analyses. All the crabs were sexed and measured for carapace width (CW), using a digital caliper (accuracy 0.05 mm). Female crabs were examined for the presence of eggs. The eggs of ovigerous females were separated and counted with the aid of a stereomicroscope. To assess the population distribution of the symbiont species on their hosts, the observed frequency distribution was tested for any significant difference from random by comparing it with the Poisson distribution. A Chi-squared (x2) test of goodness of fit was used to examine differences between observed and expected (random Poisson) distributions (Sokal & Rohlf, 1995). The relationship of size (CW) between crabs occurring in pairs in the same host was evaluated by a simple linear regression.

RESULTS

Of the 27 polychaetes collected, 23 (85.18%) were inhabited by P. gibbesi. Four polychaetes contained a single individual, and 19 had two individuals (Figure 3). In all cases in which more than one crab was found in a host, they were a male and female pair. In the hosts examined, 42 crabs were found, 21 males and 21 females. Five of the females were carrying eggs (Table 1). The population distribution of P. gibbesi in the polychaetes did not display a random pattern (Chi-square of goodness of fit: x2 ¼ 5.75, df ¼ 1, P ¼ 0.016). This was explained by the large number of polychaetes found with a male and female pair, compared to the number predicted by the Poisson distribution (Figure 4). No correlation was found between the sizes (CW) of pairs of males and females inhabiting hosts (simple linear regression, P ¼ 0.18) (Figure 5). The crabs tended to prefer larger-sized hosts (length of tube) (Figure 6).

DISCUSSION

Polyonyx gibbesi was present in high frequency in its host, indicating that its occurrence was not accidental or sporadic at the study site. The presence of ovigerous females in the

Fig. 2. Dorsal view of male and female of the commensal porcellanid crab Polyonyx gibbesi.

polyonyx gibbesi from north-eastern brazilian coast

Fig. 3. Frequency of host under different presence conditions of Polyonyx gibbesi.

population indicates the existence of mature and sexually active individuals that were effectively reproducing, at least during the sampling period. In all cases in which more than one crab was found in a host, they were a male and female pair. Symbiotic crustaceans are expected to live as heterosexual pairs in or on hosts, and exhibit monogamy when their hosts are large enough to support a few (e.g. two) individuals, but not more, when the hosts are relatively rare and when predation risk away from the hosts is high (Baeza & Thiel, 2003, 2007; Thiel et al., 2003; Baeza et al., 2011; Baeza, 2008). The present observations of P. gibbesi agree in general terms with previously suggested explanations of the population distribution and mating system of symbiotic crustaceans (Baeza & Thiel, 2003; Baeza & Piantoni, 2010; Baeza et al., 2011). Species that are intimately associated with other living organisms may derive important benefits (protection and food), but may also incur substantial costs (defence and restricted mobility) from their symbiotic lifestyle (Thiel et al., 2003). These costs are primarily owing to the impossibility that most host organisms can satisfy all requirements of their symbiont, and consequently, the symbiont may have to leave its host temporarily to fulfil these needs, e.g. to obtain food or mating partners (Thiel et al., 2003). To reduce the costs of leaving the host to obtain a mating partner, many symbiont species inhabit their hosts as heterosexual pairs (Vannini, 1985). This is probably the case for P. gibbesi, as observed in this investigation and also previously by Gray (1961) and Grove & Woodin (1996).

Fig. 4. Population distribution of the porcellanid crab Polyonyx gibbesi. Observed frequency of crabs in the hosts differs significantly from expected Poisson random distribution.

Another observation of this study was the lack of association between the size of the individuals (couple) and their host. The size of the crabs was always greater than the size of the opening of the host siphon. This probably indicates that these crabs choose the host during their early stages of development and metamorphose into the adult form while resident within the host, as reported previously for other pinnotherid crabs (Grove & Woodin, 1996). This also eliminates the possibility of the crabs moving between different host individuals during the adult phase, and further suggests that male – female pairs of P. gibbesi might represent long-term (perhaps lifetime) monogamous pairs. Therefore, the wide variation in size found between individuals from the same host is probably related to different periods of colonization, growth, and/or differential mortality between sexes. Polyonyx gibbesi was found associated mainly with largersized hosts (tube length), as also reported by Grove & Woodin (1996). This is probably related to the limited space provided by the smaller-sized host individuals. Recent theoretical considerations suggest that host structural complexity and host size (relative to the species using a host) are the most important parameters modulating the cost and benefit of refuge monopolization and, therefore, the distribution of symbiotic crustaceans (Baeza & Thiel, 2003, 2007; Baeza, 2008; Baeza & Piantoni, 2010). The availability of space or food resources from individual hosts may have strong effects on the intraand inter-specific interactions among associates (Baeza et al., 2001). Thus the size of the host and its characteristics

Table 1. Descriptive statistics of demographic categories of Polyonyx gibbesi and its polychaete host. Crabs

N

CW (mean)

SD

CW (maximum)

CW (minimum)

Mean eggs + SD

Males Females Ovig. females

21 16 5

7.63 10.57 10.56

0.88 1.14 0.80

8.95 12.1 11.65

5.5 8.1 9.5

— — 1171.6 + 534.5

Host

Mean length

SD

Mean Diam

SD

Siphon

SD

N ¼ 17

53.58

9.97

2.58

0.26

0.48

0.06

CW, carapace width; Diam, maximum diameter of tube; Ovig., ovigerous; Siphon, siphon aperture; SD, standard deviation.

3

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REFERENCES Amaral A.C.Z. and Nonato F.E. (1996) Annelida Polychaeta: caracterı´sticas, glossa´rio e chaves para famı´lias e geˆneros da costa brasileira. Campinas, SP: Editora da UNICAMP, 124 pp. Baeza J.A. (2008) Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlantica, in the tropical eastern Pacific coast. Marine Biology 153, 387 –395. Baeza J.A., Bolan˜os J., Hernandez J.E., Lira C. and Lo´pes R. (2011) Monogamy does not last long in Pontonia mexicana, a symbiotic shrimp of the amber pen-shell Pinna carnea from the southeastern Caribbean Sea. Journal of Experimental Marine Biology and Ecology 407, 41–47.

Fig. 5. Relationship between the size of carapace width (CW) of males and females, when a couple cohabited on a single host.

Baeza J.A. and Piantoni C. (2010) Sexual system, sex ratio, and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex-allocation theories. Biological Bulletin. Marine Biological Laboratory, Woods Hole 219, 151–165. Baeza J.A. and Stotz W.B. (1995) Estrutura poblacional del cangrejo comensal Allopetrolisthes spinifrons (H. Milne Edwards, 1837) (Decapoda: Porcellanidae) sobre su hospedador habitual Phymactis clematis (Actiniaria) y em dos nuevos hospedadores. Revista de Biologı´a Marinha 30, 255–264. Baeza J.A., Stotz W. and Thiel M. (2001) Life history of Allopetrolisthes spinifrons, a crab associate of the sea anemone Phymactis clematis. Journal of the Marine Biological Association of the United Kingdom 81, 69–76. Baeza J.A. and Thiel M. (2003) Predicting territorial behavior in symbiotic crabs using host characteristics: a comparative study and proposal of a model. Marine Biology 142, 93–100. Baeza J.A. and Thiel M. (2007) The mating system of symbiotic crustaceans: a conceptual model based on optimality and ecological constraints. In Duffy J.E. and Thiel M. (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford: Oxford University Press, pp. 250 –267.

Fig. 6. Mean size and standard deviation of host length under different presence conditions of Polyonyx gibbesi.

(supply, resource value and defensibility) will greatly affect the life history of crustacean associates, and may act as a limiting factor. The expansion of the known distribution of P. gibbesi to the State of Sergipe may contribute to changing the current concept of anti-tropical distributions of this species and other marine invertebrates from the western Atlantic. Probably, the current state of knowledge about this species’ distribution is the result of its commensal lifestyle, which makes it difficult to collect, as well as the scarcity of investigations along the north-eastern Brazilian coast.

ACKNOWLEDGEMENTS

We thank Dr Paulo da Cunha Lana from the Universidade Federal do Parana´ for the identification of the polychaete. All the collections in Brazil were carried out according to state and federal laws (ICMBio#27111427) regarding wildlife. This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

Belleggia M., Boschi E.E., Schejter L., Bremec C., Sa´nchez F. and Figueroa D.E. (2010) First record of Polyonyx gibbesi (Anomura: Porcellanidae) in the Argentine Sea. Marine Biodiversity Records 3, 1–3. DOI: 10.1017/S1755267209991011. Gore R.H. and Abele L.G. (1976) Shallow water porcelain crabs from the Pacific coast of Panama and adjacent Caribbean waters (Crustacea: Anomura: Porcellanidae). Smithsonian Contributions to Zoology 237, 1–30. Gray I.E. (1961) Changes in abundance of the commensal crabs of Chaetopterus. Biological Bulletin. Marine Biological Laboratory, Woods Hole 120, 353–359 Grove M.W. and Woodin S.A. (1996) Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biological Bulletin. Marine Biological Laboratory, Woods Hole 190, 359–366. Haig J. (1960) The Porcellanidae (Crustacean, Anomura) of the eastern Pacific. Allan Hancock Pacific Expeditions 24, 1 –440. Rodrı´guez I.T., Herna´ndes G. and Felder D. (2005) Review of the Western Atlantic Porcellanidae (Crustacea: Decapoda: Anomura) with new records, systematic observations, and comments on biogeography. Caribbean Journal of Science 41, 544–582. Ross D.M. (1983) Symbiotic relations. In Abele L.G. (ed.) The biology of Crustacea. New York: Academic Press, pp. 163–212. Sokal R.R. and Rohlf F.J. (1995) Biometry: the principles and practice of statistics in biological research. 3rd edition. New York: W.H. Freeman and Co.

polyonyx gibbesi from north-eastern brazilian coast

Thiel M., Zander A., Valdivia N., Baeza J.A. and Rueffler C. (2003) Host fidelity of a symbiotic porcellanid crab: the importance of host characteristics. Journal of Zoology, London 261, 353–362. and Vannini M. (1985) A shrimp that speaks crab-ese. Journal of Crustacean Biology 5, 160–167.

Correspondence should be addressed to: G.L. Hirose Departamento de Biologia Universidade Federal de Sergipe Avenida Marechall Rondon s/n Bairro Rosa Elze, CEP: 49100 000 Sa˜o Cristo´va˜o, Sergipe, Brazil email: [email protected]

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