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Ostrea puelchana (D'Orbigny 1842): a new host of Tumidotheres maculatus (Say, 1818) in northern Patagonia, Argentina/Ostrea puelchana D'Orbigny 1842 nuevo hospedador de Tumidotheres maculatus (Say, 1818) en el norte de Patagonia, Argentina.

Pinnotherid crabs are a group of parasite or commensal inhabitants of bivalves, gastropods and echinoderms, plus polychets tubes (Fenucci, 1971; Williams, 1984). Frequently associated to commercial species, however, little is known about the biology of Patagonian species (Fenucci, 1971; Torres, 2006; Ocampo et al., 2007). Adverse effects have been reported on bivalve hosts of parasite crabs. Physical damage or malformations to gills, gonads and other tissues have been observed (Christensen & McDermott, 1958); interference with filtration efficiency and oxygen consumption rate have also been registered (Bierbaum & Shumway, 1988) as well as reduction on the reproductive potential and on meat production (Tablado & Lopez-Gappa, 1995; Narvarte & Saiz, 2004). Moreover, the presence of the crab implies an increase in processing time of bivalves from commercial catches (Narvarte & Saiz, 2004).

In San Matias Gulf (SMG), located northern Patagonia, Tumidotheres maculatus (= Pinnotheres maculatus, see Campos, 1989) has been reported as a commensal of mussels Mytilus platensis and naked penshells Atrina seminuda (Boschi et al., 1992; Ocampo et al., 2007). It has also been suggested as a parasite of the Tehuelche scallop Aequipecten tehuelchus (Narvarte & Saiz, 2004). Fenucci (1971) reported the occurrence of a young female crab within a native oyster Ostrea puelchana close to M. platensis fishing grounds at Mar de Plata (38[degrees]02'S, 57[degrees]30'W). It was considered as a rare case, with weak evidence to confirm a commensal association. Oysters have been studied in SMG for decades; however, there are no reports of this crab-oyster association up to now.

During a research on the ecological status of the flat native O. puelchana grounds of SMG, we recorded the presence of T. maculatus living inside the pallial cavity of the oysters. The prevalence of crabs within oysters was estimated for each oyster ground and its effect on the host was examined.

A total of 4,754 oysters were collected by diving during the fall and spring seasons of 2009 and 2010 at four natural grounds of SMG: Las Grutas, El Sotano, Caleta de los Loros and Puerto Lobos (Fig. 1). Shell height was measured with electronic digital caliper from the umbo to the growth edge. Oysters were weighed and carefully opened. Mantle cavity and tissues were examined and the presence and position of crabs were recorded. Martins & DTncao (1996) identification key was used to identify crab species. Sex was determined by differences in genital openings by macroscopic observation. Morphological features of the crabs were measured on pictures and analyzed with image free software Image-J [R]. The distance from the frontal margin to the posterior margin was defined as the carapace length (cl), while maximum carapace width (cw) was considered as the maximum distance between lateral margins. Gill and flesh condition of the infected oysters were observed on each freshly collected animal.

Occurrence of crabs was quantified as the percentage of oysters larger than 40 mm harbouring a crab. Minimum oyster size was based on minimum size of both Patagonian mussels and scallops hosts (42 mm and 51 mm respectively) (Tablado & Lopez-Gappa, 1995; Narvarte & Saiz, 2004). To evaluate the effect of crabs on their hosts, the relationship between the size and total weight of the oysters with and without crabs was analyzed using the one-way analysis of variance (ANOVA), with a logarithm transformation of the data. Homoscedasticity was tested using the Levene test. The regression lines of size vs total weight of each group were compared using an analysis of covariance (ANCOVA).

[FIGURE 1 OMITTED]

The effect of crabs on oysters was also assessed by the condition index (CI), defined as weight of soft parts/total weight. For each season at each ground one-way ANOVA was used to determine the significance of differences of CI between oysters with and without crabs. Levene test was used to test homoscedasticity. A correlation between cw of T. maculatus and height of the oysters harboring them was explored.

Pinnotherid crabs appeared only in oysters bigger than 55 mm (Table 1, Fig.2). All crabs were found alive in the pallial cavity and were identified as specimens of T. maculatus. Infected oysters hosted a single crab; no molts were found. Oysters were infested by single male (47.7%), or single female (15.1%). Crabs in poor preservation conditions and/or in immature morphological stages were unsexed and grouped as undifferentiated crabs (36.4%).

The incidence of the crab in the oysters at each of the four sites shows markedly higher numbers of pea crabs in spring samples of El Sotano (ES) and Caleta de los Loros grounds (CL) (Table 1). Probably the higher incidence is related to the big numbers in those samples.

[FIGURE 2 OMITTED]

Examination of the infected oysters showed no damage or shortness of the gills. The size-weight relationships in each group of oysters were significant (infested oysters: weight = 0.31 x size+3.07, P < 0.01; non-infested oysters: weight = 0.27 x size+3.21, P < 0.01). Homocedasticity among the regression lines was tested (P = 0.27). The size-weight relationship showed differences between groups (P = 0.014, Table 2), however the slope in both relationships showed no significant differences (P = 0.066, Table 2).

For site at each season no differences were found between variances of CI ([p.sub.CLfall] = 0.239; [p.sub.ESfall] = 0.065; [p.sub.CLspring] = 0.387; [p.sub.ESspring] = 0.766). The CI of oysters with and without crabs showed significant differences for the fall samples in CL (P < 0.01) and for the spring sample at ES (P = 0.008). However, no significant differences were found for the other samples ([p.sub.ESfall] = 0.879; [p.sub.CLspring] = 0.322).

In several studies a positive correlation between the sizes of infesting crab and its host has been observed (Christensen & McDermott, 1958; Kane & Farley, 2006) and shelter size seems to influence adult crab size. This trend appears to be more apparent among female crabs (Kane & Farley, 2006, Tablado & Lopez-Gappa, 1995) which are lifelong endosymbionts. Male are free-ranging and move among hosts. We did find a positive but low correlation for male crabs ([R.sup.2] = 0.211, P = 0.017). Small crabs were found in large oysters but the opposite was not the case.

The occurrence of T. maculatus inside O. puelchana is significant since it is a recently observed phenomenon. It has a lower incidence than those of other hosts of the area (56% in A. tehuelchus, Narvarte & Saiz, 2004; 15-74% in Atrina seminuda, Soria unpublished data; more than 80% in M. platensis, Morsan unpublished data), but it is comparable to the incidence of crabs in Zygochlamys patagonica when it was first detected in 1984 at San Jose Gulf grounds (range of prevalence: 1.19-12.2%; Gomez-Simes, 1993). Similar values (7-16%) were found for M. platensis in Necochea grounds in 1970 (Fenucci, 1971). Since actual occurrence of T. maculatus in O. puelchana reaches 16.7% on SMG grounds (Table 1), we conclude that an interspecific relationship is established between the two species. Particularly, a commensal relationship is established between crabs that feed on food filtered by flat oysters. Although no deleterious effect on gills was observed, we found differences in CI for same samples. If there is an energetic disadvantage relative to the presence of the crab as found in other species (Bierbaum & Shumway, 1988), in this species is unknown.

SMG oyster grounds have been surveyed since 1970, and no precedent of this commensal association had been reported before. Two hypotheses can explain our findings. One hypothesis arises from an ecological perspective. The presence of the crabs inside flat oysters represents evidence of a colonization process. O. puelchana larvae frequently set on A. seminuda or on M. platensis, therefore intraspecific relationships between these species take place. The overlapping of distribution areas of O. puelchana and those of traditional and highly-infected hosts in SMG may have played a key role in the onset of this process. The second hypothesis refers to fishing activities. Our findings may represent a consequence of disturbance caused by fishing to the benthic ecosystem. Due to commercial extraction of traditional hosts crabs may have started looking for new hosts. It has been demonstrated that T. maculatus can choose host (Kruczynski, 1973), therefore their distribution is not controlled by host abundance. O. puelchana rests on the sea bed with the bowl-shaped (right) valve downwards and the flat (left) valve upwards. Despite the shells slightly open for filtration, it is likely that T. maculatus enters when the aperture is exposed. The presence of pea crabs within specimens of Pododesmus sp. that occurred in our samples supports the hypothesis of the search of new hosts.

Although oysters were mainly infested by male crabs, no (definite) pattern can be recognized. Seasonality in crab occurrence has been reported for several hosts (Christensen & McDermott, 1958; Alves & Pezzuto, 1998; Narvarte & Saiz, 2004; Sun et al., 2005; Asama & Yamaoka, 2009). In SMG, seasonal variation of the incidence of crabs was reported for A. seminuda (Soria, unpublished) and for A. tehuelchus, where gravid females were observed in February and November (Narvarte & Saiz, 2004). The incidence of infestation of T. maculatus within O. puelchana along the year, i.e. if the occurrence of crabs remains at constant levels or if it has peak periods of invasions, has not been evaluated. Moreover, reproductive season of these crabs remains unknown. A careful check made throughout the year may reveal the annual recruitment pattern. On the other hand, the conditions that regulate this type of commensalism have to be elucidated. Whether crab densities, distribution of receptive crab females, food availability, salinity or other factors are controlling this intraspecific relationship remains unknown.

Additionally, T. maculatus range size (Table 1) was lower than those of A. tehuelchus (1-16 mm, Narvarte & Saiz, 2004) or of M. platensis (1.2-10 mm, Fenucci, 1971; 3.8-9.5 mm, Boschi et al., 1992). Differences in crab prevalence between grounds are also intriguing considering the spatial distribution of oyster beds. The occurrence of T. maculatus within O. puelchana may reflect an expansion of crab distribution to shallow waters. O. puelchana and A. tehuelchus with crabs are found at shallow waters (less than 25 m deep; Table 1), while previously reported hosts are distributed from 40 up to 120 m depth (Fenucci, 1971; Gomez-Simes, 1993; Tablado & Lopez-Gappa, 1995). The difference in crab size between bivalve hosts, and the absence of T. maculatus in the shallowest oyster grounds (Las Grutas) may also reflect this fact. Furthermore, as males change hosts frequently, a correlation between sizes is not expected (Tablado & Lopez-Gappa, 1995), which is consistent with our findings. Female crabs might not be entering slightly open shells of O. puelchana due to their carapace size.

In further studies, special considerations should be given to the sex-ratio and the crab-host size relationship, which might be related to host size, and to the time that the bivalve remains closed. In the future, a study will be conducted that combines ecological data with the morphological feature of the crabs inhabiting this and other bivalve species from SMG.

DOI: 10.3856/vol40-issue1-fulltext-21

ACKNOWLEDGEMENTS

We express our gratitude to Dr. Daniel Roccatagliata for helping us with the crab determination. Institutional support was given by IBMyPAS. This study was funded by PICT 2006-1674 and PICT 2007-1338 from ANPCyT.

REFERENCES

Alves, E.S. Dos & P.R. Pezzuto. 1998. Population dynamics of Pinnixa patagoniensis Rathbun, 1918 (Brachyura: Pinnotheridae) a symbiotic crab of Sergio mirim (Thalassinidea: Callianassidae) in Cassino Beach, Southern Brazil. Mar. Ecol., 19(1): 37-51.

Asama, H. & K. Yamaoka, 2009. Life history of the pea crab, Pinnotheres sinensis, in term of infestation in the bivalve mollusk, Septifer virgatus. Mar. Biodivers. Records, 2: 77.

Bierbaum, R. & S.E. Shumway. 1988. Filtration and oxygen consumption in mussels, Mytilus edulis, with and without pea crabs, Pinotheres maculatus. Estuaries, 11(4): 264-271.

Boschi, E.E., C.E. Fischbach & M.I. Iorio. 1992. Catalogo ilustrado de los crustaceos estomatopodos y decapodos marinos de Argentina. INIDEP, Mar del Plata, 94 pp.

Campos, E. 1989. Tumidotheres, a new genus for Pinnotheres margarita Smith, 1869, and Pinnotheres maculatus Say, 1818 (Brachyura: Pinnotheridae). J. Crust. Biol., 9(4): 672-679.

Christensen, A.M. & J.J. McDermott. 1958. Life-history and biology of the oyster crab, Pinnotheres ostreum Say. Biol. Bull., 114: 146-179.

Fenucci, J.L. 1971. Notas sobre las dos especies de Pinnotheres mas comunes en el litoral bonaerense (Decapoda, Brachyura, Pinnotheridae). Physis A, 30: 355-367.

Gomez-Simes, E. 1993. Pinnixa brevipollex y Pinnotheres maculatus (Crustacea: Brachyura: Pinnotheridae) en el Golfo San Jose, Chubut, Argentina. Physis A, 48: 25-28.

Kane, K. & G.S. Farley. 2006. Body size of the endosymbiotic pea crab Tumidotheres maculatus: larger hosts hold larger crabs. Gulf Caribb. Res., 18: 27-33.

Kruczynski, W.L. 1973. Distribution and abundance of Pinnotheres maculatus Say in Bogue Sound, North Carolina. Biol. Bull., 145: 482-491.

Martins, S.T.S. & F. D'Incao. 1996. Os Pinnotheridae de Santa Catarina e Rio Grande do Sul, Brasil (Decapoda, Brachyura). Rev. Bras. Zool., 13(1): 1-26.

Narvarte, M.A. & M.N. Saiz. 2004. Effects of the pinnoterid crab Tumidotheres maculatus on the Tehuelche scallop Aequipecten tehuelchus in the San Matias Gulf, Argentina. Fish. Res., 67: 207-214.

Ocampo, E., N.E. Farias, N.M. Chiaradia & M. Cledon. 2007. Occurrence of pinnotherid crabs (Decapoda: Brachyura) in mollusk populations of San Antonio Oeste, Patagonia Argentina. In: The Crustacean Society Mid-year meeting, Coquimbo, 69 pp.

Sun, W., S. Sun, W. Yuqi, Y. Baowen & S. Weibo. 2005. The prevalence of the pea crab, Pinnotheres sinensis, and ist impact on the condition of the cultured mussel, Mytilus galloprovincialis, in Jiaonan waters (Shandog Province, China). Aquaculture, 253: 57-63.

Tablado, A. & J. Lopez-Gappa. 1995. Host-parasite relationships between the mussel Mytilus edulis L., and the pea crab, Tummidotheres maculatus (Say), in the Southwestern Atlantic. J. Shellfish Res., 14(2): 417-423.

Torres, E.R. 2006. Primer registro para Argentina de Pinnixa valdiviensis Rathbun, 1907 (Decapoda, Pinnotheridae). Invest. Mar., 34(2): 175-179.

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Received: 28 July 2010; Accepted: 12 December 2012

Maria del Socorro Doldan (1), Erica M. Oehrens-Kissner (1), Enrique M. Morsan (1) Paula C. Zaidman (1) & Marina A. Kroeck (1)

(1) Instituto de Biologia Marina y Pesquera "Almirante Storni" (IBMyPAS) Guemes 1030, San Antonio Oeste (R8520CXV), Rio Negro, Argentina

Corresponding author: Maria del Socorro Doldan (msdoldan@gmail.com)
Table 1. Site name, mean depth, prevalence, and measurements.
Numbers in brackets represent oysters smaller than 40
mm. cl: carapace length, cw: carapace width.

Tabla 1. Sitios, profundidad media, prevalencia, y mediciones.
Los numeros entre parentesis representan las ostras
menores a 40 mm. cl: largo del caparazon, cw: ancho del
caparazon.

Year                   Site name       Mean        Sampled
                                     depth (m)   oysters (n)

2009 Fall sample     Caleta de los      18        159 (10)
                     Las Grutas          6        146 (43)
2009 Spring sample   Caleta de          20        293 (22)
                       los Loros
                     Las Grutas          8         60 (9)
                     El Sotano         14.7      1197 (259)
                     Puerto Lobos       15         243 (5)
2010 Fall sample     Caleta de los      15        234 (20)
                        Loros
                     Las Grutas          8        215 (33)
                     El Sotano          15         98 (7)
                     Puerto Lobos       15           242
2010 Spring sample   Caleta de los      20        1023 (78)
                       Loros
                     Las Grutas         10           60
                     El Sotano          15         58 (1)

Year                   Site name       Prevalence
                                          (%)

2009 Fall sample     Caleta de los        3.2
                     Las Grutas            0
2009 Spring sample   Caleta de            1.4
                       los Loros
                     Las Grutas            0
                     El Sotano          0 - 12.5
                     Puerto Lobos          0
2010 Fall sample     Caleta de los        1.3
                        Loros
                     Las Grutas            0
                     El Sotano            7.1
                     Puerto Lobos          0
2010 Spring sample   Caleta de los      0 - 16.7
                       Loros
                     Las Grutas            0
                     El Sotano             0

Year                   Site name      Host size (mm)         Crab
                                      Mean [+ o -] SD

                                                           c range
                                                             (mm)

2009 Fall sample     Caleta de los   79.5 [+ o -] 14.4   3.24 - 5.26
                     Las Grutas              -                -
2009 Spring sample   Caleta de       92.6 [+ o -] 5.7    4.14 - 4.37
                       los Loros
                     Las Grutas              -                -
                     El Sotano       77.1 [+ o -] 16.7   1.95 - 6.74
                     Puerto Lobos            -                -
2010 Fall sample     Caleta de los   74.8 [+ o -] 7.85   2.91 - 7.95
                        Loros
                     Las Grutas              -                -
                     El Sotano       83.6 [+ o -] 8.2     1.67 - 2.9
                     Puerto Lobos            -                -
2010 Spring sample   Caleta de los   76.7 [+ o -] 16.8   2.33 - 6.22
                       Loros
                     Las Grutas              -                -
                     El Sotano               -                -

Year                   Site name

                                       cw range
                                         (mm)

2009 Fall sample     Caleta de los    3.4 - 5.29
                     Las Grutas            -
2009 Spring sample   Caleta de        3.64 - 5.23
                       los Loros
                     Las Grutas            -
                     El Sotano        1.9 - 6.18
                     Puerto Lobos          -
2010 Fall sample     Caleta de los    2.8 - 8.71
                        Loros
                     Las Grutas            -
                     El Sotano        1.63 - 2.86
                     Puerto Lobos          -
2010 Spring sample   Caleta de los    2.2 - 6.71
                       Loros
                     Las Grutas            -
                     El Sotano             -

Table 2. Results of ANCOVA applied to the ln (size) vs
ln (weight) relationship between oysters with and
without crabs.

Tabla 2. Resultados del ANCOVA aplicado a la relacion
entre el ln (talla) vs ln (peso) entre ostras con y sin
cangrejos.

                           Source of variation

                   df     SS      MS       F       P

With vs            1     0.035   0.035   6.042   0.014
  without crabs
Error             1361   7.891   0.006
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Author:Doldan, Maria del Socorro; Oehrens-Kissner, Erica M.; Morsan, Enrique M.; Zaidman, Paula C.; Kroeck,
Publication:Latin American Journal of Aquatic Research
Date:Mar 1, 2012
Words:2852
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